Tracking The Advance Of Modernity By The Hybrid Nature Of IBD Segments – The Depletion Of Our Hybrid Heritage Revisited
The implications of short DNA segment sharing between populations in Africa, Europe and Asia are compelling. Povysil and Hochreiter (2014), Austrian researchers on the Institute of Bioinformatics in Linz, published a preprint on new results that focus on population structure, based on the genetic heritage of humans, Neandertals and Denisovans. Applying HapFABIA, a new method for the identification of very short identity by descent (IBD) segments tagged by rare SNVs (single nucleotide variants) or tagSNVs, for now just based on chromosome 1 data from the 1000 Genomes Project (Phase 1, actually consisting of 1,092 individuals: 246 Africans, 181 Admixed Americans, 286 East Asians, and 379 Europeans), 105,652 valid IBD segments were detected:
The vast majority (101,209) of the detected IBD segments (105,652) is shared by Africans (at least one African possesses the segment), of which 64,894 are exclusively found in Africans. Only 9,003 and 4,793 IBD segments are shared by Europeans and Asians, respectively. 558 IBD segments are exclusively found in Europeans and 1,452 exclusively in Asians. (Povysil et al., 2014)
Mapping these results against the Denisovan genome at 31X coverage (Meyer et al., 2012), and the Altai Neandertal genome at 52X coverage (Prüfer et al., 2014), resulted in a global division into segments that are Neanderthal-like, Denisovan-like, or “Archaic”, ie. matching both the Denisova and Neandertal genome. Intercontinental sharing of segments should thus provide some indication of origin and post-admixture gene flow between the continents.
This focus on the current distribution of purported Neanderthal, Denisovan and “Archaic” IBD segments is a valuable extension to previous previous results described in Hochreiter’s “Rare Haplotypes in the Korean Population” (2012) and “HapFABIA: Identification of very short segments of identity by descent characterized by rare variants in large sequencing data” (2013) that still may not have received due attention or assessment yet. The inflated portion of European-African shared DNA snippets in the African-European-Asian triangle already caught my attention in Expanding Hybrids And The Rise Of Our Genetic Common Denominator. It goes without saying that Asians should have more archaic DNA than Europeans, but despite the total Neanderthal contribution being apparently higher in the Asian genome, I found the accumulated European contribution as compared to the Asian contribution to be consistently higher for rare DNA segments. Due to different filtering and standards the quantitative differences were even more extreme for the 2014 preprint (8,6% European versus 4,6% Asian) than in mentioned previous publications (2012: 8,4% versus 6,1%; 2013: 11,8% versus 6,8%). Remarkably, this combines with an even more massive attestation of European-African shared segments, while Asian segments remain hardly shared by Africans. Reluctance to subsequently consider this shared European-African portion as essentially European seems to be the logical consequence of embracing Out of Africa. However, the African tendency for smaller sized IBD segments being noted in the preprint, doesn’t equally involve the shared European-African portion at all. Hochreiter et al. (2013)’s Figure 8 already revealed that the distribution curves of “Neanderthal” segment sizes don’t differ so much between Asian and European samples, as compared with on average shorter African samples. All the contrary, compared with the Asian reference the European curve in figure 29A of the preprint (2014) reveals a slight left-shift for the private Neanderthal-like IBD segments towards smaller sequences than the overall European “Neanderthal” distribution in figure 28B, suggesting the European IBD segments of the African shared part are on average distinguishably longer than typical for private African IBD segments. According to figure 23 also the overall Asian left-shift for African shared IBD segments is considerably higher than for Europe, though apparently this feature doesn’t involve the Neanderthal-like part. Actually, instead the right-shift of private Asian “Neanderthal” segments is closely linked with the Asian excess of Neanderthal DNA, apparently without this having resulted in a higher count of Asian IBD segments. Thus, the African tendency for smaller IBD segments as being noted in the preprint, seems to be separate from the shared European-African “Neanderthal” distribution! To the effect that a considerable part of African variation can actually be derived from the European distribution.
Actually, Europeans have more variation than Asians as they share more different IBD segments. Indeed, on average (Castellano et al., 2014) European heterozygosity (0.387 per thousand coding bases) is also higher than Asian heterozygosity (0.358), what is far less than African heterozygosity (0.507) and much higher than Neanderthal heterozygosity (0.128). Since ‘about 33% of the derived alleles seen in the Neandertals are shared with the present-day humans and about 19%, 24%, and 24% of the derived alleles seen in the Africans, Europeans, and Asians, respectively, are shared with the Neandertals’ (Castellano et al., 2014), it may be confirmed that Neanderthal-derived variability in Europe should be slightly higher for Europeans than Asians, and considerably higher for Africans.
After having filtered out the IBD segments being already present in the ancestral genome of humans and other primates, the preprint presents an interesting interbreeding analysis. On average more Asians share the few IBD segment, indicating less variation and genetic unity. Indeed, this may confirm East Asians as a rather recent population expansion. Or a bottleneck, if this would also suggest a previous reduction of population size involving some hypothesized similar hybrid population. At least, the East Asian element was not visible yet in Mal’ta Boy (24,000 BP), found pretty deep inside current Mongoloid territory. A late East Asian expansion may even be corroborated by the genetic results of Tianyuan if, like I already suggested in Restoring the Gap, Part 1 – The Delayed Non-African Expansions of Modernity, Tianyuan was actually less East Asian than could be expected from its location. Bottleneck rather than population expansion may possibly be evidenced in Native Americans. Some pre-bottleneck variation of the kind may have been preserved in South East Asia. Unfortunately, these regions were not yet included in the Phase 1 samples of the 1000 Genomes Project. So far I tend to consider the East Asian component in Native Americans and (Island) Southeast Asia rather part of some more recent East Asian expansion.
For reading the IBD length distribution graphs it should be considered that overlap of different distribution curves may have produced a somewhat convolute results, where the peaks that emerge may really derive from superposed distribution curves having density peaks at quite different segment lengths. Like in wave theory distribution curves may combine through superposition to create an interference pattern that feature distinct metrics, ie. the density peaks we see might be deceiving and actually derive from a combination of underpinning “hidden” density peaks. Retrieving actual distribution curves as components of the visible part may be complex and reminds me to the geophysical maps I once had to interpret as a student using deconvolution.
Remember, each distribution curve may be modeled as the statistical result of random segment length reduction into smaller segments as a function of time, and overlap between distribution curves may cause interference. Each distribution curve may decompose into its constituent elements that reflect another admixture event or regions of low recombination rate. Real-life dependencies such as geography, genetic cohesion and natural selection are likely to have influenced, or “distorted”, the statistical distribution curves.
For instance, Asians and Europeans have very similar IBD lengths distributions though both have some minor peaks at longer segments where the distribution curves deviate. Here the chromosome cross-over process may have been retained due to a combination of natural selection, sweep and possibly a higher proportion of homozygous cross-over events. One way to find out about the underpinning reasons for the resulting convolute distribution curve is find a procedure to decompose the overall curves into their constituent components by using proper deconvolution tools and proper assumptions.
The authors of the preprint did some decomposing themselves in the panels of chapter 4 “Analyses of Lengths of IBD Segments”, using a coarse geographic grid. This already yielded an interesting array of distinct distribution curves on a geographical basis that either appear independent or sharing some dependencies. Without any doubt a denser grid of regional human genome samples would help identify more constituent distribution curves, or admixture events, though probably not for each and every minor peak if these were due to uneven effects of natural selection. The best way to assess the nature of all spikes and anomalies of all the distribution curves would be to run the analyses on all human chromosomes separately, what the authors indeed intend to do. While the preprint only presents preliminary results on chromosome 1 of the 1000 Genomes Project, this will soon be completed with results from the other chromosomes for the final version.
Let’s take a closer look at the various distribution curves for IBD segment lengths of figures 23-31, on the intuitive though – as demonstrated below – precarious assumption of an inverse relation between mean segment size and age. Figure 23 shows a noticeable signal of smaller sequences in Asia for the portion of IBD segments being shared with Africa, while for Europe the signal for an African shared ancestry background is only significant for the smallest segments below 10,000 base pairs (bp). Figure 24 shows this ancestry background signal is stronger for Europe than Asia if European/Asian/African shared segments are included, implying Europe may have played some role in transmitting small segments to Asia. Instead, Figure 25 shows that on average shared Eurasian segments are longer than private European or Asian segments, implying longer segments distributed more easily eg. by the process of natural selection than smaller segments. Where did these longer segments come from, and what pattern followed the early distribution of smaller segments outside Africa?
The next figures distinguish three types of IBD segments, ie. Neanderthal-like, Denisovan-like and “Archaic”, that are neither Neanderthal or Denisovan. For each type the segment length distribution is related to its global geographical location, for either “shared” segments that occur in various continents, or for “private” segments, that occur in a single continent only. Thus, figures 26 and 27 display geographically shared and private Denisovan segments respectively; figures 28 and 29 respectively display shared and private Neanderthal-like segments; and figures 30 and 31 display respectively shared and private “Archaic” segments.
The next figures distinguish three types of IBD segments, ie. Neanderthal-like, Denisovan-like and “Archaic”, that are neither Neanderthal or Denisovan. For each type the segment length distribution is related to its global geographical location, for either “shared” segments that occur in various continents, or for “private” segments, that occur in a single continent only. Thus, figures 26 and 27 display geographically shared and private Denisovan segments respectively; figures 28 and 29 respectively display shared and private Neanderthal-like segments; and figures 30 and 31 display respectively shared and private “Archaic” segments.
The convolute state for the European length distribution of IBD segments that match the Denisovan genome (fig.26B) has a straightforward private European component (fig.27A, density peaks at 12,000 and 46,000 bp). This means much of the European Denisovan-like segments are shared by other continents. Instead, the Asian distribution of the private component (fig.27A) is only slightly more spiked (peaks at 27,000, 40,000, 54,000 bp) than the overall Asian distribution (fig.26B), betraying few non-Asian influences here. More specifically, the convoluted overall European distribution curve (fig.26B) has additional peaks at 28,000 and 37,500 bp that may both be shared Eurasian.
Figure 29A shows a convolute state for the distribution of length for private European IBD segments that match the Neanderthal genome (peaks at 15,500 and 26,500 bp), approaching only the Asian distribution (not the African!) when shared segments are included (fig.28B). Apparently, Asians have their wide distribution curve and main density peak at 26,000 bp (nearly) in common with Europe.
The wide European (Neanderthal) and Asian (Neanderthal and Denisovan) distribution curves having peaks between 26,000 – 28,000 bp have all appearance to be due to contemporaneous main admixture events that involved Neanderthal in Europe and Neanderthal-Denisova hybrids in Asia. Actually, for this range I fail to notice a Denisovan admixture event in Asia that is separate from Neanderthal admixture. At this point, Europe’s density peak at 15,500 for Neanderthal segments (figure 29A) could be due to selective LD latency at work, confined to Europe, since without such possibly selection-driven spikes the distribution patterns of both Europe and Asia would converge to a similar bell-shaped curve. This possibility would corroborate a similar age for Asian and European admixture events. However, since this private European density peak at 15,500 bp is accompanied by a left shift towards an overall private tendency of smaller IBD segments, this feature rather seems to indicate a preceding admixture event that is almost exclusively reminiscent in Europe.
“Archaic” IBD segments, that couldn’t be identified exclusively as Neanderthal nor Denisovan, show private sister peaks for Europeans (at 34,000 bp, fig.31A) and Africans (at 33,000 bp, fig.31B). This apparently reveals the shared African-European (Mediterranean?) origin of a comparatively late admixture event, without any clear Asian affiliation.
If so, “Mediterranean” archaic segments are puzzling. Iberians feature some unexpected correlations, ie. a lower Neanderthal contribution. I am not sure this could be explained by higher rates of African gene flow: AMR populations already show that AFR admixture rather causes a boost of “ancient African” IBD segments than a reduction of verifiable archaic contribution. Unless this same pattern could be isolated from the data in a forthcoming study, it could be postulated the Denisovan and Neanderthal “deficit” in the Iberian population (figures 1 and 2) was actually caused by moving segments into the Archaic category, rather than this deficit being explained by African admixture. Indeed, the latter should have implied a massive introgression of African short IBD segments not unlike the tendency observed in the Admixed American (AMR) sample.
However, the 1000 Genome Project Phase 1 only contains Sub-Saharan African samples as a reference. “Mediterranean” could have a North African affiliation instead, while possible collateral Sub-Saharan influences as attested by the archaic segments in Europe that peak at 5000 bp in Africa can’t be excluded. I wonder if higher Neanderthal contributions attested in Ötzi and some Northern African populations may indeed be due to this apparently late admixture event, and if this wouldn’t exclude Northern Africa as an early agent of modern human genes.
Another European Archaic distribution curve that peaks at 10,000 bp (fig.30A) looks wide enough to be actually a superposition of segments associated with the fully African segments that peak at 5,000 bp (fig.31B) and fully European segments that correspond with the private density peaks for “Neanderthal” segments at 15,500 bp (fig.29A) and “Denisovan” segments at 12,000 (fig.27A, possibly a superposition all by itself). We’ve already seen the slight left-shift of the European distribution curve towards lower lengths compared with the Asian curve. The resolution of these measurement is just not high enough to be conclusive, though it is interesting these European short IBD segments may be connected and reminiscent of what may have been some of the earliest admixture events outside Africa.
Finally, the lack of private “Archaic” segments of European signature near the Asian peak at 26,000 bp (fig.31A) is telling about the Asian origin of European shared “Archaic” segments having this particular distribution.
I would conclude that the private Asian “archaic” density peak at 26,000 bp (fig.31A) fits in nicely with the other distribution curves having density peaks between 26,000 – 27,000 bp (fig.27A, private Asian “Denisovan; fig.29A, private Asian and European “Neanderthal”) that indicate a wide range of contemporaneous Eurasian admixture events involving Neanderthal in Europe and Neanderthal-Denisova hybrids in Asia. Most likely the agent of this admixture were Neanderthal populations that ‘sometimes’ already inherited such hybrid genes all by themselves.
Moreover, a large tail of density peaks could be distinguished that may or may not be relevant for assessing the admixture history of modern humans. It has to be reiterated that the dataset of 1000 Genome Project Phase 1 is limited to a very course grid of East Asians, Europeans, Sub-Saharan Africans plus some mixed American populations, all of whom were so far only analyzed for IBD segments on chromosome 1. For instance, the large chunks of Denisovan DNA discovered in Oceania were not examined. This having said, the largest IBD segments may rather be an indication of long time isolation of already admixed populations, since higher levels of homozygosity imply lower rates of DNA segment size decay by cross-over.
In summary, on top of a Sub-Saharan multitude of small sized IBD segments, largely confined to the African continent, a coarse grid of admixed IBD segment subsets in different grades of size decay may be perceived, or admixture layers on a world-wide scale, that for now could be distinguished as follows:
- An early “European” layer of Neanderthal-like, Denisovan-like and “Archaic” IBD segments having a (projected) density peak at about 15,000 bp
- A “Eurasian” layer of basically Neanderthal-like IBD segments, supplemented in East Asia by Denisovan-like IBD segments, having a density peak at about 26,000-27,000 bp
- A “Mediterranean” subset of “Archaic” IBD segments having a density peak at about 34,000 bp
- A “Eurasian” layer of basically Neanderthal-like IBD segments, supplemented in East Asia by Denisovan-like IBD segments, having a density peak at about 40,000-42,000 bp
- A European (and possibly shared Asian) tail of “Denisovan” IBD segments having a density peak at about 45,000 bp
- An Asian tail of “Denisovan” IBD segments having a density peak at about 54,000 bp
- A European tail of “Neanderthal” IBD segments having a density peak at about 56,000 bp
It remains to be seen how many of these categories will persist once the dataset has been extended to include all chromosomes. Once the effects of natural selection and regions of low recombination rate are filtered out, and the subsets of restricted geographic currency tightly assigned to conservative regions where isolated populations could retain their homozygosity and larger IBD segments much longer since admixture – as possibly the case in Northern Africa (subset 3) – the true admixture story could be revealed.
Let’s first try to map these different density peaks on the current insights that concern the expansion of modernity. Purported ‘evidence for a single dispersal […] during a rapid worldwide expansion out of Africa in the Late Pleistocene’ dictated the prevailing view on modern human origins for a long time. Strange enough, most often a coastal route through south Asia was sought for the initial, single dispersal event out of Africa, nowadays dated ‘as early as ~130 ka ago‘ – while ‘in comparative craniometric studies the Levantine series and other early modern humans from Africa have consistently closer affinity to recent Australians than to other modern human populations’. Apparently, something else caused modern African population to be quite different, and other non-Australian populations as well: ‘However, recent genetic studies, as well as accumulating archaeological and paleoanthropological evidence, challenge this parsimonious model. They suggest instead a “southern route” dispersal into Asia as early as the late Middle Pleistocene, followed by a separate dispersal into northern Eurasia’ (Reyes-Centeno et al., 2014). Indeed, ‘a second dispersal through the Levant at ~50 ka and into northern Eurasia’ (Reyes-Centeno et al., 2014)!
Unfortunately, this new view of dual human expansion rather reads as an apologia in defense of the coastal South Asian dispersal hypothesis than that it supplies a clarification on the newly proposed second route through northern Eurasia. Indeed, Indian Indo-European and Dravidian samples ‘exhibit closer genetic and phenotypic affinity to the hypothetical second dispersal descendants (the Japanese, Aeta/Agta, and Central Asian populations)’, though it is remarkable such a detail apparently deterred the authors, declared Recent Out of Africa (ROA) adherents, only now from scoffing at the evidence.
I dare to suggest that as for now unpublished inside information on the 45 ka old Ust-Ishim genome – at 42X coverage, recently announced by Svante Pääbo – from northern Eurasia (near Omsk, southwestern Siberia) may have been decisive for this sudden change of heart. Indeed, if Mal’ta Boy (MA-1, a ~24 ka old non-Mongoloid Siberian whose genome was published by Raghavan et al., 2013) had already been identified as a direct descendent of Ust-Ishim, both early modern hominines may be allocated the same Central Asian affinity, and should thus be recognized as members of the same lineage being held responsible for the replacements of the Australoid elements in India – that should have been there instead according to the “classic” Out of Africa hypothesis.
Now, the present preprint of Povysil et al. (2014) may only give a hint on this first “Australoid” dispersal phase of modern humans. The 1000 Genomes Project Phase 1 they used, simply doesn’t include the South Asian nor Oceanian genomes necessary for an analysis. However, the overall private Asian distribution curves (figs.23-25) all reveal themselves “wider” than the corresponding European distribution curves, thus besides indicating higher densities of the longest IBD segments the Asian curves also demonstrate higher densities of the smallest IBD segments. The same applies for African shared. Fig.23 shows length Asian vs. Asian/African and European vs. European/African. For Asian there is a clear bias to shorter IBD segments if they are shared with Africans and here is a peak at shorter segments. For Europeans this effect is less clear, though there still is an enrichment of short segments around 5,000 bp for African sharing.
As for the second modern human dispersal phase, by now proposed to run through northern Eurasia, the Phase 1 data analysed doesn’t include the proper samples either. East Asia, nor even Japan, isn’t a proper approximation for ancestral Northern Eurasia: so much became clear from the genetic composition of Mal’ta Boy. However, Europe probably is, since this Siberian sample shared considerable drift and ancestry with western Eurasians. Apparent early modern influences in Europe may indeed be attested by eg. the “modern” remains in Kent’s Cavern (KC4), dated by Higham et al. at 44,2- 41,5 kyr cal BP., or the pre-Aurignacian remains in Italy’s Grotta del Cavallo that at Uluzzian culture level had an estimated age of 45-43 ka cal BP (Benazzi, 2012) – both being thus of an age similar to Ust-Ishim! As mentioned before, the complete DNA sequence of the latter is forthcoming, and though ‘Neandertal DNA in the femur suggest that the Ust-Ishim man lived soon after the interbreeding, which Pääbo estimated at 50,000 to 60,000 years ago’ (Gibbons, 2014) there is no mention of Denisovan admixture – what may potentially contradict an eastern identity of the “Denisovan” peak at 12,000 bp in Europe (fig.27A) – in case we should expect any related eastern origin of this kind. At least, the low segment-length distribution of the Denisovan-like IBD segments (whose density peaks at 12,000 bp) suggests an earlier incorporation in the modern gene pool than the main body of Eurasian Neanderthal-Denisovan segments whose densities peak between 26,000 – 27,000 bp. It would be most valuable if any of those “early short” European segments could eventually be recognized in the genome of Ust-Ishim!
In other words, I would identify the first category of IBD segments – having a deconvoluted density peak at about 15,000 bp for the early “European” layer comprising Neanderthal-like, Denisovan-like and “Archaic” IBD segments – as indicative for what currently passes as “the second modern human dispersal through northern Eurasia”. However, I am not sure the private European density peaks at 12,000 for “Denisovan-like” IBD segments (fig.27A) and near 10,000 for “Archaic” IBD segments (fig.31A) should indeed be of this same category. Why, if these components have a completely different distribution in Europe and Asia. The “Archaic” portion is more significant than the Denisovan portion in both Asia and Europe (fig.10, not shown here), what might reduce European “Denisovan” to actually a mere subset of the European “Archaic” category. Such a European connotation of ancient IBD segments could be due as well to a local strain of Neanderthal that possibly inherited from another, more ancestral member of the Denisovan clade, such as the ~400,000-year-old hominine of Sima de los Huesos, Spain, whose mitochondrial DNA indicated an early split (Meyer et al., 2013). It can’t be excluded any of these events included hominines that were actually less related to the Neanderthal and Denisovan reference samples.
Could Neanderthal DNA confirm such kind of ancient local variation? According to Castellano et al. (2014) ‘genetic diversity of Neandertals was lower than that of present-day humans and that the pattern of coding variation suggests that Neandertal populations were small and isolated from one another.’ However, despite the time-gap with the Altai Neanderthal, ‘[t]he fact that the three Neandertals carry longer tracts of homozygosity and differ more from one another than presentday humans within continents further suggests that Neandertals may have been subdivided in small local populations’. Apparently, a smaller long-term effective population for Neanderthal than present-day humans didn’t prevent them from diverging locally. Actually, Neanderthal heterozygosity may vary. It’s considerably higher in the west (0.143 for El Sidrón, Spain, ~49 ka old – or up to 0.163 at 20X coverage) than in the east (0.113, Altai, ~50 ka old), Vindija at ~44 ka old being intermediate (Table S12, Castellano et al., 2014). Apart from possible dating issues, El Sidrón heterozygosity is comparable to (or higher than) Denisovan heterozygosity (0.145 at a minimum age of 48–30 kyr ago – or down to 0.131 at 20X coverage), the latter being attributed both Neanderthal and Archaic admixtures: it was ‘estimated that 17% of the Denisovan DNA was from the local Neandertals. […] Four percent of the Denisovan genome comes from yet another, more ancient, human’ (Pennisi, 2013). Likewise for Europe, inherited archaic admixture of a divergent local source through a “hybrid” variety of Neanderthal is certainly a feasible possibility. Unfortunately, there is no way to predict the physical differences of such a local variety: ‘dental remains from the Sima de los Huesos of Atapuerca, for which ages between 350,000 and 600,000 years have been proposed, already carry Neanderthal-like morphological features that are not seen in the Denisova molar’ (Reich et al., 2010), while the archaic features in the Denisovan tooth specimen may rather derive from archaic introgression (Veeramah & Hammer, 2014). However, if Neanderthals were the “carrier” hominines from where those short non-Neanderthal IBD segments introgressed, then it could be postulated these segments should be found embedded within larger trunks of Neanderthal-like segments. Were they? Again, this can’t be retrieved from the data. Still, it’s crucial for understanding the admixture process and the hominines involved to find some positional correlation between the different types of IBD segments. If no correlation exists whatsoever, the null hypothesis of modern humans being the one and only agent for hybridization between hominine (sub)species can’t be rejected, and still this result may essentially contradict paleogenomic evidence of archaic hybridization that already happened before the appearance of modern humans. Especially the smaller IBD segments that inevitably float around independently within the modern human genomes would appear to evidence a tight association with the modern human lineage as an “agent” for direct, ancient admixture. That the smallest IBD segments being shared across continental populations date back to a time before humans moved out of Africa may be valid for the African distribution, though not necessarily (or much less so) for Asian and European distributions. This has been explained above: much of the smaller shared African segments clearly follow non-African distribution patterns.
IBD-segment size is not necessarily related directly to age, though the overall distribution of each admixture event – or selective sweep – could be assumed to be it is, or should be. The African diversity of small length IBD segments, however, is more difficult to correlate to a certain time-related profile. Hence, private African density peaks at 5,000 bp for Neanderthal-like, Denisovan-like and ‘Archaic’ alike have all appearance to form a modern human evolutionary “baseline” of great time depth. However, if – as suggested by current paleogenetic evidence – homozygous family groups of low effective population sizes were the norm for archaic hominines, and to a lesser extend even for pre-Neolithic modern humans, small length IBD segments could never have formed or thrived in the variety they do nowadays. Hence, one central assumption that emerge concerning the origin of IBD segment variety is hybridization between concurrent hominine lineages rather than balanced selection of concurrent polymorphisms as a result of within group diversification. This, despite of the fact that the opposite, diversification as a function of time, was always one of the cornerstones of the Recent Out of Africa paradigm. However, the latter can’t explain local accumulations of rare tagSNVs on the chromosome. It is quite unlikely such mutations arise independently on various lineages by chance, so the number of tagSNVs on each IBD segment determines its distance from the common genotype, as well as the IBD segment’s detectability. Hochreiter at Dienekes Anthropology Blog: ‘Short segments have often many tagSNVs: e.g. 3kbp segments have 50 SNVs. We found that short segments are tagged as good as long segments, therefore the false discovery rate should not increase for short segments.’
The mere size of small IBD segments marked by such an array of clearly distinguished tagSNVs suggests an already advanced stage of DNA fragmentation by the process of chromosome cross-over throughout generations. Moreover, it suggests heterozygous interaction with DNA of a lineage that essentially lack those tagSNVs, thus in the initial stage of having an appreciable genetic distance. Still, there must be a limit in breaking up segments by cross-over before the IBD simply disappear below detection level. Also, in the same process of fragmentation small pieces of the segment might be chopped off that only contain a few tagSNV markers that thus lost its tight association with the rest of the segment. Probably this will never occur for coding base pairs, though in all other cases this process may be inevitable and found to continuously reduce the IBD segment size, or eventually even to drain the number of detectable IBD segments in store. What happens next, would these chipped off fragments that lost genetic linkage, and residuals of disintegrated segments, including tagSNVs gone astray, simply disappear in a sink hole, or instead be randomly incorporated into common segment variability? Most probably, such fragmented, unrecognizable chomps of “grinded” DNA just recombine with an alternative segment, typically the most common one. Like already asserted in my previous blog articles, this would render a big deal of eg. Neanderthal derived introgressed DNA unaccounted for by the present detection methods that all depart only from much larger units, ie. candidate introgressed sequences.
On the long term this ongoing process of fragmenting the originally quite homozygous strains of introgressed archaic DNA by cross-over thus should have had a dual effect: the reduction of introgressed segments to lower density peak values, having few fixed differences compared to the archaic reference genome; and the integration of fragmented introgressed DNA, chipped off below sequence detection level, into the main body of genome variety. Indeed, whatever their own explanation, Vernot & Akey (2014) detected 6.1X more fixed differences (FD) for the sequences they labeled as “non-introgressed” (17.3 vs. 2.8 FD/Mb) in comparison with the fixed differences between modern humans and Neanderthal for introgressed sequences. This value was claimed as uniform, while larger non-introgressed sequences having more fixed differences were considered significantly depleted of introgressed (Neanderthal) sequences. The latter could thus be instead rather the end result of an advanced state of disintegration of the introgressed sequences, and the subsequent full integration by recombination of smaller introgressed base pairs units into common genome variability.
More radical long term results might be expected with hybrid recombination of coding DNA, either increasing the effects of purifying selection against hybrid heterozygosity, or positive selection of mutated genes that possibly incorporated a recombined mixture of ancestral and derived alleles – to the effect this DNA lost its recoverable archaic correlation. Recombination shuffles the allele content between homologous chromosomes, but needs a certain degree of heterozygosity for producing new combinations of DNA. Since these processes thus are the very result of the disintegration of introgressed DNA, Sankararaman’s (2014) ‘unexpected finding’ that ‘regions with reduced Neanderthal ancestry are enriched in genes’ doesn’t necessarily imply ‘selection to remove genetic material derived from Neanderthals.’. His observation that ‘functionally important elements’ (low B) are ‘significantly correlated to low Neanderthal ancestry’ explicitly relates to the availability of low variability chunks of Neanderthal DNA exempt of any type of recombined code. Indeed, if hybrid recombination spawned new coding variants, successful or deleterious, reduction of introgressed DNA that remained in its original state, ie. without recombination, should be expected.
In conclusion, there is no reason to consider the smallest IBD segments as anything else but preserved hybrid heterozygosity, not unlike the longer segments. Rather than attesting ancient interaction that involves a modern human host population, already rife of the currently known common segments, recombination set the stage for genetic change. Increased heterozygosity by intense hybridization in between a larger quantity of ancient hominine lineages should have accelerated IBD segment size reduction, segment disintegration and recombination. Extensive African hybridization may even have preceded a possible African or non-African backflow of the known common segments that persist in modern human DNA, thus increasing variability even more by continued recombination.
The authors were right to drop earlier attempts to date the admixtures based on the length of IBD segments. Basic assumptions on neutral inheritance and genetic offset with regard to mean recombination patterns between recognizable ancestors without gene flow, can’t be met. Relative dating is equally challenging, now heterozygosity itself determines the speed of disintegration of introgressed sequences. Hybridization and hence increased heterozygosity, may be postulated as symptomatic for a certain level of modernity, though the few available ancient genomes already attest increased heterozygosity for Denisovans and some Neanderthal before the arrival of modernity, while their cultural level can’t be distinguished as inferior compared to contemporary modern humans. Could the mere profusion of hominine lineages in Africa have been the trigger for hybridization to start off, ie. early enough to explain their disproportional availability of the smallest IBD segments? For the various distribution curves, including the smallest IBD segments, to have any dating value at all, it would be most relevant to investigate geographic clines in more detail and to exclude the effects of natural selection. I reckon the distinction between statistic models and the quirks of natural selection will become clear once, as announced in the preprint, data from the other chromosomes will be included in the analysis – and hopefully at a denser grid of genome samples. Once private IBD segments on geographically shared distribution curves may be identified thus to reveal the geographic ranges of the ancestral hominines involved, this will be very helpful in recognizing the migrational patterns of the admixed populations that we all are.
Updated 1st of May, 2014: Map of sequenced hominines added and a reference to the article of Ann Gibbons on the announced genome of Ust-Ishim.
- About the 1000 Genomes Project
- Benazzi – The first modern Europeans, 2012, link
- Castellano et al. – Patterns of coding variation in the complete exomes of three Neandertals, link
- Dienekes – Sepp Hochreiter on IBD sharing between modern humans, Denisovans and Neandertals, Blog April 14, 2014, link
- Gibbons – Oldest Homo sapiens Genome Pinpoints Neandertal Input, 2014, link
- Higham et al. – The earliest evidence for anatomically modern humans in northwestern Europe, 2011, link
- Hochreiter et al. – Rare Haplotypes in the Korean Population, at ASHG 2012, link
- Hochreiter et al. – HapFABIA: Identification of very short segments of identity by descent characterized
by rare variants in large sequencing data, 2013, link
- Meyer – A High-Coverage Genome Sequence from an Archaic Denisovan Individual, 2012, link
- Meyer et al. – A mitochondrial genome sequence of a hominin from Sima de los Huesos, 2013, link
- Pennisi – More Genomes From Denisova Cave Show Mixing of Early Human Groups, 2013, link
- Povysil et al. – Sharing of Very Short IBD Segments between Humans, Neandertals, and Denisovans, 2014, link
- Prüfer et al. – The complete genome sequence of a Neanderthal from the Altai Mountains, 2013, link
- Raghavan et al. – Upper Palaeolithic Siberian Genome Reveals Dual Ancestry of Native Americans, 2013, link
- Reich et al. – Genetic history of an archaic hominin group from Denisova Cave in Siberia, 2010, link
- Reyes-Centeno et al. – Genomic and cranial phenotype data support multiple modern human dispersals from Africa and a southern route into Asia, 2014, link
- Sánchez-Quinto et al. – North African Populations Carry the Signature of Admixture with Neandertals, 2012, link
- Sankararaman – The genomic landscape of Neanderthal ancestry in present-day humans, 2014, link
- Veeramah & Hammer – The impact of whole-genome sequencing on the reconstruction of human population history, 2014, link
- Vernot & Akey – Resurrecting Surviving Neandertal Lineages from Modern Human Genomes, 2014, link
Two competing papers that recently explored the possible genetic effects of Neanderthal-related hybridization, caught my attention. Loss of genetic integrity caused by a hybridization event may lead to rapid genetic changes within a species, what may have been an important agent for the rapid morphological changes associated with the advent of modern humans. However, true hybridization between species, or hybrid speciation, is a punctuated event often characterized by chromosome rearrangements. Both studies intend to describe hybrid-related gene-loss as an ongoing process. Instead, McVicker et al. (2009), referred to in both studies, declared ongoing ‘selection to remove less-fit functional variant from a population’ to the effect of varying sequence differences across the genome between species, not necessarily the result of hybridization.
Anatomically modern humans overlapped and mated with Neandertals such that non-African humans inherit ~1-3% of their genomes from Neandertal ancestors. We identified Neandertal lineages that persist in the DNA of modern humans, in whole-genome sequences from 379 European and 286 East Asian individuals, recovering over 15 Gb of introgressed sequence that spans ~20% of the Neandertal genome (FDR = 5%). Analyses of surviving archaic lineages suggests that there were fitness costs to hybridization, admixture occurred both before and subsequent to divergence of non-African modern humans, and Neandertals were a source of adaptive variation for loci involved in skin phenotypes. Our results provide a new avenue for paleogenomics studies, allowing substantial amounts of population-level DNA sequence information to be obtained from extinct groups even in the absence of fossilized remains.
Genomic studies have shown that Neanderthals interbred with modern humans,and that non-Africans today are the products of this mixture. The antiquity of Neanderthal gene flow into modern humans means that genomic regions that derive from Neanderthals in any one human today are usually less than a hundred kilobases in size. However, Neanderthal haplotypes are also distinctive enough that several studies have been able to detect Neanderthal ancestry at specific loci. We systematically infer Neanderthal haplotypes in the genomes of 1,004 present-day humans. Regions that harbour a high frequency of Neanderthal alleles are enriched for genes affecting keratin filaments, suggesting that Neanderthal alleles may have helped modern humans to adapt to non-African environments. We identify multiple Neanderthal-derived alleles that confer risk for disease, suggesting that Neanderthal alleles continue to shape human biology. An unexpected finding is that regions with reduced Neanderthal ancestry are enriched in genes, implying selection to remove genetic material derived from Neanderthals. Genes that are more highly expressed in testes than in any other tissue are especially reduced in Neanderthal ancestry, and there is an approximately fivefold reduction of Neanderthal ancestry on the X chromosome, which is known from studies of diverse species to be especially dense in male hybrid sterility genes. These results suggest that part of the explanation for genomic regions of reduced Neanderthal ancestry is Neanderthal alleles that caused decreased fertility in males when moved to a modern human genetic background.
In both studies, the identification of introgressed sequences is not exactly done by counting Neandertal-specific mutations. Instead, only a pre-selected set of candidate introgressed sequences, using patterns of variation in contemporary human populations by a method of Plagnol & Wall (2006), is compared to the Neanderthal reference genome. Logically, this involves predominantly ‘adaptive’ sequences, where strong selective forces are at work. Other studies (Hochreiter, Hawks) already attested a completely different picture when departing from Neanderthal-specific mutations eg. to characterize candidate haplotypes, even revealing up to 40% more Neanderthal specific haplotypes in Europe compared to Asia (explained in Rokus Blog: Expanding Hybrids And The Rise Of Our Genetic Common Denominator).
Vernot & Akey’s study compared the fixed differences between modern humans and Neanderthal for introgressed versus non-introgressed sequences, and arrived at 6.1X more fixed differences (FD) for non-introgressed sequences (17.3 vs. 2.8 FD/Mb). This value was claimed as uniform, while larger non-introgressed sequences having more fixed differences were considered significantly depleted of Neanderthal introgression.
Sankararaman (2014): ‘An unexpected finding is that regions with reduced Neanderthal ancestry are enriched in genes, implying selection to remove genetic material derived from Neanderthals.’. Moreover, there is ‘evidence for widespread negative selection against Neanderthal ancestry’ to the result that sequences having a higher density of ‘functionally important elements’ (low B) are ‘significantly correlated to low Neanderthal ancestry’. Since 20% of the genome where B is highest have about 1.54 x higher Neanderthal-like sequences, it could be deduced the portion of Neanderthal sequences on the modern human genome before the onset of this replacement process was ~3% against only ~2% nowadays. However, this does not explain the much higher estimate for Ötzi (5.5%), just a few thousand years ago.
This replacement process hit the X-chromosome harder than elsewhere on the genome, in the current papers dealing with this subject explained as a side-effect of hybridization. However, Vicoso (2006):‘Under some conditions, the X chromosome is expected to accumulate beneficial mutations at a faster rate than the autosomes’. This accumulation process effectively involves the replacement of proven, stable genes by non-deleterious mutated genes by positive selection. Wouldn’t this open the alternative possibility that replacement of conservative (defined ‘Neanderthal’) sequences by ones having a higher count of fixed differences, is just a normal evolutionary process? Instead, negative selection tends to keep the average number of fixed mutations of otherwise stable ‘original’ sequences low – at least until its successful replacement.
The gene content of X chromosomes is generally considered very stable, so large scale replacements should indicate important evolutionary shifts. The X chromosome is thought to preferentially accumulate genes with sex-biased fitness effects, and actually there isn’t any reason not to believe sex-biased fitness was quite important in post-Neanderthal populations. Moreover, nobody would deny the evolutionary shift was high since Neanderthal, and actually only accelerated since the Neolithic revolution.
Wouldn’t it be much more productive to find out where the successful sequences of higher fixed mutation counts are still coming from, and what ongoing genetic process might produce new sequences? The genetic laboratory for evolutionary change is still barely understood. Actually, variable haplotypes are most likely to originate in the copynumbers of duplicate sequences, where mutations are allowed without restriction or deleterious consequence. There is no way to tell apart breakaway mutated duplicates from a modern human genetic heritage whose unity and design we may only presume. Most of all, the Neanderthal genome may have offered a mechanism all of its own to engineer modern genetic replacements:
A comparison to any single present-day human genome reveals that 89% of the detected duplications are shared with Neandertals
We identified only three putative Neandertal-specific duplications with no evidence of duplication among humans or any other primate […] and none contained known genes. (Green et al., 2010)
I suggest the observed process of genetic replacement should first be verified with the Neanderthal duplicated potential before an ongoing removal of Neanderthal derived sequences in modern humans may be taken for granted.
- Green et al. – A Draft Sequence of the Neandertal Genome, 2010, link
- Hawks – Which population in the 1000 Genomes Project samples has the most Neandertal similarity?, Blog February 08, 2012, link
- Hawks – Neandertal ancestry “Iced”, Blog August 15, 2012, link
- McVicker et al. – Widespread Genomic Signatures of Natural Selection in Hominid Evolution, 2009, link
- Plagnol & Wall -Possible ancestral structure in human populations, 2006, link
- Sankararaman – The genomic landscape of Neanderthal ancestry in present-day humans, 2014, link
- Vernot & Akey – Resurrecting Surviving Neandertal Lineages from Modern Human Genomes, 2014, link
- Vicoso & Charlesworth – Evolution on the X chromosome: unusual patterns and processes, 2006, link
Earlier this year a new study identified a fossil canid, excavated from Razboinichya Cave in the Siberian Altai Mountains, as a member of the dog lineage. Indeed, mtDNA of this Pleistocene specimen of the ‘Mammoth steppe fauna’ resulted most similar to that of most modern dogs.
The origin of domestic dogs remains controversial, with genetic data indicating a separation between modern dogs and wolves in the Late Pleistocene. However, only a few dog-like fossils are found prior to the Last Glacial Maximum, and it is widely accepted that the dog domestication predates the beginning of agriculture about 10,000 years ago. In order to evaluate the genetic relationship of one of the oldest dogs, we have isolated ancient DNA from the recently described putative 33,000-year old Pleistocene dog from Altai and analyzed 413 nucleotides of the mitochondrial control region. Our analyses reveal that the unique haplotype of the Altai dog is more closely related to modern dogs and prehistoric New World canids than it is to contemporary wolves. Further genetic analyses of ancient canids may reveal a more exact date and center of domestication.
These results bolster previous ideas of an early appearance of domesticated dogs, though how they relate with their wolf kin remains shrouded in mystery. The resolution considerably exceeds previous results on Belgic samples thousands of miles away, where just 57 base pairs could be extracted from the mitochondrial control region of six large Pleistocene canids from Goyet cave (samples G1-6), and one from Trou des Nutons (sample TN-1), what unfortunately didn’t allow the reconstruction of much phylogenetic structure. The new results confirm the latter as a feature of Pleistocene dogs rather than a defect in previous results:
When investigating the phylogenetic informativeness of our dataset combining the Altai specimen, 72 extant dogs and 30 wolves, 35 prehistoric New World canids and four coyotes we also found low support for either a clearly resolved branching pattern or star-shaped evolution (Druzhkova et al., 2013)
Apparently dog evolution has an extremely long trajectory, and became even more complicated by the strong impact of much later, Holocene events. Their early divergence is also suggested by outstanding differences in morphology that distinguish dogs from wolves in their shortened muzzles, broader palates, crowded teeth and the broad, heavy frontal shields at the top of their skulls. The oldest (unsampled) Goyet dog, at 36,000 cal BP even older than the Altai specimen, was ‘not intermediate in form between the fossil wolves and the prehistoric dogs, but conforms to the configuration of the other Palaeolithic dogs, which are approximately 18,000 years younger’ (Germonpré et al., 2009). However, despite Goyet also supplied a representative morphological reference, Druzhkova’s team didn’t try to establish a link with this Belgium phenomenon of early dog occurrences. Even worse, the authors utterly ignored new insights that rather urge for a revision of the canid phylogenetic tree in the vein of Pilot et al. (2010). The traditional concept of a nested dog-clade, essential to the identification of Canis lupus familiaris (the domestic dog), and their putative geographical origin, already turned out incompatible with the results of Goyet. New inconsistencies may confirm the phylogenetic tree employed by Druzhkova’s team was already obsolete.
The view that dogs are the tamed descendants of the common wolf has always been the most popular one, though the scrutiny of investigators yielded ambiguous evidence. Prolific contacts between wolves and early modern humans rather tend to obfuscate early progress in the process of dog domestication:
The Palaeolithic sites yielding putative dog remains might be best described as extended-use camps or hunting sites and some of these are associated with dwellings made from mammoth bone (e.g., Germonpré et al., 2008, 489). Unambiguously identified wolf remains occur routinely in many of these sites, often at relatively high frequencies for a large carnivore. (Crockford & Kuzmin, 2012)
Incidental dog-like canids could already be distinguished in Upper Palaeolithic sites, without being sure these individual creatures could indeed be derived of tamed dogs in the periphery of human habitation rather than being the representatives of an extinct lineage of wolves. Interaction with Neanderthal may remain the only evidence that truly suits the popular preposition of the tamed wolf pur sang:
Trou de la Naulette is a famous Neanderthal site excavated by Dupont in the 1860s […]. According to the notes of Dupont, the fossil canid skull was found in the Second Horizon, the same containing the Neanderthal remains.
The Trou de la Naulette […] skulls have missing values and cannot be identified. (Germonpré et al., 2009)
Only the first appearance of dog-like features in fossils offered the opportunity to prove the acceptance of wolves as pets. For over a century Pleistocene fossils with a dog-like anatomy have been found littered over a wider area in northern Eurasia, and despite an incidental association with prehistoric human presence some reasonable doubts remain about the progress of their domestication. Dogs have traditionally been regarded the tamed version of Eurasian wolves, with the implicit assumption their differences could be fully explained by human interference and a domestic lifestyle. Earlier publications even went a lot further. Wayne et al. (1999) asserted on the basis of mtDNA that ’dogs and gray wolves may have diverged […] about 135,000 years before present’, adding that dogs ‘may have been domesticated earlier and have only recently changed in conformation with changing conditions associated with the shift from hunter-gather cultures to more agrarian societies about 12,000 years ago’. Genetic variety of dogs even exceeds the variety of the Holarctic wolf. Far from being their obvious “ancestral” counterparts, genetically speaking wolves falls within the range of genetic variety of dogs while on the basis of descend rather the opposite should be expected:
Greater mtDNA differences appeared within the single breeds of Doberman pinscher of poodle than between dogs and wolves. Eighteen breeds, which included dachshunds, dingoes and Great Danes, shared a common dog haplotype. Alaskan malamutes, Siberian huskies and Eskimo dogs also showed up in the common dog haplotype and were no closer to wolves than poodles and bulldogs. These data make wolves resemble another breed of dog. (Serpell, 1995, p.33)
Indeed, dogs are clearly the most diverse domestic species, both genetically and by morphology. Hence, Pleistocene dog domestication was traditionally considered a quite intuitive concept. Modern investigation tend to confirm the unique genetic identity of dogs in relation with wolves:
We identified 3,786,655 putative single nucleotide polymorphisms (SNPs) in the combined dog and wolf data, 1,770,909 (46.8%) of which were only segregating in the dog pools, whereas 140,818 (3.7%) were private to wolves (Axelsson et al., 2013)
However, the pendulum of scientific ‘consensus’ already tended to swing away from Pleistocene domestication in favor of still ill-understood Neolithic events when Druzhkova’s team caused considerable confusion with their published results on the Altai specimen, the second oldest Pleistocene dog. It is funny to watch great names on the scientific scene stumble in their enthusiasm, utterly unable to digest the full spectrum of conflicting information and grasp the consequences. Probably to many this new results were all too much in too short a time. Indeed, the Pleistocene Altai dog emerged genetically closer to modern dogs than to contemporary wolves, but there is more. The specimen also attested closely related with prehistoric New World canids, including both pre-Columbian domestic dogs and extinct eastern Beringian wolves, the latter being no less revolutionary for our understanding of dog evolution.
One glance at Druzhkova’s Consensus Neighbor Joining Tree makes clear the mentioned New World canids don’t simply refer to the pre-Columbian dogs that Native Americans brought with them when their ancestors left Asia. This study also incorporates the extensive mtDNA database of extinct eastern Beringian wolves published by Leonard at al. (2007). In 2002, Savolainen et al. published the discovery of three wolf mtDNA haplotypes found in wolves of China and Mongolia that cluster within the main dog haplogroup or clade A (‘A total of 71.3% of dogs had haplotypes belonging to clade A’), but now also this older group of ice age wolves has its mtDNA nesting within this main dog clade. This haplotype can’t be found in current American wolves, and apparently has an age and origin that overrule any special and tight association with east Asian wolves and dogs. Moreover, the eastern Beringian wolf diverged in many ways from current Holarctic wolves, while other features were more dog-like. The sub-species was specialized to consume more carrion and differed significantly in shape from ‘both the sample of modern North American wolves and Rancho La Brea (California) Pleistocene wolves’ (Leonard et al., 2007). Contrary to their contemporary southern neighbors and modern wolves, ‘[e]astern Beringian wolves tend to have short broad palates, probably adapted for producing relatively large bite forces suggesting the killing of bulky prey, such as bison and horse’ (Leonard et al., 2007). Apparently holarctic wolf subspecies were once distinguished along ecological lines that ceased to exist:
Notably, the Pleistocene C. lupus from eastern Beringia by the skull shape, tooth wear, and isotopic data is also reconstructed as specialized hunter and scavenger of extinct North American megafauna (Leonard et al., 2007). In addition, East-Beringian wolves genetically differ from any modern Northern American wolf, and instead they appear most closely related to Late Pleistocene wolves of Eurasia. This uniquely adapted and genetically distinct wolf ecomorph suffered extinction in the late Pleistocene, along with other megafauna.(Baryshnikov et al., 2009)
For sure the origin of the modern ‘Holarctic’ grey wolves lays in more southern latitudes, without much certainty if the wolf that ultimately replaced the variety of more northern ‘ice age’ latitudes was already part of a single wolf population that encompassed the southern glacial borderlands and refuges of Eurasia and North America, or that they expanded from any place in particular. Most likely the cradle of modern wolf evolution was somewhere south of the glacial habitat. Ancient strains of the grey wolf are nowadays recognized in the Egyptian jackal, otherwise often considered transitional to the golden jackal, that reveal mtDNA divergence with grey wolves up to about 800 kya. The Indian subcontinent still includes three diverse, distinct wolf lineages — Indian wolf, Tibetan wolf and Eurasian wolf. Mitochondrial DNA analysis suggests the Himalayan wolf is distinct from the Tibetan wolf, and represents the most divergent wolf lineage. Such genetic diversity is generally considered indicative of origin. We need to be cautious, though, since we don’t know the hybridization record of South Asian wolves, that shared their habitat for thousands of years with other canids. The recent detection of gray wolf mtDNA in the golden jackal of Senegal even ‘brings the delineation between the African wolf [Canis lupus lupaster] and the golden jackal [Canis aureus] into question’ (Gaubert et al., 2012). But even the Golden Jackal is genetically closer related than the coyote (Rueness et al., 2011, based on 726 bp of the Cyt b gene: a region of mitochondrial DNA commonly considered useful to determine phylogenetic relationships between organisms and within families and genera due to its sequence variability), hence its western distribution could eventually imply a southwestern Eurasian origin of the wolf. This location of origin may be further elaborated and even extended to the Holarctic wolf by the phylogenetic investigation of Pilot’s team (2010). Their results distinguished a single major subdivision of Holarctic wolves based on 230 bp mtDNA control region sequences of 947 contemporary European wolves that – contrary to Indian and Himalayan wolves – also applies to the worldwide wolf population:
Based on the phylogenetic trees and networks constructed, we defined two haplogroups, 1 and 2
The two haplogroups were separated by five mutational steps: three transitions, one transversion, and one insertion/deletion.
In all the trees and networks constructed, haplotypes from the two groups were clearly separated, although they did not always constitute two monophyletic clades
Haplotypes of Indian and Himalayan wolves were separated from all the other haplotypes by more than 6 mutational steps
In ancient European wolves, haplogroup 2 was predominant. All ancient samples from Belgium, Germany, Czech Republic, Hungary, and Ukraine, ranging in age from 44,000 to 1,400 years B.P., belonged to this haplogroup. Only one haplotype of ancient wolf (w7), sampled in western Russia and dated from 2,700 – 1,200 years ago, belonged to haplogroup 1
Our results are consistent with Germonpré et al. , who showed that the ancient European haplotypes are placed in one part of the wolf haplotype network rather than being scattered across the complete network.
[…] contemporary data may suggest substantial changes in haplogroup frequencies over the last 40,000 years from the predominance of haplogroup 2 to the predominance of haplogroup 1.
[…] mtDNA haplotypes of Pleistocene wolves from eastern Beringia belonged to a distinct haplogroup that does not occur in contemporary North American wolves. This haplogroup corresponds to haplogroup 2 in our study […] and some of the ancient European and Beringian wolves even shared a common haplotype (Pilot et al., 2010)
The ambiguous assignment of only one haplotype (w20, from Turkish Trakia) and the intermediate position of Balkan wolves in general (figure 1 in Pilot et al., 2010) is in agreement with the aforementioned southwest Eurasian origin of Holarctic wolves, and even more specific to the origin of modern wolves whose mtDNA cluster in haplogroup 1. Instead, dogs cluster to ancient European wolves and their relatives in the Pleistocene arctic region, whose mtDNA cluster in haplogroup 2. The ancient predominance of dog-like mitochondrial DNA in wolves thus can’t be exclusively associated with some ‘Beringian-like’ tendencies in the Pleistocene Eurasian wolf phenotype, that otherwise has all appearance to be intrusive from the east. This counter-intuitive geographic separation of ancestral Holarctic wolves in the west, nearby old centers of human occupation, and dog-like haplotypes far away from any human interference at all, isn’t necessarily irreconcilable to dog domestication. Actually, wild animals that had the opportunity to co-evolve with humans never experienced the same magnitude of extinction that happened e.g. in the Americas: ‘It has long been thought that extinctions in Africa were less severe than in other regions of the world due to the long term coevolution of humans and megafauna’ (Louys et al., 2006). In general, such animal populations being situated closer to the known centers of human evolution turned out less prone to domestication as well. Coevolution apparently involved wild animals getting wilder and less prone to domestication. Animals that remained curious and less cautious for humans met their end during and after the great megafaunal extinctions. The Beringian wolf phenotype may have belonged to the latter category, and became extinct. However, before this happened some individuals were attested to have already mixed with western wolf populations. Probably it was no coincidence this phenotype emerged as the prime target of human interaction and, eventually, domestication.
The nature of Holocene extinction, that started at the end of the last Ice Age, is contested, though generally considered due to both climate change and the proliferation of modern humans. The impact of this phenomenon was not limited to the extinction of numerous species. Hofreiter (2010) stressed that ‘studies like that by Pilot et al. are starting to reveal that at least some surviving species are also depleted in genetic diversity compared with their Pleistocene ancestors.’ Somehow the dogs were exempted from this depletion, for they still are ‘a genetically diverse species that likely originated from a large founding stock possibly derived from wolf populations existing in different places and at different times’ (Vilà et al., 1999) – even though most of these ancestral wolf populations are now extinct, and replaced by new wolf populations that are not representative to the founding stock. The effect of this Late Pleistocene change of grey wolf populations was huge. Meachen’s team (2012) ‘suggest that Pleistocene coyotes may have been larger and more robust in response to larger competitors and a larger-bodied prey base’, being consistent with the view that even the early American grey wolves in the tar pits could thrive in their niche only after this post-megafaunal development of the coyote evolving away from wolf-like forms. Leonard et al. (2007) relied ‘on an early arrival of the more gracile wolf from the Old World and migration to areas below the Wisconsin ice sheet’ to explain the presence of two distinct Pleistocene gray wolves in North America, though actually the southern type is rare or problematic before 10,000 BP while eastern Beringian wolves attest too many infinite dates and genetic diversity to have simply evolved locally and derive from this hypothesized population of immigrant American common ancestors. Instead, sudden grey wolf competition may have supplied an additional reason for the sudden post-Glacial downsizing of the coyote, while also current hybridization patterns in North America tend to confirm the modern grey wolf’s more recent introduction from Eurasia:
[…] extensive admixture zones in North America, where four morphologically distinguishable wolf-like canids can potentially interbreed: the gray wolf of Old World derivation, the coyote and red wolf (both of which originated in North America), and the Great Lakes wolf. (VonHoldt et al., 2011)
Meanwhile, the genetic tie of eastern-Beringian wolves with Eurasian gray wolves – and early dogs! – discourages premature conclusions on dog domestication in the Americas, not in the least because this tie considerably precedes the attested Native American immigration ~15,000 years BP. More likely, eastern Beringian wolves managed to preserve their dog-like genetic legacy longer than elsewhere on the northern hemisphere, until worldwide disaster struck the ice age megafauna:
the eastern-Beringian ecomorph was hypercarnivorous with a craniodental morphology more capable of capturing, dismembering, and consuming the bones of very large mega-herbivores, such as bison. When their prey disappeared, this wolf ecomorph did as well, resulting in a significant loss of phenotypic and genetic diversity within the species. Conceivably, the robust ecomorph also was present in western Beringia in the Late Pleistocene, but specimens were not available for this study. (Leonard et al., 2007)
The ecological and derived morphological segregation of Pleistocene wolves in a northern ice age subspecies and the subspecies of southern ice age refuges appears to have had a genetic component that survives in dogs and wolves respectively:
According to Hofreiter , this may imply that Pleistocene wolves across Northern Eurasia and America may have represented a continuous and almost panmictic population that was genetically and probably also ecologically distinct from the wolves living in that area today. (Pilot et al., 2010)
The southern subspecies may have comprised several isolated gray wolf populations in Eurasian and American ice age refuges, not all of which necessarily survived the global wave of post-glacial loss of diversity, or extinction. Indeed, ‘[…] most of the genetic diversity of megafaunal animals may have been lost at the end of the Pleistocene, even in surviving species’ (Hofreiter 2007). Some of the general post-glacial loss of diversity may be due to more recent expansions and replacements, and since most of the sampled eastern Beringian wolves attest ‘infinite dates’ (Leonard et al., 2007 sup.) it is likely their stock was already present in the region for a longer time. However, at least the northern subspecies is strongly indicated to have been a single Pleistocene population that was also genetically distinct:
[Leonard et al., 2007] found evidence that the Beringian wolves were morphologically different from modern North American wolves and from Pleistocene wolves from more southern regions. Moreover, the differences in morphology suggest that the Pleistocene Beringian wolves were adapted to hunting and scavenging members of the now extinct megafauna, a conclusion supported by isotope analysis. Finally, these wolves not only represented a different ecomorph, they were also genetically distinct. Not a single sequence of their mitochondrial DNA haplotypes exactly matched sequences found in modern and historical wolves identified to date. However, some of the sequences perfectly matched, albeit only for short stretches, sequences obtained from Eurasian Pleistocene wolves, from as far west as the Czech Republic. Thus, Pleistocene wolves across Northern Eurasia and America may actually have represented a continuous and almost panmictic population that was genetically and probably also ecologically distinct from the wolves living in this area today. Despite their high mobility, these wolves did not escape the megafaunal extinctions at the end of the Pleistocene, even though the causes of their extinction are unclear. The specialized Pleistocene wolves, thus, did not contribute to the genetic diversity of modern wolves. Rather, modern wolf populations across the Holarctic are likely be the descendants of wolves from populations that came from more southern refuges as suggested previously for the North American wolves (Hofreiter, 2007)
Germonpré (2009) noted similar trends like Beringian wolves in skulls from Trou Baileux, Trou des Nutons, Mezin 5469, Mezin 5488 and Yakutia, that all are considered to be from fossil wolves. Leonard et al. (2007) analyzed the eastern Beringian wolves genetically and attributed the disappearance of this robust prehistoric ecomorph to ecological changes that occurred after the Last Glacial Maximum. Even though her team also based themselves on a database of pre-Columbian dogs when they rejected domestication of modern North American wolves for the dogs of Native Americans, only Druzhkova’s team combined both data sets to make a genetic comparison between Beringian wolves and dogs. His unfortunate inadequacy to compare his results on the Altai dog with Germonpré, whose results on Pleistocene Belgian dogs of comparable age and morphology were hampered by the low resolution of just 57 bp of the mitochondrial control region, may be solved by the results of Pilot’s team he was not acquainted with. Like the Pleistocene Belgium dogs of Goyet Cave, Altai dog of Razboinichya Cave clearly cluster with ancient Holarctic wolves rather than modern wolves, but their close genetic relationship with modern dogs is based on the virtual extinction of the Holarctic wolf source population rather than some advanced stage of dog domestication. As such, criticism against the existence of Pleistocene ‘dogs’ is still valid:
One of the features that M. Germonpré et al.’s so-called ‘Palaeolithic dogs’ (and the Razboinichya specimen) have in common is that they represent one or a few dog-like individuals found amongst many typical wolf individuals.
[…] the ‘Palaeolithic dogs’ […] may simply be rather ‘short-faced’ wolf individuals that lived within a population of typical wolves that interacted in various ways with human hunters. While the dog-like morphology of some Late Pleistocene wolves may have arisen due to persistent interactions with people over varying lengths of time, it is misleading to call this relationship ‘domestication.’ (Crockford & Kuzmin, 2012)
The similarity of Pleistocene dogs with certain types of Pleistocene wolves may be deceiving. Not unlike Beringian wolves, the Paleolithic dogs tend to have short, broad palates with still large carnassials:
Compared to wolves, ancient dogs exhibit a shorter and broader snout (Lawrence, 1967; Olsen, 1985; Sablin and Khlopachev, 2002). All Palaeolithic dogs in our study conform to this pattern. (Germonpré et al., 2009)
European Palaeolithic dogs, characterized by, compared to wild wolves, short skulls, short snouts, wide palates and braincases, and even-sized carnassials (Germonpré, 2012a)
There exists an older notion of a late Pleistocene lineage of dag that might have existed during the late Pleistocene until these became globally extinct during the last 20,000 years. This possibility of ‘an aberrant lineage of dog-like canids might have existed throughout the northern hemisphere during the late Pleistocene’ was recently explored by Thalmann, to the somewhat unsettling result that no exact mtDNA matches could be retrieved in modern dogs or modern wolves. At least the sudden Neolithic reduction of the carnassials in the perceived dog lineage may indicate a recent bottleneck that could explain such an extinction of mtDNA lineages for dogs, while the extinction of these mtDNA lineages in wolves has already been cited as a typical post-Glacial phenomenon: also ‘the mtDNA of the Belgian fossil wolves shows a large amount of genetic diversity that has not been described for modern wolves’ (Germonpré et al., 2009).
This ‘aberrant lineage of canids’ probably existed in the ecomorph stock that had its gravity in NE Asia and northern America, and incidentally reached far into the west. Being closely related with Eurasian wolves, an early tendency towards speciation was arrested by the Late Glacial events that led to the predominance of the Holarctic wolf. Mere extinction may have been the result, or advanced hybridization processes that eventually lead to ‘the fusion of the parent species’ gene pool and a loss of species.’ (Reece et al., 2011), not unlike the ABC Island brown bears that are recently identified as the descendants of a polar bear population that was gradually converted into brown bears via (male-dominated) brown bear admixture: ’This process of genome erosion and conversion may be a common outcome when climate change or other forces cause a population to become isolated and then overrun by species with which it can hybridize’ (Cahill et al., 2013). By the time the Eurasian ice age wolf ecomorph became extinct, human interaction or ‘dog domestication’ was already ongoing, leading to the preservation of much of the genetic diversity that has disappeared in wolves. The now attested genetic continuity in the Pleistocene Altai dog supplies evidence it didn’t take such a long time since the Pleistocene to get nowhere. On the contrary, the origin of dogs can now be perceived firmly rooted in the Pleistocene whatever the type of domestication applicable to the earliest interactions with humans. Germonpré (2012b) announced a forthcoming investigation of stable isotopes on Pleistocene dogs to verify if their diet can be related to that of prehistoric humans from the same time and region. Instead, Belgian Pleistocene wolves were already attested to consume the same kind of bulky prey that Leonard et al. (2007) deduced for eastern Beringian wolves based on their bite, such as horse and large bovids. Could the Pleistocene abundance of meat offer an alternative explanation for the unaltered size of the carnassials of Pleistocene dogs? If so, would there exist any other criteria that suffice to prove the veracity of Pleistocene dog domestication at all?
The persistence of large carnassials up to Neolithic times would also imply a dependency of fresh meat that may have been ever harder to obtain. On the eve of the Neolithic transition, when increased population pressures virtually forced human culture into the direction of food production, a dog must have been an expensive asset only a few could afford. Until recently everywhere in Polynesia starch-rich poi from the taro corm was used to fatten the dogs for use as food because meat was too valuable to be used as dog food. This transition of breeds like the Hawaiian Poi dog and the Maori Kuri dog, both extinct, from predators to fattened up food resources, was only possible in a Neolithic society with an abundance of starch-rich products. The Neolithic change to starch-rich diets induced some dogs to adapt genetically (Axelsson et al., 2013). This important event in dog evolution apparently caused an explosion of population growth and genetic replacement – until very recently confused with a one and only domestication event in the Neolithic rather than already during the Pleistocene.
Only nowadays dog domestication is being appreciated as a true evolutionary process. Their divergence from wolves wasn’t just a superficial accumulation of qualities favored by human preferences, such as color and character, hardly worthy of major biological interest. Instead, novel adaptations including brain functions, starch digestion and fat metabolism indicate more fundamental changes, each having evolutionary advantages all of their own that tend to set dogs apart from wolves. One amazing result of current investigation is these changes must have been closely associated with dog populations in Southeast Asia, even to the point that dogs were hypothesized to originate from an otherwise unspecified Asiatic wolf, albeit ‘with minor genetic contributions from dog–wolf hybridization elsewhere’ – for this occasion assumed to have inhabited eastern Asia south of the Yangtze River (Ding et al, 2011). Actually, there is no shred of evidence wolves or other members of the “Canis” genus were present in this area, thus adding up to a major inconsistency in dog evolution:
The earliest archaeological evidence of ancient dogs was discovered in Europe and the Middle East, some 5–7 millennia before that from Southeast Asia. However, mitochondrial DNA analyses suggest that most modern dogs derive from Southeast Asia, which has fueled the controversial hypothesis that dog domestication originated in this region despite the lack of supporting archaeological evidence. (Sacks et al., 2013)
Once again high genetic variability emerged as a poor advice to pinpoint the geographic origin of a species. Not unlike the results on human DNA, for dogs the archeological record is all out of tune with genetic evidence, or the way it is currently interpreted. Also for dogs scientific efforts to understand the origin were increasingly directed away from observations considered inconvenient to the traditional ‘scientific’ scenarios, and aberrated in the realm of increasingly unintelligible constructs. Intriguing parallels with the Recent Out of Africa (ROA) paradigm may be elucidated, where high human genetic variability of the purported African homeland is alternately considered evidence for a recent origin of modern humans – or the result of archaic hybridization (Hammer et al., 2011). Likewise, modern science erroneously sought the putative center of dog domestication where genetic variability reaches peak values, that for dogs could be found in Southeast Asia. Dogs even mimic the genetic signals of change in modern humans:
Sets of functionally related genes show highly similar patterns of evolution in the human and dog lineages. This suggests that we should be careful about interpreting accelerated evolution in human relative to mouse as representing human-specific innovations (for example, in genes involved in brain development), because comparable acceleration is often seen in the dog lineage. (Lindblad-Toh et al., 2005)
Rather than being deterred by the lack of archeological evidence, modern investigation contented itself with pursuing false positives to discard Pleistocene dogs like this Altai canid as an incipient dog that did not give rise to late Glacial – early Holocene lineages and probably represents wolf domestication disrupted by the climatic and cultural changes associated with the LGM (Ovodov et al, 2012). For convenience of the naysayers this fate was shared by an abundance of other ‘incipient dogs’ allegedly up to 36,000 BP whose remains were found littered over a wide area, not only including the canid skulls from Goyet (Belgium), that so far counts as the oldest specimen, but also from disparate places like Predmostí (the Czech Republic), and Mezin and Mezhirich (the Ukraine). Four out of thirteen ambiguous finds fished from the bottom of the North Sea (Southern Bight), were firmly identified as Pleistocene dogs in the thesis of Datema, 2011. In the deepest part of the famous Chauvet cave, France, a track of footprints from a large canid could be associated with the one of a child (Garcia, 2005), whose torch wipes were dated at c. 26,000 BP. Still other investigators remained to even discard the notion of these Pleistocene dogs being incipient at all – to the chagrin of Germonpré’s team that as late as 2012 felt obliged ’ to remedy some errors, misunderstandings and misrepresentations’ on the case. Now, the results of Druzhkova’s team blow away this apparent prevalence of a Southeast Asian origin of dog domestication in more recent scientific investigation, that not unlike the Recent Out of Africa paradigm became genetically supported by unfortunate conclusions on variability of mtDNA (Savolainen et al., 2002) and of Y-DNA (Ding et al., 2010) respectively. However, unlike ROA, archeological and fossil evidence that a common ancestor was present in the putative geographic origin, i.e. traces of early domestication and a habitat for prehistoric wolves in Asia South of Yangtze River (ASY) as proposed by Pang et al. (2009), is still dearly missing.
The study of VonHoldt et al. (2010) had already revealed disproportionate hybridization especially for the ancient breeds in east- and southeast Asia by Chinese and Middle Eastern wolves (supplemental Figure 5 at k=5). Apparently hybridization inflated heterozygousity of south-east Asian nuclear DNA and lured the scientific community into an “Out of Southeast Asia hypothesis. Instead, Sacks et al. (2013) introduced a new interpretation of this Southeast Asian hypothesis by stating that ‘isolation of Neolithic dogs from wolves in Southeast Asia was a key step accelerating their phenotypic transformation’, to offer a scenario where a new type of dog emerged in the Neolithic that virtually pushed earlier Palaeolithic dogs into extinction:
Archaeological and ancient DNA evidence suggesting that late Palaeolithic dogs were replaced by Neolithic immigrants in regions as disparate as Japan, the Middle East, and North America
The apparent origins of most modern dog matrilines from Southeast Asia has been interpreted as evidence that dogs were first domesticated in this region (Savolainen et al. 2002; Pang et al. 2009). However, the lack of archaeological evidence of dogs in Southeast Asia until some 5,000–7,000 years later than in central and western Eurasia, suggests either that the single genealogical history reflected in mtDNA could be misleading (e.g. VonHoldt et al. 2010) or that most modern dogs trace their ancestry proximately to Southeast Asia, but as a secondary center of diversification associated with Neolithic rather than Palaeolithic peoples (Brown et al. 2011).
[…]our findings support the hypothesis for a massive Neolithic expansion of dogs from Southeast Asia rather than a Palaeolithic origin of dogs from this region. (Sacks et al., 2013)
Thus accelerated Neolithic evolution and the absence of wolves in Southeast Asia to mate with, are now considered the main agents for the rapid change of Palaeolithic dogs into modern dogs, the latter being especially successful in increasing their numbers on a worldwide scale.
Inadvertedly, hybridization was here mentioned as a factor to be dealt with. Actually, recurrent hybridization events already prevented Canis evolution to be a straightforward linear succession towards present-day species. This process should also have blurred out the nascent differences typical of a more detailed branching tree full of evolutionary dead-ends, as traditionally employed also for canid evolution. Again, not unlike human evolution, mosaic evolution was a feature also for canids that can be traced back even to the early divergence of wolves and jackal:
considering C. etruscus and C. arnensis as wolf-like and jackal-like dogs, respectively, is an oversimplification not always valid, because C. arnensis is more similar to C. lupus than C. etruscus regarding some cranial characters (e.g., Fig. 1b), while C. etruscus seems to exhibit a broader set of peculiar features. Recent genetic studies confirm this hypothesis, as jackals do not constitute a homogeneous genetic group despite their great morphological affinity, albeit different analyses do not fully agree on their phylogenetic relationships (Cherin et al., 2013)
Some prehistoric canid characteristics are simply ancestral, what back in time can be illustrated by some degree of convergence to rather coyote-like forms, suggesting even jackals evolved partly parallel with the ancestors of the gray wolf:
This paper reports a new species of dog (Canis accitanus nov. sp.) from the Fonelas P-1 site (dated close to the Plio-Pleistocene boundary) in Granada, Spain. This new taxon shows cranial features more similar to coyote-like dogs (C. lepophagus, C. priscolatrans, C. arnensis or C. latrans) than to wolf-like dogs (C. etruscus, C. mosbachensis or C. lupus), such as a long and narrow muzzle, a little-developed sagittal crest and frontal bones raised only a little above the rostrum. (Garrido & Arribas, 2008)
As raised in a previous blog, in some cases mosaic evolution may be the result of hybridization events or cross-species gene flow during some extended period during speciation, or even afterwards as long as cross-breeding may still result in viable offspring. According to Gaubert et al. (2012) ‘hybridization among Canis taxa has proved to be common and to involve significant phenotypic changes in hybrid generations, reaching fixation in several cases’.
Naturally, cross-breeding may result in increased variability – as long as the elimination of deleterious hybrid fitness components by selection doesn’t purge most of the polymorph alleles. However, admixture with modern wolves can’t fully explain the genetic deviation of modern dogs since much of their polymorph alleles simply can’t be found in wolves. This does not contradict wolf admixtures in a later stage, what apparently occurred in the ancestors of Neolithic dogs. Since ‘[…] the European and American breeds clustered almost entirely within the Southeast Asian clade, even sharing many haplotypes, suggesting a substantial and recent influence of East Asian dogs in the creation of European breeds’ (Brown et al., 2011), it shouldn’t come as any surprise that ‘morphologic comparisons suggest that dogs are closest phenotypically to Chinese wolves’ (Wayne et al., 1999). The evolution of Neolithic dogs must have been highly impacted by Pleistocene dogs near East Asia, what suggests late-Pleistocene admixture to explain that ‘one osteological feature diagnostic of dogs is also found among Chinese wolves’ (Savolainen et al., 2002). However, the more complex hybrid character of all descendant dog breeds may be illustrated by the ‘higher proportion of multi-locus haplotypes unique to grey wolves from the Middle East, indicating that they are a dominant source of genetic diversity for dogs rather than wolves from east Asia, as suggested by mitochondrial DNA sequence data’ (VonHoldt et al., 2010).
Hybridization between dog breeds require a broad genetic base to start with. However, the direct ancestors of modern wolves and their deduced range of genetic variability don’t supply a sufficient source for the total range of dog variability. Still, an abundance of other traits attest the impact of hybridization processes. Neoteny, the retention of juvenile characteristics into adulthood, is often considered an important characteristic of dogs. Serpell considered this a result of hybridization:
Our feeling on the development of breeds is expressed by Haldane (1930, pp. 138), writing about the evolution of species, when he stated that there is ‘every reason to believe that new species may arise quite suddenly, sometimes by hybridization, sometimes perhaps by other means. Such species do not arise, as Darwin thought, by natural selection. when they have arisen they must justify their existence before the tribunal of natural selection’. (Serpell, 1995, p.42)
Brown’s team (2011) does a remarkable job in distinguishing a Southeast Asian development in recent dog evolution, though his classification doesn’t suffice to reveal the origin of dog Y chromosome haplotypes. Genomic analysis of prehistoric canids, modern dogs and wolves indicate a basal placement of some dog haplotypes in the phylogeny. One middle-eastern haplotype actually resulted “ancestral”, being attested also in Dhole, black-backed jackal and a wolf from China (haplotype 12). Middle-eastern dog Y-chromosome haplotypes resulted shared with wolves and/or Southeast Asian dogs (haplotypes 8, 10 and 11) or none (haplotypes 7 and 9, though both being rather distantly related with wolves). Only Southeast Asian dogs were easily distinguished from all other related canines combined. Despite alignment bias being possibly the prime reason for these results, more recent wolf admixture and even cross-species hybridization can’t be ruled out. Indeed, the most basal members of Canis tend to be more “doggish” in looks and behavior, while the more “wolfish” phenotype of the northern hemisphere seems to have made its appearance only about 300,000 years ago. In other words, canids are increasingly “doggish” with their genetic distance from true grey wolves, what can be illustrated by the incremental series Indian wolves; Egyptian wolves; Golden jackal; coyote; Ethiopian wolf (Charles Darwin equivocally hypothesized this species gave rise to greyhounds); “the other jackals” (a polyphyletic group that despite great morphological affinity miss any further taxonomic integrity); and Dholes respectively, the latter having a phenotype most similar to the dingo while being of the genus “Cuon,” and as such not even part anymore of genus “Canis.” The wide-spread “doggish” appearance among non-wolf canids might indeed raise the question of ancient attempts to achieve interspecies hybrids.
The confusion extends to other domesticated animals: also the domestication of sheep, amongst the first species to be domesticated by man, is characterized by considerable genetic variability and a certain lack of wild matches. Kijas et al. (2012) state that despite a common origin of all domestic breeds of sheep, their ‘analysis revealed this domestication process must have involved a genetically broad sampling of wild stock.’ Moreover, like with dogs, the genetic variability of sheep has a weak global population structure and lack of association between genetic diversity and distance from the perceived domestication center, interpreted thus:
This suggests a highly heterogeneous predomestication population was recruited, and the genetic bottleneck which took place was not as severe during the development of sheep as for some other animal domesticates. It is also possible that cross-breeding with wild populations persisted following the initial domestication events to generate the diversity observed. (Kijas et al. (2012)
However, a purported single origin certainly contradictory with a broad genetic base. The possibility of cross-breeding with wild populations, as raised by Kijas’ team, virtually depends on the assumption that ‘high levels of gene flow have occurred between populations following domestication’. However, admixture appears contradictory with the observed homogeneity:
For SNP pairs separated by 10 kb or less, a high degree of conservation of LD phase was observed between all breeds […] Given that LD at short haplotype lengths reflects population history many generations ago, this also supports a common ancestral origin of all domestic breeds of sheep. The result is in contrast to cattle, where two distinct groups emerge from a similar analysis, even at haplotype lengths of 0–10 kb, reflecting the Bos taurus taurus and Bos taurus indicus sub-species and their separate domestication events (Kijas et al., 2012)
Instead, Pedrosa’s team rather adhered to the view that ‘introgression is generally ruled out as the cause of clearly differentiated maternal lineages in livestock, since introgression via females seems quite improbable.’ Indeed, just like with dogs, hybridization can’t be easily assumed just because of the theoretic possibility offered by closely related species or sub-species in the wild.
The center of sheep domestication currently encompasses the natural environment of at least three subspecies of Ovis, whose genetic boundaries are sometimes difficult to conceive: Argali (O. Ammon), Urial (O. Vignei), and Mouflon (O. Orientalis), the most western variety. Mitochondrial DNA of sheep doesn’t show any close relationship with argali or urial sequences (Pedrosa, 2006), what is remarkable since hybridization between the various subspecies has been observed in the wild. However, if hybrid admixture was limited to the domestication event this would almost insinuate a domestication purpose! For sheep cross-breeding may have been recognized from the start as predominantly detrimental to their specific qualities in the process of domestication, what should be a compelling argument to discard the persistence of cross-breeding with wild populations as a valid explanation for the observed genetic diversity of the domesticated form. On the contrary, the existence of widely spread and divergent mtDNA lineages without any current match in wild populations rather seems to indicate ancient hybridization events that preceded the fixation of domesticated sheep:
Time since divergence of types B and A estimated from the Cyt b gene [for sheep lineages] (around 150 000 to 170 000 years ago) agrees with the values obtained from Cyt b for goat lineages by Luikart et al. (2001; around 200 000 years ago) as well as those obtained for cattle (Bradley et al. 1996). Lineage C proved to have diverged earlier (between 450 000 and 700 000 years ago). (Pedrosa, 2006)
Another positive for early hybridization “by design” involves the domestication of chicken, that may descend from up to four Gallus species and their subspecies:
Four species of genus Gallus inhabit Southeast Asia: […] Red junglefowl has a strong sexual dimorphism with males having red fleshy wattles, and it is most widely distributed over the area. La Fayette’s junglefowl morphologically resembles red junglefowl, but it inhabits only Sri Lanka. Gray junglefowl has body plumage on a gray background color and is distributed from southwest to central India. Morphologically distinct green junglefowl is limited to Java and its immediate vicinity, Bali and Lombok [corr.: the Lesser Sunda Islands]. It has been debated whether any single species of the four, especially red junglefowl, predominantly contributed to the genome of domestic chickens (a single-origin hypothesis) or whether multiple species of the four made a substantial genetic contribution to domestic chickens (a multiple-origin hypothesis). (Sawai et al., 2010)
Actually, the Green junglefowl has a lot more eastern penetration into the Lesser Sunda islands, what somewhat invalidates Sawai’s ‘Javan’ origin hypothesis for this species. However, its unique isolation resulted in a genetically divergent species whose ability to hybridize with chicken is highly restricted.
Evidence abounds that Red junglefowl is the prime progenitor of domesticated chicken:
Haplogroup E is predominant among Indian, Middle Eastern, and European chickens and is an indication that the roots of European chickens lie within the Indian subcontinent. (Gongora, 2008b)
However, not unlike dogs, the calculated mtDNA divergence date with this purported progenitor by far exceeds archeological evidence of domestication:
According to archeological findings, the divergence time of domestic chickens from junglefowls is estimated to be on the order of 10,000 years. The MCMC method reveals, however, that the extent of nucleotide divergence after the split of red junglefowl from the chicken ancestor is […] 58,000 +/- 16,000 years ago. This dating is nearly six times older than what the archeological remains suggest. (Sawai et al., 2010)
Like with dogs it is tempting to attribute this divergence discrepancy to an ‘aberrant wild subspecies’ as the progenitor of the domestic form. Despite the historic distribution of Red junglefowl is limited to Southeast Asia in the range between the Indus valley, Yunnan (southern China) and Lombok, the oldest undisputed domestic chicken remains, dated 5400 BC, have been recovered from archaeological sites in northern China. Though chicken near that age (5000 BC) were also attested in cultural contexts in the Ganges region of India, this has led to debate about whether the natural range of Red Junglefowl reached much further north in prehistory. However, unlike dogs, this genetic diversity doesn’t extend to mtDNA, despite the lack of a major mismatch between the mtDNA haplotypes of domesticated and wild subspecies.
Only 56 out of all 206 Red junglefowl mtDNA sequences, recovered from the control region (CR) and available to a 2013 study of Miao’s team, were not found in domestic chicken. Of these, only seven from Yunnan and the island of Hainan (China) could be accommodated as new haplogroups W-Z within the monophyletic tree of domestic chicken, thus probably confirming rather Chinese roots of domesticated chicken (in the vein of Liu and Oka). An additional unclassified 21 haplotypes from Vietnam, Sumatra and Haryana (Northern India) appear not too distantly related, while 28 other haplotypes from Haryana and Indonesia could only be classified as ‘divergent’:
As for the red junglefowl, 76.2% (157/206) of the CR haplotypes were assigned to haplogroups in this genealogy (Figure 4; see Supplementary dataset 1). Apart from the common haplogroups A–G, the wild fowl harbored haplogroups W–Z, which were not detected in domestic chickens. Of the remaining sequences (49/206) not classified in the genealogy, 28 haplotypes from India and Indonesia (for example, ‘outgroups’ in Figure 1) had too many variants to be assigned; variation included many transversions (see Supplementary dataset 1). This suggested that they were remotely related to the other chickens (Miao et al., 2013)
This sequence divergence is such that natural hybridization with grey and green junglefowl respectively has been the suggested source of these divergent mtDNA lineages, though Miao’s team justly stresses this hypothesis requires a more comprehensive survey.
In Bangladesh the ‘phylogenetic tree showed low genetic distance and close relationship within and between the chicken populations of Bangladesh, which were closely related with G. g. murghi of Indian origin’ while a minority of domestic chicken and one red junglefowl were related with G. g. bankiva and G. g. gallus, ‘implying the origin of gene flow to Bangladesh’ (Islam & Nishibori, 2012).
This shocking lack of evidence for a truly unadmixed wild ancestral population has severe repercussions on the origin question of domestic chicken. The first three Gallus g. Bankiva accession numbers ever investigated (AB009430, AB009431 and AP007718) were found sufficiently different to originally exclude the Javanese wild subspecies from the group of domesticated chicken ancestors altogether:
On the whole, the analyzed data fit into two main clades […]: one formed by the continental red jungle fowl subspecies and all domestic chicken samples, which we named the continental clade, and another exclusively constituted by G. g. bankiva samples from Java that we named the island clade. (Liu et al., 2006a)
However, Oka et al. (2007) modified the interpretation of AP007718, and attributed a subsequent bankiva sample (AP003323) to one of the known chicken haplogroups, thus bringing also the Gallus g. bankiva subspecies into the fold of ancestral chicken:
G. g. bankiva [~Javanese red junglefowl] sequence ([AP007718, corr.]), which is distantly related to domestic chickens, was located on the outside of the Type C clade. However, another G. g. bankiva sequence ([AP003323, corr.]) and two G. g. gallus sequences [AP003322 and AB007725] were included in Type C. One G. g. spadiceus [~Burmese red junglefowl] sequence (AB007721) was close to the domestic chicken and very similar to Type A. The other G. g. spadiceus sequence (AP003323) was included in Type E. (Oka et al. – 2007).
Despite a genetic distance of no less than 30 mutation steps (Figure 3, Oka et al. 2007), AP007718 is slightly closer related with haplogroup C as defined by Oka’s team. It was not too farfetched to attribute an ancestral status to this chicken haplogroup:
[…] it is suggested that Types D, F and G diverged from Type C, and that Type E diverged from Type B.
[…] we suggest that Type F was derived from a group of Indonesian native chickens
It is suggested that Types A and B chickens (i.e. chickens of Chinese and Korean origin) were derived from Type C (i.e. they are of Southeast Asian origin) – Oka et al. (2007)
Such an all-encompassing phylogenetic system for chicken mtDNA, that includes ~75% of all wild specimen, seems irreconcilable with the extant picture of low genetic distances for chicken mtDNA:
It should be noticed that all the haplotypes that shared by or restricted to the red jungle fowls in clades A, B, E, and F diverged from the potential root in each clade by no more than 4-mutation distance, which was within the mutation distance observed between the domestic chicken and the potential wild progenitor G. g. gallus (Liu et al., 2006a)
Apparently, for all chicken and continental Red junglefowl together, the calculated mtDNA age is far less than nuclear DNA would suggest. However, since the monophyletic tree of chicken mtDNA can’t convincingly reflect the evolutionary history of the Gallus parent species, this should imply that current Red junglefowl populations simply lost their original mtDNA diversity quite recently due to introgression from feral chicken.
Better survival of ancestral mtDNA haplogroups in sheep and dogs could be due to evolutionary strain elsewhere that applied exclusively on their wild progenitors after the domestication events. Currently, gene flow between wolves and dogs, or between sheep and their wild progenitors, virtually doesn’t happen in the wild. Wolves would rather eat than mate a dog, and sheep don’t even survive to meet a wild partner in its habitat. Red junglefowl didn’t experience or acquire such an efficient natural barrier against gene flow from feral domesticated forms. Up to modern times this situation still didn’t affect the competitiveness of Red junglefowl populations in the wild. In general, in a natural habitat admixture of wild animals with their domesticated kin tends to compromise the competiveness of their feral offspring. Genetically there is few to gain and much to lose from domestic chicken that e.g. lost their ability to fly; feral sheep don’t even exist and only wolves evolved to abstain from cross-breeding with feral domesticated kin – even without strict biological barriers. However, since modern wolves predominantly attest another mtDNA clade, it is more than likely that evolutionary adaptation included less vulnerability to gene flow and ultimately led to the extinction of dog-introgressed wolves that were purportedly available in the Pleistocene (Germonpré et al., 2012a). The current vulnerability of Red junglefowl is unknown, but all indicates gene flow and introgression from domesticated chicken is rampant. The success of Green junglefowl west of the Wallace biogeographic division where they share the habitat with Javan Red junglefowl, while the latter hardly penetrated further east than Lombok (except for some unreliable observations). Wallace’s Line is the western border of a transitional region between Asiatic and Australian floras and faunas, where organisms show a high degree of isolation and endemism. Here, the Lesser Sunda Islands chain was definitely accessible from the west in the Pleistocene, what is attested even by the elephant that made an appearance up to Timor. West of this line, Java never ceased to be part of the Asian ecozone and hence was never truly isolated to justify Green junglefowls divergence from Red junglefowl populations. Instead, current cohabitation in Java together with the local subspecies of Red junglefowl could be indicative of future replacement tendencies for Gallus that mimic the gray wolf divergence from dogs towards the modern Holarctic wolf.
However, chicken introgression could even be indicated for the vastly divergent Green junglefowl, on the basis of nuclear DNA, attesting that ‘shared haplotypes are evenly distributed over all samples of red junglefowl, whereas this is not the case for those of green junglefowl’ (Sawai et al., 2010).
Purportedly introgressed chicken haplotypes in the green junglefowl were found to significantly increase Green junglefowl nucleotide diversity. This result is remarkable, since green junglefowl allegedly diverged 3.6 million years ago from the common ancestor of chicken and red junglefowl (Sawai et al., 2010), and first generation female hybrids were found notably infertile. Introgression of mtDNA would thus be close to impossible here. To break natural barriers in the forests, introgression of nuclear DNA may only be achieved for next generation hybrid offspring, that indeed must be readily available on a local basis in feral chicken populations. Indeed, Green junglefowl hybrids are still around being in high demand and part of an old Indonesian tradition.
Meanwhile, ‘attempts to investigate domestication and dispersal using mtDNA data from modern chickens have been confused by the tangled phylogenies which reflect millennia of overlapping dispersals and over a century of interbreeding for both commercial lines and show breeds’ (Storey et al,. 2012). Hence, only nuclear DNA remains to offer more insight into the origin of genetic diversity in domesticated chicken, while mtDNA diversity may only supply information on the world-wide history of the domestication process itself. Interestingly, ‘regional distribution of the clades was observed, which indicates some geographic structuring in chicken populations’ (Liu et al., 2006a). Structure, that thus should tell us the tale of domestic chicken from a single source rather than multiple domestication events. Also this feature is structurally different from domesticated animals like dogs and sheep, where high mtDNA diversity was preserved. This may be explained by a quite distinguished purpose of chicken domestication, as ‘it has also been proposed based on comparative morphology, historical depictions, and genetic relatedness that egg type chickens are the most ancient breed […] Therefore, the phylogeographic assumption that females have greater geographic inertia may be violated in the study of chickens by the widespread use of eggs’ (Storey et al., 2012). No other domestic vertebra experienced selective processes that applied so exclusively on females, what inevitably contributed to the severe reduction of mtDNA diversity as being observed.
The original proposal that haplogroup C ultimately derives from China, where prehistoric Red junglefowl populations could merely be assumed, might be as good as any, and actually reminds to the proposal of an ‘aberrant lineage of wolf’ for the ancestor of domestic dogs:
Although Japanese chickens displayed the highest nucleotide diversity […] for the clade C (Fig. 2D), the absence of red jungle fowl samples in clade C favors that this clade originated from South China. A recent domestication of clade D or gene Xow from domestic into the wild red jungle fowl population are two possible explanations for the fact that clade D mainly contained of red jungle fowl and gamecocks. These distinct patterns combined with archaeological records as well as with the geographic distribution of G. gallus are consistent with clades C and D originating relatively recently, perhaps in South and Southwest China and/or surrounding areas (Liu et al., 2006a)
Deviation from a simple star-like distribution pattern of this geographically restricted grouping may be due to the success of more recent breeds that instead propagated the few international mtDNA lineages, such as Haplogroup E. Due to the selective forces of human intervention such perpetual replacements completely obfuscated, for instance, the debate on early Polynesian arrivals in the Americas, where allegedly pre-Columbian chicken and their potential offspring happen to group predominantly with international mtDNA rather than the Polynesian haplogroups of more limited distribution:
The single ancient sequences reported from Tonga Mele Havea and Ha’ateiho, Samoa Fatuma Futi, Hawaii Kualoa, Niue Paluki, one sequence from Easter Island Anakena (early settlement phase Cal AD 1270–1400), and the putatively pre-Columbian (Cal AD 1304–1424) Chilean El Arenal-1 sequence belong to haplotypes 8 and 5 within haplogroup E (Fig. 1). Haplotype 8 equates to the E1 haplotype reported in Liu et al. [2006a], which is ubiquitous worldwide and 100% identical to haplotypes from European Barred Plymouth Rock, White Plymouth Rock, White Leghorn, and New Hampshire as well as native chicken sequences from [India, corr.], Central Asia, and China. In contrast, five of the other contemporaneous archaeological chicken sequences from Easter Island cluster with haplotypes 145 (n = 4) and 148 (n = 1), which are part of an uncommon group comprising mostly Indonesian chickens within haplogroup C (Fig. 1). Ancient Easter Island haplotype 145 is identical to one sequence of Red Junglefowl from the Philippines. Within other modern chickens, the closest related sequences have been recorded from Lombok and Java in Indonesia and the Philippines. Given their unique phylogenetic position and their pre-European contact dates, haplotypes 145 and 148 presumably represent a record of early Polynesian chicken transport, potentially overwritten subsequently in the western Pacific. The noticeably less star-like pattern of haplogroup C, centered on the less frequent haplotypes 91 and 95, is likely to be an artifact of incomplete sampling or a different population history. (Gongora et al., 2008a)
Nowadays, the haplogroup C denomination is confined to a much smaller group of continental chicken, while Oka’s and Gongora’s haplogroup C definition has been currently passed over to Liu’s (ancestral) haplogroup D, once tentatively proposed by Liu’s team for a loose group of cock-fighting chicken and Red junglefowl though currently thought to be closely associated with an Austronesian legacy in Indonesia, Madagascar and (hence?) Africa, and Polynesia:
Among the three Guamanian haplogroup D samples, three lineages were observed. One matched contemporary samples from the Philippines, Indonesia, and Japan. The other lineages were unique, but were closely related to contemporary samples from Indonesia, Japan, the Philippines, and China as well as India, Sri Lanka, Thailand, and Madagascar. Among the 40 haplogroup D samples from Vanuatu, seven lineages were observed. Four were exact matches to contemporary samples from Indonesia, Japan, the Philippines, and Southern China, as well as prehistoric Easter Island samples. The major Vanuatu lineage (n = 17), also found in a Red Jungle Fowl from the Philippines, was distributed across all four islands sampled (Dancause et al., 2011)
Conceivably the oldest ‘chicken’ haplogroup, the Indonesian hotspot of mtDNA haplogroup D distribution opens up an entirely new perspective on chicken domestication. Near the Island Southeast Asian origin of Polynesian Haplogroup D chicken, Bekisars are still the first generation (F1) hybrid offspring with Green junglefowl. Bekisars, whose colorful roosters have a glossy blackish green plumage, were the mascots of the original inhabitants of the Sunda Islands. Indeed, fresh chicken hybrids of the green junglefowl are still in demand. Seafaring cultures in the neighborhood allegedly took advantage of their unique crowing sound, loud enough to be heard for two miles over the sea, and consequently hybrids were part of their traveling gear. Because of the location, results of hybridization experiments on local chicken may be most noticeable in chicken populations whose history was especially related to mtDNA haplogroup D.
Currently, the role attributed to green junglefowl hybrids in the earliest Polynesian explorations is a popular theme. This has everything to do with the radiocarbon dating of apparently pre-Columbian chicken of El Arenal, Chile, that allegedly lived sometime between ad. 1321 and 1407 (Storey et al., 2007), and its purportedly ancestral relation with a peculiar local breed:
It has been suggested that the unique type of chicken known as the Araucana, which has no tail and lays blue eggs, is descended from pre-European stock bred by the Mapuche (formerly called Araucanos) people of Southern Chile (Storey et al., 2007)
An Oceanic origin, still contested, has been partly substantiated:
All ancient West Polynesian samples, early samples from Anakena, Easter Island and Kualoa, Hawaii, and the El Arenal sample share a single unique point mutation (a T to C transition) at site 214. One of the modern Araucana feather samples also shares this unique mutation. Three other SNPs (all transitions) at sites 278, 303, and 339 are shared by these West Polynesian, early Anakena and Hawaii, and the Chilean bone samples and sequences reported from modern chickens in Southeast Asia, specifically samples from the Yunnan region of China and Vietnam (Storey et al., 2007)
Indeed, in 1532, Spanish conquistador Francisco Pizarro recorded the presence of chickens in Peru, where the Inca used them in religious ceremonies. ‘That suggests chickens had already been there for a while’ (Storey in Archeology, Volume 61 Number 1, 2008).
However, all (meanwhile) three purported Pre-Columbian chicken remains turned out to have their mtDNA in the most common haplogroup E. But, in accordance with ‘modern Chilean sequences [that] cluster closely with haplotypes predominantly distributed among European, Indian subcontinental, and Southeast Asian chickens, consistent with a European genetic origin’ (Gongora et al., 2008a), this common haplotype (mtDNA E) was also present in ancient Polynesian chicken. Prehistoric chicken remains from Easter Island stand out for the dominant presence of mtDNA D, however, so ‘the two lineages may have converged before they were dispersed, as a polymorphic population, to Hawaii and Easter Island. Both haplogroups appear in early period archaeological sites in East Polynesia’ (Storey et al., 2012).
The search for haplogroup D in the Americas was not all in vain:
Haplogroup D has not yet been detected in any ancient chicken bone samples from Europe or from Thailand. Thus far it has only been identified in ancient Polynesian and Micronesian chicken remains as well as a single Peruvian sample. Haplogroup D has not yet been detected in any ancient chicken bone samples from Europe or from Thailand. Thus far it has only been identified in ancient Polynesian and Micronesian chicken remains as well as a single Peruvian sample. The available sample size for this study is too small to be representative
The early date of the Peruvian assemblage from which this haplogroup D sample was recovered raises the possibility that it could represent a descendant of a chicken haplogroup introduced from Polynesia. The fact that the sequence from the chicken bone from the Torata Alta site in Peru is identical to one from Fais in Micronesia also may support a possible Pacific connection. (Storey et al., 2012)
The Green Junglefowl is the only species of junglefowl that produces grey tinted eggs, indeed a possible forerunner of the bluish Araucana eggs. Instead, Red junglefowl miniature eggs vary between pure white and a deep creamy-buff. Ancient breeds often have tinted eggs (Silkies, Sussex) that approximate Gray junglefowl, whose eggs vary from very pale cream to rich warm buff, though the latter are often freckled and even spotted. The brownish red spotted eggs of the Singhalese Gallus Lafayette, or Ceylon junglefowl, appear profoundly out of range though reminds the French marran breed. Funny detail is that brown eggs, commonly associated with ‘natural’, are actually without equivalent in natural gallus species.
Nishibori et al. (2005) elaborated molecular evidence of Gallus hybridization except for the Green junglefowl. Plain hybridization has been well substantiated with the Grey junglefowl (India):
Our data imply that carotenoids are taken up from the circulation in both genotypes but are degraded by BCDO2 in skin from animals carrying the white skin allele (W*W). Surprisingly, our results demonstrate that yellow skin does not originate from the red junglefowl (Gallus gallus), the presumed sole wild ancestor of the domestic chicken, but most likely from the closely related grey junglefowl (Gallus sonneratii). This is the first conclusive evidence for a hybrid origin of the domestic chicken, and it has important implications for our views of the domestication process (Eriksson et al. – 2008)
Thus, the most common chicken being yellow-legged, modern chicken should be descendants of hybrids that originate predominantly from India, home of both the Grey junglefowl and an Indian subspecies of Red junglefowl: ‘Recently, […] molecular data also show that Indian Red junglefowl (G. g. murghi) also contributes to the domestication’ (Sawai et al., 2010).
The wide distribution of this hybrid form may be tempting to assume also a hybrid origin of domestic chicken. However, the ancient Sussex breed, though their large lightly tinted tan eggs might still suggest Gray junglefowl influences, also has white legs and skin in every variety. Brahmas, one of the largest breeds of chicken having fully feathered, white legs, derive from Shanghai, China. Such breeds far outside the range of red junglefowl tend to corroborate to the evidence that on a world-wide scale yellow legged hybrids were not part of the oldest introduction of domesticated chicken, or that successive waves of hybrids introduced different expressions of a hybrid nature.
How come early hybridization of domestic stock still receives so little attention? Faunal interference before the successful Neolithic domestication events may be deduced from biogeographic evidence. Some animals are thought to have translocated by humans already in prehistoric times. For instance, the natural range of Asian wild dogs (or Dholes) may reached much further than nowadays, still genetic evidence also insinuates a human role in their current distribution:
the grouping of Sumatran and Javan haplotypes with those from India (south of the Ganges) and Myanmar, as opposed to those from Malaysia and Thailand, should be noted.
Further studies are required to clarify these results but in the absence of alternative explanations, these results may be suggestive of human translocation of dholes from one of these regions into Sumatra and/or Java. But since there is no documented evidence for such translocation(s), and given that dholes have been long considered vermin (and not hunted for sport, cf. red fox introductions to Australasia), this hypothesis must remain highly speculative (Iyengard et al., 2005)
At least the genetic results of Brown’s team (2011) cited above into the direction of Dhole or other admixture in domestic dogs was hastily swept under the carpet, when they found the novel Y-chromosome haplotype 12 that besides being recognized as ‘ancestral’ was also shared by Dhole, black-backed jackal, and a wolf from China. The Dhole (Cuon alpinus), also called the Asiatic wild dog, red dog, red wolf, or whistling dog, was widespread across North America, Europe and Asia during the Pleistocene. The species’ range, however, became restricted to Asia after the late Pleistocene mass extinctions c. 12 000–18 000 bp, when it became extinct across North America and Europe, along with several other large species such as mammoths and dire wolves. Like the African wild dog, they have the same number of 78 chromosomes like dogs, as do wolves, coyote and the golden jackal. However, hybridization with any of them has been attempted nor recorded. In appearance Dholes are not unlike shepherd dogs, that purportedly resemble Pleistocene dogs most:
In the PCA and DFA plots, the Palaeolithic dogs are situated near the Central Asian Shepherd dog, which was assigned in the DFA to the prehistoric dog group. This suggests that their skull shape resembles that of the latter breed which was originally used as a flock guardian and as a protector against predators such as bears, striped hyenas and wolves (Labunsky, 1994). The latter property in a dog could also have been useful for Palaeolithic people (Germonpré et al., 2009)
More features of modern dogs are intermediate between Dholes and wolves. Female dogs have 8 to 12 teats, while wolves have only 4 to 8. Female Dholes are on the other end of the spectrum having 12 to 14 teats rather than 10.
Dholes can be recognized in the fossil record by their reduced number of teeth: 40 instead of 42, due a missing molar (M3) in the lower jaw: 220.127.116.11/18.104.22.168, against dogs: 22.214.171.124/126.96.36.199. However, the number of teeth for dogs is known to vary, and in his thesis Datema (2011) uses two reference cranials of dog (Canis lupus familiaris) with exactly this Dhole-like dental formula to investigate whether some dog-like remains recently fished up from the bottom of the North Sea (Southern Bight) really belonged to Pleistocene dogs or rather to “Cuon alpinus”. Was the Dhole indeed a member of the Mammoth Steppe Fauna?
One of Datema’s fossil Canidae specimen, labeled NMR90, was suspected to belong to Cuon alpinus. In this sample M3 is missing, like in Dholes. However, at least with respect to mandible lengths a-b and c-b this specimen was rather intermediate between wolf and Dhole and most similar to dogs:
NMR90, a recently found posterior half of an extremely small jaw (with P4 and M1) of estimated Late Pleistocene age) is suspected, due to its apparent small size and dental formula, that it most probably belongs to neither wolf nor dog (nor fox, which is considerably smaller), but to Cuon alpinus
The specimen range of NMR90 falls entirely outside [below] the population range of C. l. lupus and also entirely outside [above] the population range of Cuon alpinus, but well within the range of C. l. familiaris for a-b (table 4.2 and fig. 4.2). For c-b the specimen range of NMR90 falls entirely outside [above] the population range of Cuon alpinus, entirely within the C. l. familiaris range and overlaps slightly (1.36 mm) with the C. l. lupus population range, although most of the specimen range of NMR90 (2.75 mm) falls outside [below] the C. l. lupus range. (Datema, 2011)
Even though the sample was ultimately classified as a Dutch Dhole from the Southern Bight, this comparative study reveals how tentative such results may be. On the contrary, it has all appearance that Pleistocene dogs represented much more than an aberrant species of wolf. They were close relatives to the ice age ecomorph and probably all other Holarctic Pleistocene wolves that couldn’t resist the ‘human kiss of death’, and ‘hence’ became utterly outcompeted by an aggressive new type of wolf from the south that could. And Pleistocene dogs, embraced by the eerie love of humans, might have diverged even further for being purposely hybridized from the start!
Indeed, hybridization is one of the first recorded obsessions of modern humans. The famous Aurignacian “Venus and the Sorcerer” rock painting in Chauvet cave, Ardeche, already depicts the cross-species mating of an anthropomorphic steppe bison and a female lion, sexually united by a black female pubic triangle. Bull-related fertility and the procreation of hybrid monsters remained a recurrent theme in mythology up to the Greek Minotaur and the Frankish Quinotaur. There could be more. When the Sumerian Enkidu killed the Bull of Heaven, and hence was doomed to die, his friend Gilgamesh was in great grief and swore: “I will wander through the wilderness in the skin of a lion”. We might think this was a strange way to please the gods, though Chauvet Cave would suggest a rich mythology preceding Gilgamesh being based on this bond between species. We can’t dismiss this genuine fascination of early modern humans as purely theoretical. Actually, even the huge body of mythological themes related to shapeshifting has all appearance to be closely connected to an early human fascination for cross-breeding. We simply can’t exclude the possibility that hybridization experiments were already attempted long before the Neolithic.
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With the attestation of Neanderthal and Denisova DNA in the human genome, and strong indications for the genetic contribution of also other archaic hominines previously considered ‘extinct without issue’, the simple model of prefabricated, homogenous modern humans that moved ‘out-of-Africa’ to replace the human evolutionary residue all over the world in a single blow, failed dramatically. Now, the scientific community is literally forced to pay attention to decades of accumulated counter-evidence and criticism.
One issue concerns the implied range expansions of a single ‘bottlenecked’, homogenous population that extended its African habitat to entirely new environments and climates. This should have been attested by selective sweeps in the genome – but it doesn’t.
While most people assumed that the out-of-Africa expansion had been characterized by a series of adaptations to new environments leading to recurrent selective sweeps, our genome actually contains little trace of recent complete sweeps and the genetic differentiation of human population has been very progressive over time, probably without major adaptive episodes.
[…] if some introgressed genes were really advantageous, they should have spread and fixed in the human population, but […] there is no widespread signature of strong selective sweeps in Eurasia. (Alves et al., 2012)
Selective sweep can be recognized by a large reduction of genetic variation near a favorable gene on the chromosome, caused by a quick expansion within a population of the gene by natural selection. Only a few complete sweeps and near-complete sweeps could be found, ‘suggesting that there was relatively little directional adaptive evolution associated with the “origin of modern humans.” Measuring by genetic change, agriculture was many times more important than the appearance of modern humans throughout the world’ (Hawks, 2012-07-20). Does this imply that genetic change of modern humans was predominantly not the result of sudden adaptive mutations? Possibly humans acquired their genetic adaptations to their respective extant environments in a different way:
[…] there are precious few genetic changes shared by all (or even most) humans today, that are not also shared with Neandertals, Denisovans, or plausible other archaic human groups (such as archaic Africans).
That of course follows from the fact that a fraction of today’s gene pool actually comes from those ancient groups. Their variation is (by and large) human variation. (Hawks, 2012-07-20)
Apparently, there was a host of archaic hominines out there, previously considered the evolutionary ‘dead ends’ from all over the world, whose traces can still be perceived as superimposed variability in the modern human genome. That is, up to now investigation on archaic admixture is mainly focused on the differences between modern populations, that increasingly emerge as the relicts of intense ‘archaic’ hybridization processes. ‘Neandertals and Denisovans fall within the variation observed for human nuclear sequences. Thus, only few fixed differences can be identified’ (Meyer et al., 2012). This way, out of 3.2 billion sequenced Neanderthal base pairs only about 600 Mb could be unambiguously attributed to Neanderthal introgression, what is low in comparison with Meyer’s estimation that 6.0% of the genomes of present-day Papuans derive from Denisovans. But, archaic hominines also shared a considerable genetic common denominator with modern humans, whose possible incorporation remains poorly analyzed. A variable portion of archaic DNA actually being shared with modern humans could affect the observed magnitude of introgression, but earlier assertions that Denisovans were indeed more divergent were never confirmed. Without clear traces of selective sweep, the true origin of ambiguously shared and distinctly archaic portions of the genome are impossible to tell apart. Reported examples of selective sweep remain rare:
We also identify over 100 Neandertal-derived alleles that are likely to have been the target of selection since introgression. One of these has a frequency of about 85% in Europe and overlaps CLOCK, a key gene in Circadian function in mammals. This gene has been found in other selection scans in Eurasian populations, but has never before been linked to Neandertal gene flow. (Sankararaman et al., 2012)
The circadian function refers to a chrono-biological adjustment to an external rhythm like daylight, what logically implies a genetic adaptation to the northern Neanderthal habitat with an exclusive advantage for northern populations. Such an introgressed innovation that apparently behaves like a new favorable mutation remains an exception, since hybrid incorporation and repatterning of whole chunks of introgressed DNA doesn’t require selective sweep.
These days many investigators try to reconstruct the past demography in their own way, though often the effort remains haunted by some remarkably conservative out-of-Africa assumptions. A wealth of newly published information on the subject is currently waiting for a proper interpretation to close the gap between our modern genome and the sequenced data retrieved from some of our ancestors. Conflicting perspectives often result in contradictory assertions that may be counter-intuitive and in need of reconciliation one with the other. The following investigation belongs to this category:
Science DOI: 10.1126/science.1224344
Meyer et al. – A High-Coverage Genome Sequence from an Archaic Denisovan Individual, 2012, link
We present a DNA library preparation method that has allowed us to reconstruct a high-coverage (30X) genome sequence of a Denisovan, an extinct relative of Neandertals. The quality of this genome allows a direct estimation of Denisovan heterozygosity, indicating that genetic diversity in these archaic hominines was extremely low. It also allows tentative dating of the specimen on the basis of “missing evolution” in its genome, detailed measurements of Denisovan and Neandertal admixture into present-day human populations, and the generation of a near-complete catalog of genetic changes that swept to high frequency in modern humans since their divergence from Denisovans.
This study has several interesting results worth mentioning: an extremely low genetic diversity of Denisova humans that can’t be observed in any modern population; the observation that Europeans have 24% less Neanderthal admixtures (“not being shared by Africans”) than Asians; and apparent indications of some hybridization event in the past, still noticeable in the chromosomes of all modern Denisovan descendents.
Low genetic diversity of Denisovans puts the asserted homogeneity of the modern human species in a new perspective. Despite all earlier speculation on an African bottleneck, designed to explain modern genetic homogeneity from a phylogenetic perspective, current genetic variability is now found to exceed the attested variability of ancient Denisovans for all modern ‘phyles’, or ethnicities:
Several methods indicate that the Denisovan hetero-zygosity is about 0.022%. This is ~20% of the heterozygosity seen in the Africans, ~26–33% of that in the Eurasians, and 36% of that in the Karitiana, a South American population with extremely low heterozygosity. Since we find no evidence for unusually long stretches of homozygosity in the Denisovan genome, this is not due to inbreeding among the immediate ancestors of the Denisovan individual. We thus conclude that genetic diversity of the population to which the Denisovan individual belonged was very low compared to present-day humans. (Meyer et al., 2012)
Nevertheless, Denisovans lack any relevant African affiliation. Their ‘phyle’ should have been separated long enough from the other branches of human evolution to have reached a genetic diversity comparable to Africans. Apparently, since this didn’t happen, genetic variability doesn’t simply translate to the age of an otherwise isolated population. Investigators may now dedicate their diligence to duplicate their calculations for a purported recent African bottleneck, and design a corresponding recent Denisovan bottleneck. Or they could just admit the geographic maxima of modern variability in Africa may rather represent archaic admixture than the age of a single human phyle.
Unfortunately, the Meyer study doesn’t mention the Neanderthal-like admixtures of Africans, except by saying that the ‘genetic contribution from Neandertal to the present-day human gene pool is present in all populations outside Africa’. It is important to keep this voluntary restriction in mind in reading their most remarkable assertion: ‘We estimate that the proportion of Neandertal ancestry in Europe is 24% lower than in eastern Asia and South America’ (Meyer et al., 2012).
This runs contrary to more detailed genetic analyses that previously revealed slightly higher levels of Neanderthal admixture in Europe. John Hawks counted derived SNP alleles of the 1000 Genomes Project being shared with the (Neanderthal) Vindija Vi33.16 genome, and found the surpluses in Europe and East Asia where rather comparable:
The Europeans average a bit more Neandertal than Asians. The within-population differences between individuals are large, and constitute noise as far as our comparisons between populations are concerned. At present, we can take as a hypothesis that Europeans have more Neandertal ancestry than Asians. If this is true, we can further guess that Europeans may have mixed with Neandertals as they moved into Europe, constituting a second process of population mixture beyond that shared by European and Asian ancestors. (Hawks, 2012-02-08 )
Unfortunately, the attested agreement between non-African and Neandertal genomes, and between Melanesian and Denisova genomes for that matter, didn’t result yet in the full identification of all specific genetic loci involved. Basically, the observed agreement was initially based on the differences between Africans and non-Africans in comparison with the archaic genome being investigated. Hence, the overall picture of archaic ‘differences’ may be distorted by shared components within the African reference group, that Meyer’s team didn’t include in their investigation and that Hawks didn’t quantify for his modern genomes that share derived SNP alleles with the (Neanderthal) Vindija Vi33.16 genome. In other words, this Neanderthal ancestry in Europe allegedly being 24% lower than Asia (according to Meyer et al.) is essentially meaningless without additional information that quantifies sharing:
My initial reaction to this difference is that it reflects the sharing of Neandertal genes in Africa. Meyer and colleagues filtered out alleles found in Africa, as a way of decreasing the effect of incomplete lineage sorting compared to introgression in their comparison. But if Africans have some gene flow from Neandertals, eliminating alleles found in Africans will create a bias in the comparison. If (as we think) some African populations have Neandertal gene flow, that probably came from West Asia or southern Europe. So as long as the present European and Asian (and Native American) samples have undergone a history of genetic drift, or if (as mentioned in the quote) they mixed with slightly different Neandertal populations, this bias will tend to make Asians look more Neandertal and Europeans less so.
Anyway, this demands further investigation. (Hawks, 2012-08-30)
Apparently, the legacy of the Out-of-Africa dogma caused Meyer et al. to take the African part for granted and just to look at the non-African part. We are lucky to have some additional information already at hand to more or less visualize how the Meyer et al. results could still be in tune with earlier results, that rather emphasized a closer match of Neanderthal admixtures with Europeans. The Austrian study of Hochreiter et al. (2012) actively incorporates the internationally shared Neanderthal and Denisova alleles in their calculations to measure the probability of uneven distribution (Fisher’s exact test) and to obtain the corresponding odds ratios, that give a symmetrical representation of the relative genetic enrichment for each type of admixture. From here on, all depends on how we perceive the human genome and what part of it we are willing to recognize as true Neanderthal or Denisova admixture, or something else.
Hochreiter’s study retrieved data from the Korean Personal Genome Project (KPGP) combined with those from the 1000-Genomes-Project:
Genotyping […] 1,131 individuals and 3.1 million single nucleotide variants (SNVs) on chromosome 1 […] identified 113,963 different rare haplotype clusters marked by tagSNVs that have a minor allele frequency of 5% or less. The rare haplotype clusters comprise 680,904 SNVs; that is 36.1% of the rare variants and 21.5% of all variants. The vast majority of 107,473 haplotype clusters contains Africans, while only 9,554 and 6,933 contain Europeans and Asians, respectively. (Hochreiter et al., 2012)
According to this data, only 6,490 (113,963 minus 107,473) of the rare haplotype clusters on chromosome 1 were exclusively non-African. The vast majority of all rare haplotypes, however, are shared with Africans one way or the other:
We characterized haplotypes by matching with archaic genomes. Haplotypes that match the Denisova or the Neandertal genome are significantly more often observed in Asians and Europeans. Interestingly, haplotypes matching the Denisova or the Neandertal genome are also found, in some cases exclusively, in Africans. Our findings indicate that the majority of rare haplotypes from chromosome 1 are ancient and are from times before humans migrated out of Africa. (Hochreiter et al., 2012)
The 9,554 and 6,933 European and Asian haplotypes thus per definition include a considerable overlap with extant African rare haplotypes. Moreover, the size of such an African overlap is proportional with the total count of shared Eurasian haplotypes. Mathematically it could be deduced that at the very least, 3,064 (ie. 9,554 minus 6,490) out of 9,554 ‘European’ haplotypes, and 443 out of 6,933 ‘Asian’ haplotypes should be also African. The maximum count of African rare haplotypes, however, that made it ‘Out-of Africa’ and are currently shared with non-Africans, remained well below 10%. Since over 90% of the African rare haplotypes are thus not shared with Neanderthals and Denisovans, in an Out-of-Africa scenario this would mean that a similar proportion of the European and Asian rare haplotypes could be expected to be non-Neanderthal and non-Denisova. Could we really rely on the ancestral origin of so many shared haplotypes? Just being shared African doesn’t make these haplotypes ancestral all of a sudden, and less without a proper quantification.
Let’s first try to quantify the potential Neanderthal admixtures a bit. Hu’s analyses of archaic segments should give an adequate peek inside the various admixtures for an educated guess:
Archaic hominin admixture with modern non-Africans was detected by genome wide analysis of Neanderthal and Denisovan individuals.
To gain better understanding in demographic and evolutionary significance of archaic hominin admixture, […] we identified 410,683 archaic segments in 909 non-African individuals with averaged segment length 83,460bp. In the genealogy of each archaic segment with Neanderthal, Denisovan, African and chimpanzee segments, 77~81% archaic segment coalesced first with Neanderthal, 4~8% coalesced first with Denisovan, and 14% coalesced first with neither (Hu et al., 2012)
Considering the above, apparently very few (or none?) of all the non-archaic haplotypes that made it out of Africa became rare. Such results, naturally, would imply one enormous problem about the construct Homo Sapiens Sapiens (HSS). Instead, the lack of rare haplotypes outside Africa that could be safely assigned unambiguously to what is generally considered the constituent forerunner of modern humans, indeed echoes much earlier claims of ancestral homogeneity. As already referred to above, population geneticist are very much acquainted with the concept of an early HSS bottleneck, since this was once designed to explain away all evidence of this kind. Hence, I appreciate the reasons why Hochreiter et al. prefer to consider the rare Denisova- and Neanderthal-like rare haplotypes in Africa ‘ancestral’, even those being exclusively African, but this preposition logically implies the existence of allegedly HSS ancestral haplotypes in Eurasia that are neither rare nor absent in Neanderthal and Denisova. Combined with the ever more unpopperian association of frequent haplotypes with HSS per definition, it has now all appearance Homo Sapiens Sapiens is nothing but the current genetic common denominator in disguise.
As for now, apparently the Neanderthal admixtures indeed account for the greater part of the Eurasian archaic components. The discovery of the Denisova component was just mere luck, and the odds are high that more archaic hominines contributed to the Eurasian admixtures. For all we know, on the eve of the transition to modern humans Europe was only inhabited by Neanderthal. However, the likelihood of additional archaic admixture in South East Asia are being widely discussed. Moreover, Hu’s results almost exclude the possibility that substantial African archaic admixtures, at least those not yet being fully incorporated in the ‘bottlenecked’ HSS population, expanded out of Africa. Altogether, it wouldn’t be farfetched to consider most of the 14% Eurasian remainder to be essentially archaic Asian. Actually, Hu’s 14% Eurasian admixtures currently unaccounted for could easily correspond to the genetic contribution of up to four Asian archaic hominines like Denisovan’s – wherever those may have existed in isolation from Denisovan-like populations that – as for now – potentially inhabited the large geographic stretch between their attested remains in the Altai mountains and their attested genetic contributions in Melanesia. Mendez et al. (2012) suggested ‘that the archaic ancestor contributing the deep lineage to Melanesians and the specimen from Denisova were members of genetically differentiated populations’, what indeed should make us wonder about the Asian location, or nature, of such unsampled hominine groups we are still missing from the record of potential archaic admixtures. Even locally admixted homo erectus have already been proposed.
Now, Hu’s fixed non-Neanderthal-non-Denisovan remainder and the ambiguous 4% apparently shared component between both sampled hominines, suggest ~40-50% ancestral overlap between Neanderthals and Denisovans for the admixtures attributed to Denisovans, against only ~4-5% ancestral overlap for Neanderthal-like admixtures. The unambiguous Denisovan component left may be considered fully Asian in origin, even though Meyer et al report an opposite effect on the current availability of Denisovan alleles all over the world:
Interestingly, we find that Denisovans share more alleles with the three populations from eastern Asia and South America (Dai, Han, and Karitiana) than with the two European populations (French and Sardinian) (Z = 5.3). However, this does not appear to be due to Denisovan gene flow into the ancestors of present-day Asians, since the excess archaic material is more closely related to Neandertals than to Denisovans (Meyer et al., 2012)
Indeed, the contribution from Denisovans is found ‘almost’ exclusively in island Southeast Asia and Oceania. Hence, Meyer’s assumption this effect is directly related to a higher proportion of archaic Neanderthal alleles in Asia justifies a ‘worse case’ scenario, where the ‘true’ Asian share could probably increase to 18-19%, against up to 81% rare archaic haplotypes that could now be tentatively attributed to essentially Eurasian Neanderthal admixtures. For now we are only interested in the counts of Neanderthal-like admixtures, so we could propose a conversion of Hochreiter’s rare haplotype counts results, that reduces the non-African count of rare haplotypes to ~5,224 Neanderthal non-African haplotypes, and that reduces the ‘non-exclusive Asian’ haplotypes to ~5,581 Neanderthal non-exclusive Asian haplotypes, while the same maximum of Hochreiter’s 9,554 haplotypes could still be assumed to be both ‘Neanderthal’ and ‘non-exclusive European’.
For sure, such an increased proportion for Neanderthal-like admixtures in Europe doesn’t make Meyer’s results more intuitive. All the contrary, Meyer’s 24% lower European contribution should make us wonder where the differences went to. Apparently, a changed proportion of non-African Neanderthal-like admixtures in Europe compared to Asia needs proportional compensation elsewhere. Unfortunately, this effect has not been illustrated in any of the studies that aim to quantify Neanderthal admixtures one way or the other.
For a better comprehension I elaborated several possible solutions, combining the information of Hochreiter, Meyer and Hu. Hochreiter supplied values for three linear equations that involve six variables, representing the rare haplotype counts characterized as ‘exclusive European’, ‘exclusive Asian’, ‘Eurasian’, ‘Afro-Asian’, ‘Afro-European’ and ‘Afro-Eurasian’ . Meyer’s published proportion between European and Asian haplotypes introduces a fourth equation, that for comparison could be alternated with a more intuitive scenario that has non-African European and Asian rare haplotypes evenly distributed. However, a set of linear equations may only be solved (but not necessarily) if the number of equations is the same as the number of variables. Thus two variables remain undefined, what means that an array of solutions is still possible. I worked out a number of different scenarios, each based on two additional assumptions that are necessary to solve the equations. Thus, for scenario #1 I choose zero values for the Eurasian and Afro-Asian components; for scenario #2 I choose zero values for the Eurasian and Afro-Eurasian components; for scenario #3 I kept the Eurasian and Afro-European components on zero; for scenario #4 the same for the Afro-Asian and Afro-Eurasian components; for scenario #5 the Afro-European and Afro-Eurasian components were kept zero; for scenario #6 the same for the Afro-European and Afro-Asian components; and for scenario #7 zero values were assumed for the Afro-Eurasian and European component, the latter being valid only for the Meyer variant of the equations.
Scenarios #3-5 can’t be solved for natural values and scenario #6 is ambiguous. The remaining scenarios #1, #2 and #7 all show the predominance of shared Afro-European rare haplotypes, while Afro-Asian, Eurasian and Afro-Eurasian components are lower and not always required for a valid result. The effect of Meyer’s result can be illustrated for scenarios #1 and #2, where lower Neanderthal-like proportions for Europe in comparison with Asian apparently imply a higher count for shared Afro-European haplotypes and lower counts for Afro-Asian and Afro-Eurasian haplotypes.
These scenarios reveal the Afro-Asian component as fairly irrelevant, and the Afro-Eurasian component emerges as moderately weak. Only the Afro-European component remains definitely prominent in all scenarios. Remarkably, simulations that increase the Eurasian shared component are directly proportional to increases of the Afro-European component, while both are inversely proportional to the Afro-Eurasian component. This behavior supports the hypotheses that the Afro-Eurasian shared component is only moderately present; that at least the Asian Neanderthal admixtures don’t share any African origin or association in particular; and that Neanderthal haplotypes rather seem to have expanded proportionally into Africa and Asia alike from a European center. Especially the increased Afro-European component is remarkable, since an ancestral origin results problematic for rare haplogroups that feature a structural deficit in Asia.
At this stage it is impossible altogether to distinguish between haplotypes that introgressed through Neanderthal admixtures and those that may be ‘safely’ regarded ancestral to both Neanderthal and modern humans – so we should refrain from doing so beforehand. How ancestral the shared African haplotypes could possibly be? African substructure is no longer viable as a major explanation of Neanderthal admixtures in Eurasia. Actually, African substructure was already contradictory with the earlier Out-of-Africa bottleneck-and-homogeneity paradigms, and an additional west-to-east substructure to explain essentially different admixture patterns for Europe and Asia, is even less conceivable. Instead, ‘recent admixture with Neanderthals accounts for the greater similarity of Neanderthals to non-Africans than Africans’ (Yang et al., 2012). Less exclusive scenarios, that allow for early admixture events in the ancient Near Eastern contact zone, aren’t any less problematic for the discrepancy and leave the much lower Afro-Asian component without explanation. The most progressive and intuitive Out-of-Africa scenario, that considers the predominantly European distribution of Neanderthal haplotypes and predicts an increased admixture rate in Europe, now results falsified by this closer examination of Meyer’s 24% lower European rate. Apparently, the current distribution of admixtures only appeared to be in favor of any overall Out-of-Africa framework. The apparent lack of shared Afro-Asian haplotypes doesn’t indicate an African route for Asian admixtures, nor does the low count of shared Afro-Eurasian haplotypes advocate the importance of an ancestral component. Instead, an underpinning West-East dichotomy or Eurasian substructure already in place for the Neanderthal population before the attested admixture has already been proposed as a valid explanation:
Europeans and Asians could show distinct components of Neanderthal admixture if they had admixed with European and central Asian Neanderthals, respectively (Alves et al., 201)
The Afro-European shared haplotypes can’t be older than the long term genetic differentiation of Eurasian Neanderthals, what adds up to the already expounded rejection of African substructure in a recent Out-of-Africa scenario. A better explanation may be found in a massive expansion (or ‘backmigration’) of European populations into Africa, and a corresponding submersal of almost their full share of Neanderthal admixtures inside Africa subsequent to some late-Neanderthal admixture event.
Now the falsification of an important shared ancestral compenent in the African count of rare haplotypes becomes evident, Hochreiter’s data, reporting that ‘haplotypes matching the Denisova or the Neandertal genome are also found, in some cases exclusively, in Africans’, may be viewed in an entirely new perspective. If introgression of Denisovan admixtures was part of a rather ancient gene flow, albeit considerably younger than the Eurasian Neanderthal differentiation still noticeable in the strongly regionalized Neanderthal admixtures, some Denisovan alleles could have reached Africa contemporaneously with the ‘other’ archaic admixtures that arrived there through the European route, as displayed by the calculated haplotypes pattern above. Especially the world-wide distribution of shared Neanderthal-Denisova alleles raises some questions into this direction.
More detailed analysis on the immune gene OAS1, involved in ‘Denisovan’ introgression, revealed this gene was embedded in a very divergent string of DNA, referred at as the ‘deep lineage’ haplotype. Its divergence from all the other extant OAS1-related haplotypes was strong enough to exhibit the signature of archaic introgression, what means the haplotype ‘may have introgressed into the common ancestor of Denisova and Melanesians via admixture with an unsampled hominin group, such as Homo erectus’ (Mendez et al., 2012). The haplotype resembles the Denisovan haplotype ‘with the exception of one site (position 30504), at which the extant human carries the derived C and the Denisova specimen carries the ancestral T’, but even more striking is the current homogeneity of the deep lineage:
Broadly distributed throughout Melanesia, the deep lineage exhibits very low intraallelic diversity […], with an estimated TMRCA of ~25 kya (Mendez et al, 2012)
The attested Denisovan fossils in the Altai mountains had a slightly more ‘ancestral’ version of the gene, thus being different from the extant ‘deep lineage’. Actually, this unique signature boils down to a single hybridization event for this haplotype that involved one ancestral parent not unlike, but slightly different from the sampled specimen of Denisova Cave. Also Meyer’s observation that ‘Papuans share more alleles with the Denisovan genome on the autosomes than on the X chromosome’ and that eg. on chromosome 11 Denisovan ancestry is estimated to be lower in Papuans than in East Eurasians, corroborate to this hypothesis:
[…] there is significant variability in Denisovan ancestry proportion compared with the genome-wide average not just on chromosome X, but also on individual autosomes that have estimates that are also lower (or higher) than the genomewide average. (Meyer et al., 2012 sup)
Unfortunately, despite the negative evidence accumulated by Meyer et al. in their supplement against their own sex-biased modern population-history pet theories, their main article stopped short of dwelling on far more interesting factors such as hybrid chromosome repatterning that include ‘natural selection against hybrid incompatibility alleles, which are known to be concentrated on chromosome X’ and a marked uneven distribution of Denisovan ancestry also in the autosomes.
The disproportionate absence of Denisovan admixtures on the X chromosome virtually excludes a sex-biased demographic history in Oceania as an explanation and indeed, in their supplement Meyer et al. elaborated a potential rejection on logical grounds: also migrating males bring in their share of X chromosomes, so this way it can’t just disappear. A removal of Denisovan chromosome X by natural selection after the gene flow can be excluded as well: selection acting on genomic functional elements can be detected by its indirect effects on population diversity at linked neutral sites (McVickers et al., 2009), but Meyer’s team was right that they couldn’t establish that archaic ancestry was affected by the proximity to genes. However, natural selection against hybrid incompatibility alleles is still a poorly understood process – and especially if considered applicable just to the protein coding genes that constitute only about 3 percent of the human genome. This year the ENCODE Project Consortium confirmed actually over 80% of the genome to be involved in biochemical functions, in particular outside of the protein-coding regions. Genetic viability is most of all determined by the proper regulation of gene expression. Hence, much of the genome is considered constrained by biological constraints against evolutionary change. Of interest are the ‘large number of elements without mammalian constraint, between 17% and 90% for transcription-factor-binding regions as well as DHSs and FAIRE regions’ (Dunham et al., 2012), referring to regions linked to regulatory functions. But even here, the autors hold that depressed derived allele frequencies indicate ‘an appreciable proportion of the unconstrained elements are lineage-specific elements required for organismal function, consistent with long-standing views of recent evolution’.
It should be obvious that nature can’t expect much viable offspring from a fusion of gametes that brings together lineage specific regulatory regions in a random fashion. The deleterious effects of random hybrid recombination appear to be inversely proportional to chromosome crossover events during meiosis, that normally happens once for each generation. First generation hybrid offspring typically has enough directly inherited consistency of their regulatory regions on their genome left for being viable. But next generation chromosome crossover may already affect the regulatory processes of the haploid gametes being produced by meiosis. Initially, this seriously affects fertility and only the sheer scale of gamete production may compensate for the high probability of next-generation hybrid malfunction. This close relation between hybrid viability and a limited array of favorable crossover events, that shouldn’t compromise the regulatory functionality of the hybrid genome, apparently resulted also in a marked variability of ancestry proportions for each chromosome across the genome of Denisovan admixed populations.
For hybrids, selective processes are more efficient when directed at regulatory viability just before and during conception. Post-natal fitness, on the other hand, is most of all based on the ‘proven technology’ of coding genes whose selective advantage and usefulness were already attested in the parent species. Natural selection based on the success of coding genes thus may have been of less importance in recent hominine evolution than could be expected for the profound genetic change modern humans apparently went through. This detail can indeed be confirmed in the modern genome by the above mentioned lack of genetic sweep, despite important repatterning and recent genetic innovation due exactly to the occurrence of abundant hybridization in recent human evolution.
For the moment this issue should be considered isolated from the origin of the shared Neanderthal-Denisovan haplotypes, especially since this portion was already in place for the sampled Neanderthal and Denisovan specimen. Tentatively, this shared portion could be attributed to an earlier ‘bi-directional’ gene flow, leaving the specific Denisovan admixtures in Melanesia apparently to a subsequent hybridization event that only seems to have affected modern populations. The proposal above of a single hybridization event virtually excludes a scenario where the hybrid population could be considered firmly rooted in a local archaic population. Naturally, this runs counter to an array of earlier proposals that rather link Denisovan admixture events with a wide geographic range of Denisovan hominine presence between the Altai mountains and SE Asia (Reich); with different places during the migration of modern humans (Rasmussen); with distinct Denisovan admixture events in Oceanians and East Asians (Skoglund and Jakobsson); or with a process of continuous admixture where migration routes overlap with archaic hominine ranges (Currat and Excoffier).
However, a single late-Denisovan hybridization event doesn’t suffice as an exclusive scenario in the light of new evidence that posits Denisova Cave as a hotbed of Neanderthal contact. Abundant remains of Neanderthal were found nearby the cave:
The Chagyrskaya 6 mandible […] allows us now to link this material morphologically as well to the Neanderthals in Western Eurasia. Several questions remain: the timing and extent of Neanderthal expansion into the Altai, and especially the potential coexistence and interaction between Neanderthals and Denisovans. Based on availabe dates, the Neanderthals in Okladnikov cave and the possibly slightly earlier Chagyrskaya remains overlap with the wide range of dates for Layer 11 of Denisova cave. (Viola et al., 2012)
Both species even shared the same cave:
we have determined a high-quality nuclear genome from a pedal phalanx found in Denisova Cave in 2010. We show that the pedal phalanx derived from a Neandertal and thus that Neandertals as well as Denisovans have been present in the cave. (Sawyer et al., 2012)
Extensive contacts should at least have initiated a kind of fusion between the Neanderthal and Denisovan parent species into a single population where in time, due to multiple hybridization events, the variability of introgressed DNA would have been restored and integrated, into the Neanderthal genetic heritage and vice-versa. Hybrid repattering of admixed chromosomes probably wouldn’t have raised Denisovan heterozygosity beyond the elevated levels observed in modern populations, and less given the outstanding native homozygosity of the sampled Denisovans as a starting point. Indeed, the Denisovan sample has a reduced heterozygosity compared to any of the present-day humans analyzed by Meyer et al, though they reported the relative ratios of heterozygosity as fairly constant, what could be considered problematic for the assumption of archaic Neanderthal admixture already present in the shared DNA with Denisovans. However, 29 coding CCDS genes could be identified with more than one fixed non-synonymous SNC where ‘Denisova’ carries the ancestral allele, while in eight of these (OR2H1, MUC17, TNFRSF10D, MUC6, MUC5B, OR4A16, OR9G1, ERCC5), the Denisovan individual appeared heterozygous for all SNCs present in the gene. In table S44 it can be verified that 37% of this heterozygosity can be found in chromosome 11, 13% in chromosomes 6 and 7, and 11% in chromosome 8, while eleven chromosomes are homozygous for all investigated genes. Though Meyer’s team proposes this to be the result of duplications or repetitive regions, this heteromorph signature basically leaves the possibility of hybridization more than open. Since this results focus on the fixed non-synonymous SNC where Denisova carries the ancestral allele and modern humans the derived allele, the documented non-ancestral polymorphisms of Denisova even resemble modern-like admixtures.
According to Dienekes, within the group of polymorphic Eurasian SNPs there are less Denisovan than Neanderthal SNPs that are also monomorphic in the African Mbuti Pygmys. Because, actually the relation between Denisovans and Pygmy is ancestral and they share ancestral SNPs. This might reflect a lower penetration into Africa of the shared Denisovan-Neanderthal portion of archaic admixtures. If so, this could be partly due to a Denisovan origin of this shared portion, though some degree of Eurasian Neanderthal substructure may be involved as well. Interestingly, this also implies the tentative modern-like part of potentially admixtured (ie. polymorphic) SNPs in the Denisovan genome is actually less ‘African’ than the Out-of-Africa hypothesis should be happy with. If anything, despite some modern-like features, those admixtures should be assumed of eastern Neanderthal origin.
Another modern-like feature of the potential Denisovan-Neanderthal hybridization is the above mentioned outstanding heterozygosity of chromosome 11, that almost screams for continuity with the hybrid signature of the same chromosome in Papuans, where Denisovan ancestry is strikingly low. I really wonder what could have been the impact of these hybrid changes for the now widespread Denisovan-like mtDNA segment inserted into this same chromosome 11 of modern human populations all over the world, as described in a previous post; and what could have been the link with the survival of insert-like mtDNA in the aboriginal DNA found in the Lake Mungo 3 remains (LM3) dated 40kya. But even a much lesser extend of any gradual continuation with respect to Denisova-related selective processes against hybrid incompatibility alleles would only make sense if modern populations are themselves the continuation of these same ancient hybridization processes. Apart from what this might imply for the very nature of the modern genome in general, we could at least incorporate this signature of a continuous hybridization process, that tentatively links the Altai Mountains with Oceania, in what we know about the current distribution of Denisovan admixtures. A northern route around the SE Asiatic habitat of probably very different archaic hominine populations, some of them possibly more erectus-like or even more habilis-like, such as Homo floresiensis (Argue et al., 2012), seems at present more likely than a straightforward direct southern route:
However, in contrast to a recent study proposing more allele sharing between Denisova and populations from southern China, such as the Dai, than with populations from northern China, such as the Han, we find less Denisovan allele sharing with the Dai than with the Han (Meyer et al., 2012)
Current evidence even seems to favor a specific Korean route before turning south along the Chinese coasts down to Oceania:
The enrichment of Neandertal haplotypes in Koreans (odds ratio 10.6 of Fisher’s exact test) is not as high as for Han Chinese from Beijing, Han Chinese from South, and Japanese (odds ratios 23.9, 19.1, 22.7 of Fisher’s exact test) – see also Figure 7. In contrast to these results, the enrichment of Denisova haplotypes in Koreans (odds ratio 36.7 of Fisher’s exact test) is is higher than for Han Chinese from Beijing, Han Chinese from South, and Japanese (odds ratios 7.6, 6.9, 7.0 of Fisher’s exact test) (hochreiter et al., 2012)
It has been suggested that ancient HLA-A genes of the primate immune system only survived on human chromosome 6 by balanced selection in the Denisovan lineage. Hence, the current geographical distribution of this genes is often taken as indicative for the wherabouts of Denisovan admixed descendents. As you can see on the attached map, the hybrid Denisovan trail described above corresponds fairly well with this view, except for Yunnan and Tibet where possible Denisovan-like admixtures are largely below detection level and certainly not derived from Melanesian arrivals. It can’t be excluded that here we may find the root origin of the archaic population whose remains were so far attested only in Denisova Cave. Interestingly, this hypothetized ultimate origin of the archaic Denisovan population is adjacent to Indo-China, where hominine evolution may have been as old and divergent as in Africa.
Thus, it becomes ever more difficult to identify with, or deny descendance of a particular hominine branch. Recent human evolution is like a snowball rolling down the hill. What we are is just everything what came down from the hill, and what didn’t stop rolling. We may question our ability to really take a turn since for all we know the ball just gathers more snow and increases momentum. We can’t even say our trail downhill was human all the way, or where it started, or define what sets the participants apart from everything else around it. But here we are, something completely new on the face of the earth. And most of it, we have in common.
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