The Antiquity of Man

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Evidence for interbreeding between members of the genus Homo

Dalton, R. 2010. Neanderthals may have interbred with humans

"A genetic analysis of nearly 2,000 people from around the world indicates that such extinct species interbred with the ancestors of modern humans twice, leaving their genes within the DNA of people today.

"The discovery, presented at the annual meeting of the American Association of Physical Anthropologists in Albuquerque, New Mexico, on 17 April, adds important new details to the evolutionary history of the human species. And it may help explain the fate of the Neanderthals, who vanished from the fossil record about 30,000 years ago. "It means Neanderthals didn't completely disappear," says Jeffrey Long, a genetic anthropologist at the University of New Mexico, whose group conducted the analysis. There is a little bit of Neanderthal leftover in almost all humans, he says.

"The researchers arrived at that conclusion by studying genetic data from 1,983 individuals from 99 populations in Africa, Europe, Asia, Oceania and the Americas. Sarah Joyce, a doctoral student working with Long, analyzed 614 microsatellite positions, which are sections of the genome that can be used like fingerprints. She then created an evolutionary tree to explain the observed genetic variation in microsatellites. The best way to explain that variation was if there were two periods of interbreeding between humans and an archaic species, such as Homo neanderthalensis or H. heidelbergensis."

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Wolpoff, M. and Caspari, R. 1997. Race and Human Evolution: A Fatal Attraction. New York: Simon & Schuster.

Pages 296-7

"There is also regional continuity in nonadaptive features. Nonadaptive features can persist after they are established at high frequency, when no evolutionary forces act to change them significantly. Because of their nature, they are very unlikely to persist if the history of a region is marked by population replacements. One of the best arguments for a significant European Neandertal input into the gene pools of later Europeans is the persistence of nonadaptive traits. Features such as the shape of the hole for the mandibular nerve to enter the mandible, or the presence of a small bump on the outer edge of the femur shaft, near its top, are difficult to explain any other way.

"The mandibular foramen, for example, is an opening on the inside of the vertical part of the mandible for the branch of the mandibular nerve that reaches the teeth. This is the uncomfortable spot a dentist tries to reach with a nerve block for the mandibular teeth. in the H-O form the rim of the opening has an oval shape with the long axis of the oval oriented horizontally. Alternatively, in the normal form the rim may be broken, along its lower border, by an unbridged vertical groove. The broken rim of the usual form in living populations.

"The horizontal-oval mandibular foramen is virtually unique to European fossils. It is found in almost no other remains, including Late Pleistocene African and the Skhul/Qafzeh sample, the putative alternative ancestors of the post-Neandertal Europeans. But the horizontal-oval foramen has a significant frequency in the subsequent post-Neandertal populations of Europe and only decreases to rarity in recent Europeans. The exact form of the foramen opening is an example of nonadaptive equivalents. It is important that the foramen be there (the nerve must enter the mandibular body) but it makes absolutely no difference which form its rim has."

Wolpoff & Caspari (pg. 297) give the figures as follows:

European sample H-O frequency Normal foramen frequency
Neandertals 18% 82%
Early Upper Pal. 18% 82%
Late Upper Pal. 7% 93%
Mesolithic 2% 98%
Medieval 1% 99%

The form of the foramen opening is non-adaptive and can take different shapes. Of the observed shapes in the current Neanderthal crania, the horizontal-oval rim shape is slightly in the majority. While the shape can be used to infer that Neandertals contributed genetic material to the Upper Palaeolithic inhabitants of Europe, it cannot be utilised as a determining marker for percentage genetic contribution workings.

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If you haven't already, take a read through Eswaran's December 2002 Current Anthropology article entitled "A Diffusion Wave out of Africa: The Mechanism of the Modern Human Revolution?" He, I believe, provides a working alternative Multiregional hypothesis of modern human origins. The abstract reads:

"This paper proposes that the worldwide transition to an anatomically modern human form was caused by the diffusive spread from Africa of a genotype - a coadapted combination of novel genes - carrying a complex genetic advantage. It is suggested that the movement out of Africa was not a migration but a “diffusion wave”- a continuous expansion of modern populations by small random movements, hybridization, and natural selection favoring the modern genotype. It is proposed that the modern genotype arose in Africa by a shifting-balance process and spread because it was globally advantageous. It is shown that the genotype could have spread by directionally random demic diffusion, but only under conditions involving a low rate of interdeme admixture (“interbreeding”) and strong selection. This mechanism is investigated using a quantitative model that suggests explanations for many puzzling aspects of the genetic, fossil, and archaeological data on modern human origins. The data indicate significant genetic assimilation from archaic human populations into modern ones. A morphological advantage of the modern phenotype - possibly reducing childbirth mortality - is proposed as the cause of the transition. The evidence of this and previous human “revolutions” suggests that the shifting-balance process, proposed by Sewall Wright, was particularly important in human evolution - possibly because human populations had a small-deme social structure with low interbreeding rates that allowed it to operate. This may explain the relative uniqueness of human evolution."

Under a section named "Replacement or Assimilation?", Eswaran writes,

"Not all genetic studies show signs of bottlenecks. For example, proteins, blood groups, and alleles of the major histocompatibility complex (MHC) loci show non-Africans having a genetic diversity comparable to and often greater than that of Africans (Takahata 1995). The presence of numerous ancient alleles at the MHC loci has been interpreted as suggesting that no population bottlenecks may ever have occurred in human and hominoid evolution (Ayala 1995). Other genetic systems too do not carry the bottleneck-and-expansion signature seen in mtDNA and at some other loci. These contrasting indications from different genetic studies need an explanation, particularly because the presence of bottlenecks has been construed as supporting a replacement scenario for the modern transition. I will now show that the dichotomy in the genetic data strongly suggests that assimilation from archaic populations occurred during the modern transition.

"The resolution offered here stems from the observation that, typically, loci with high mutation rates and hence with recent polymorphism show bottlenecks while those with low mutation rates and ancient polymorphism do not. The difference is suggestive because the former would have formed unique regional patterns in hominid populations within a few hundred thousand years, while the latter, in particular the very ancient polymorphisms that predate the genus Homo, would possibly be found across the world population of hominids. The contrasting features of the genetic evidence can be explained in terms of the differing effects of the diffusion wave of modernity on polymorphisms that were global and widespread before the wave in comparison with those that were local to particular regions.

"It is already been argued above that unique African neutral alleles being carried by the diffusion wave front would have developed the typical symptoms of bottlenecked populations, leading to significant allele loss. However, with ancient and widespread polymorphisms there would also have been the possibility of allele replenishment through assimilation from archaic populations, for the same polymorphisms, so to speak, would have been found in both modern and archaic humans. A wave-front population initially identical at these loci to the global archaic populations would have subsequently diverged and shown the effects of bottlenecking only if there were essentially no assimilation at the wave front. Recall that, according to this theory, (1) all assimilation from archaic humans would have occurred only at the wave front, (2) the wave front would have been isolated from the moderns in its rear, and (3) all new modern populations would have been created at the wave front, and therefore any signs of bottlenecking in the wavefront moderns would also have appeared in the emergent populations. Now consider that without assimilation the wave front would have been completely isolated - from the moderns behind it because of its greater speed and from the archaics ahead by the bar on admixture. Under these conditions all neutral polymorphisms, whether local African or widespread, would have been bottlenecked and shown the same symptoms of reduced genetic diversity away from Africa.

"However, such a bottleneck would not have allowed many polymorphisms to survive in the wave front as it spread slowly across the Old World. For example, simulations of a wave-front population of 2,000 individuals tracked through time suggest that only around 4 neutral alleles per locus survive the bottleneck for 4,000 generations if the population has no assimilation. However, with an assimilation rate of merely one individual per generation, from archaics identical at these loci to the initial wave-front population, an average of 40 alleles remain in the wave front. [14] Thus a very considerable diversity could have been passed on to non-African populations even with low (but not zero) rates of assimilation.

"As many loci do show ancient polymorphisms of considerable diversity in non-African populations, this definitely suggests that assimilation did occur at the wave front. Otherwise, genetic diversity would have severely decreased farther from Africa. Assimilation explains why proteins, blood groups, MHC loci, etc., show no signs of an Out-of-Africa bottleneck. Thus, the empirical fact of the absence of bottlenecking [15] in ancient polymorphism implies that assimilation, not replacement, is the best explanation of the genetic data.

"However, given that the genetic evidence also shows a considerable spread of African alleles, which could happen only with a low assimilation rate, the latter was probably not much in excess of the minimum required to prevent bottlenecking in the widespread polymorphisms. To obtain an estimate of the rate of assimilation from archaic populations, we can use Wright’s (1931) rule that one immigrant (meaning here the assimilated genetic equivalent [16] of one archaic individual) every two generations is enough to prevent significant bottlenecking of the ancient polymorphism in the wave-front moderns, who would have transmitted their genes to all emergent modern populations. This, of course, is an estimate of the minimal assimilation required. Even this low rate of assimilation into the wave-front modern population - of, say, 2,000 individuals — would, in 4,000 generations, have resulted in a cumulative 60% assimilation of archaic neutral genes in that population. [17] Therefore, in this view of the genetic data, there must have been substantial non-African archaic assimilation into modern populations farther away from Africa."

Note 15 of Eswaran's paper states,

"Loci with alleles that were widespread before the wave would be less likely to show either bottlenecks or expansions. This may explain why evidence of expansions is not always apparent in the genetic data (Harpending and Rogers 2000). The differing effects of the wave on “local” and “widespread” polymorphisms would also explain why mtDNA and some nuclear genes present contrasting pictures of human evolution (Hey 1997)."

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Eswaran, V. 2003. Reply to "On the Diffusion-Wave Model for the Spread of Modern Humans". Current Anthropology 44(4): 560-561

"Now data from separate studies of noncoding autosomal regions (Zhao et al. 2000, Yu et al. 2001) have confirmed the essential features that I used (pp. 761–62) to argue the case for archaic assimilation — no (or mild) signs of bottlenecks in non-Africans at low-mutation-rate loci,[3] great non-African time depths, and sometimes a significant number of unique non-African polymorphisms. These researchers specifically state that their data are inconsistent with the strict version of the recent-African-origin model.

"Finally, in their last point, Pearson and Stone argue that data from mtDNA and the Y chromosome reject the possibility of a large amount of archaic assimilation. Apart from ignoring the possibility of selection at these loci, this argument assumes that all extant human mtDNA and Y chromosomes are of recent African origin. In fact, indications are that extant Y chromosomes have considerable time-depth and include variants from premodern non-Africans, while mtDNA shows every sign of a selective sweep that coincided with the progress of anatomical modernity, with which it was possibly indirectly linked (for details see the electronic edition of this issue).

"Multilocus studies have not supported the case that all extant global variation is exclusively derived from recent African polymorphisms, which is the direct implication of the recent-African-origin model. For every other genetic pattern (the apparent African primacy and greater genetic diversity, the diversity clines, the signals of expansions, etc.) that supported the recent-African origin against the multiregional-evolution model, the diffusion-wave model offers a more parsimonious explanation stemming from a single mechanism. For others (the sub-Saharan African/Other split, the bottlenecks, the severity of these bottlenecks, the vastly differing expansion times), the diffusion-wave model offers natural explanations where the recent-African-origin gives none. Finally, certain features of the genetic data (the absence of signs of bottlenecks and/or expansions in many loci) directly refute the recent-African-origin model and suggest that a significant non-African archaic genetic inheritance lives on in present-day populations.[4]"

Note 3 says,
"I argue that the fact that bottlenecks are not empirically evident at some low-mutation-rate loci (which would otherwise “remember” the bottleneck) is proof of archaic assimilation."

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As per Andrew Kramer, Tracey L. Crummett & Milford H. Wolpolf (2001. Out of Africa and into the Levant: replacement or admixture in Western Asia? Quaternary International 75) I consider the Levantine population to be one species.

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From: G Horvat
Date: Sat, 10 May 2003
http://www.thehallofmaat.com/maat/read.php?f=1&i=118651&t=118465

"The Neandertal mtDNA sequences are certainly different than those of modern humans, however, it should be known that they were obtained from the hypervariable regions which represent approximately 1/16 of a complete sequence and while these regions are informative to a certain extent, they are not considered to be the most reliable for connecting human sequences of one continent to those of another. What is still lacking, I think, is a good understanding of how or why mutations occur because they occur in the same locations much more often than expected. The hypervariable regions are also basically useless for chimp/human comparisons."

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Hawks, J. & Wolpoff, M. 2001. The Accretion Model of Neandertal Evolution. Evolution 55(7): 1474–1485

Abstract

"The Accretion model of Neandertal evolution specifies that this group of Late Pleistocene hominids evolved in partial or complete genetic isolation from the rest of humanity through the gradual accumulation of distinctive morphological traits in European populations. As they became more common, these traits also became less variable, according to those workers who developed the model. Its supporters propose that genetic drift caused this evolution, resulting from an initial small European population size and either complete isolation or drastic reduction in gene flow between this deme and contemporary human populations elsewhere. Here, we test an evolutionary model of gene flow between regions against fossil data from the European population of the Middle and Late Pleistocene. The results of the analysis clearly show that the European population was not significantly divergent from its contemporaries, even in a subset of traits chosen to show the maximum differences between Europeans and other populations. The pattern of changes, over time within Europe of the traits in this subset, does not support the Accretion model, either because the characters did not change in the manner specified by the model or because the characters did not change at all. From these data, we can conclude that special phenomena such as near-complete isolation of the European population during the Pleistocene are not required to explain the pattern of evolution in this region."

Discussion

"Obviously we would prefer to have a larger sample of fossil hominids to examine questions of gene flow, but we can only work with the sample at hand and accept its limitations. The Accretion model that we have addressed must depend on the same sample and, of course, has the same limitations. One could argue that the constraints imposed by the sample make any statement of evolutionary model imprecise to the point where it risks invalidity, and we sympathize with this view. Nonetheless, the Accretion model has been widely published and accepted as an explanatory hypothesis, and we cling to the simple principle that if there is sufficient reason to believe a hypothesis, there must be sufficient data to test it. Given that the very data that have been used to generate the Accretion model apparently provide no support for it, we must wonder why the model exists. The reason is an artifact of the history of anthropology. The Accretion model is a variant of polygenism, much like the pseudo-evolutionary model proposed by Coon (1962) in which human subspecies were thought to have evolved in parallel, in virtual or complete isolation from each other. Today, no one contends that living human groups have independent origins early in the Pleistocene. But polygenism has been resurrected by scientists who assert that such separate origins do in fact exist: evolution in isolation for recent human groups in the Late Pleistocene (discussed by Templeton 1998), and separate origins for ancient human groups in the Early Pleistocene, delineated for archaic Europeans by the Accretion model.

"The key feature of pseudo-evolutionary polygenism is its reliance on massive parallelism to explain evolutionary trends shared by different groups. When researchers describe the phylogeny of our genus in terms of a ‘‘bush’’ of hominid species during the past two million years, usually unstated is the fact that whenever this ‘‘bushlike’’ pattern is subjected to phylogenetic analysis, hefty levels of homoplasy are the necessary result. Such homoplasy can be explained under this hypothesis only by the interpretation that any long-term evolutionary trends are parallel developments in separated genetic systems. Even explanations of behavioral evolution have come to require parallelism to account for what can be readily observed in the archaeological record (Mellars 1989). As archaeologists grapple with the questions of how and where modern human behaviors arose in the Late Pleistocene, the fact that they appear in European Neandertals and sub- Saharan Africans at about the same time also requires that modern human behaviors evolved independently and in parallel (Zilhao and D’Errico 1999), for those who assume that Neandertals are a different species.

"The Accretion model, as a descriptive hypothesis, does not make explicit whether distinct lineages or separate demes within a single species are thought to underlie this pattern, but neither of these can resolve the problems raised by the underlying polygenic interpretation. Limiting our investigations to crania, the subject of this paper, the foremost evolutionary trend among all representatives of Pleistocene Homo is the expansion of brain size, but others include: (1) reduction in the cranial superstructures (central and lateral supraorbital and nuchal tori) and in cranial bone thickness; (2) expansion of the occipital plane of the occiput at the expense of the nuchal (muscle-bearing) plane; (3) expansion of the superciliary aspect of the supraorbital torus, while the lateral structures reduce and in some cases degenerate; (4) anterior dental reduction; and (5) nasal breadth reduction.

"Any account of evolution within our genus must explain these facts. The only explanation provided by the Accretion model and other polygenic variants is parallelism. At the extreme, Tattersall (1996, p. 52) defends an interpretation of multiple contemporary Homo species in the Pleistocene and explains the parallel evolutionary trends this interpretation requires as follows:

" ‘‘Natural selection takes place at the level of the local population, and in similar circumstances closely related populations are likely to respond to ecological pressures or other agents of natural selection upon them in similar ways. These various considerations will hold true even when such local populations have become individual evolutionary entities. When, that is, speciation has intervened between them.’’

"It is of interest to compare this with Wiley’s (1981, p. 25) definition of the evolutionary species: ‘‘a single lineage of ancestral-descendant populations which maintains its identity from other lineages and which has its own evolutionary tendencies and historical fate.’’ It is plain that if Tattersall is correct then the evolutionary species definition must be invalid, because different closely related species might be expected to have the same evolutionary tendencies. Alternatively, if the definition is valid and provides a means of comparing present and past species, then Tattersall is incorrect in presuming that a number of the same long-term evolutionary trends can take place in different species (especially in the human case; Wolpoff 1994), when the purported species are wide-ranging and contiguous. We prefer the second alternative as by far a more likely, and more testable, proposition. Parallelism does occur in evolution and is more common among closely related species than among distantly related groups. However, the level of parallelism required to support a ‘‘bushlike’’ interpretation of our evolution is insupportable, when compared to the more parsimonious alternative of gene flow among groups. There is no scientific basis for any polygenic theory of human evolution (Wolpoff and Caspari 1997).

"By directly testing the hypothesis of gene flow among these ancient groups, we provide a novel way to address the ancestry of recent humans. Rogers (1995) points out the difficulty of testing the hypothesis of replacement of ancient humans isolated within regions with humans of geographically separate origins. However, the polygenic model based on replacement depends not only on the wholesale migration of recent humans from a single source, but also on the complete isolation of archaic humans before this dispersal event. The demonstration that we cannot substantiate any isolation between ancient regions directly weakens the hypothesis of replacement by showing that the geographic source population for recent humans, in the genetic sense, must extend across more than one ancient region of the world. Even if substantial migrations occurred during the Late Pleistocene, the genetic background of this expanding population reflects a prior equilibrium population with migration from several regions. This genetic continuity should be considered by researchers who compare recent and ancient groups. Our analysis suggests strongly that the observations of Relethford (1995), who examines the differences of recent human groups in terms of an equilibrium migration model with much larger population size in Africa than in other regions, provide an appropriate basis for understanding the genetic differentiation of recent and ancient humans.

"In summary, our study demonstrates clearly that no special explanations or phenomena are required to account for the evolution of certain characters in Pleistocene Europeans that have been described as ‘‘distinctive’’ in this population. The hypothesis that this population was connected to other populations by gene flow during the Pleistocene has not been rejected by morphological evidence. This finding is consistent with molecular evidence from ancient DNA sequence variation, which shows a higher divergence between Neandertals and recent humans than among recent humans alone, but a threefold lower divergence than would be expected if these groups had diverged before the Late Pleistocene (Krings et al. 1997, 1999). It is also consistent with morphological evidence for genetic exchanges between Europeans and other populations after 40,000 years ago (Frayer 1993). A simple and homogeneous model of gene flow at levels equal to recent humans between populations of unchanging sizes is without doubt too simple to fully describe the evolution of Pleistocene humans. We have every reason to believe that different human populations have experienced different selective, environmental, and demographic histories. Nevertheless, using the currently available data, as slim as they are in places, we are able to say with confidence that the morphological differences present between Neandertals and other populations are not the result of complete isolation of Europe from other regions. They do not have to be attributed to the genetic isolation of a unique Neandertal lineage. They are compatible with an antiparallelist explanation of selection and genic exchanges, and the results of isolation by distance across the broad range of territories occupied by the human species — in other words, Multiregional evolution."

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Frayer, D. 1997. Perspectives on Neanderthals as Ancestors. In Clark, G.A. & Willermet, C.M. (eds.) Conceptual Issues in Modern Human Origins Research. New York: Aldine de Gruyter

Conclusion

"In summary, based on these comparative evolutionary rates, the average and individual rates of evolutionary change between European Neanderthals (or late Neanderthals) and early Upper Paleolithic hominids are not especially rapid. Rather, rates of change between either European Neanderthal samples and the early Upper Paleolithic are within the magnitude of change found for recent Homo sapiens. Thus, contrary to the commonly stated argument that not enough time exists for European Neanderthals to be ancestral to subsequent Europeans, these data clearly demonstrate that there was no "tremendous acceleration" in rates of change between the Neanderthals and the Upper Paleolithic Europeans. For me, these data falsify the argument that European Neanderthals as a group cannot be ancestral to subsequent Homo sapiens in Europe (at least with respect to metric features of the face and teeth) because too much change is required over too little time. Moreover, based on the rates of dental evolutionary change, there is nothing to support the contention that European Neanderthals represent a separate species. Such a conclusion would only hold if one is also willing to accept a speciation event between the early Upper Paleolithic and Neolithic, since all of these comparisons have similar, or in some case considerably higher, average or individual evolutionary rates.

"While rates of dental evolutionary change by themselves do not prove that Neanderthals are ancestral to early Upper Paleolithic Europeans, these results do indicate that European Neanderthals cannot be eliminated as possible ancestors based on speculations which require grossly elevated evolutionary rates. Moreover, the period following the Neanderthals in Europe is not characterized by absolute or relative stasis but by marked change within the Upper Paleolithic and from the Upper Paleolithic to the Neolithic. These observations should put to rest both the contention that difference between the European Neanderthals and the early Upper Paleolithic require an exorbitant rate of change and the unsupported claim that tooth size shows little absolute or relative change after the appearance of the Upper Paleolithic. Those who still maintain that European Neanderthals are unrelated to subsequent European Homo sapiens must look to other data; these data do not include the presence of so-called Neanderthal autapomorphic traits or exorbitant rates of change.

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Alan R. Templeton. 2002. Out of Africa again and again. Nature 416(7)

Abstract

"The publication of a haplotype tree of human mitochondrial DNA variation in 1987 provoked a controversy about the details of recent human evolution that continues to this day. Now many haplotype trees are available, and new analytical techniques exist for testing hypotheses about recent evolutionary history using haplotype trees. Here I present formal statistical analysis of human haplotype trees for mitochondrial DNA, Y-chromosomal DNA, two X-linked regions and six autosomal regions. A coherent picture of recent human evolution emerges with two major themes. First is the dominant role that Africa has played in shaping the modern human gene pool through at least two - not one - major expansions after the original range extension of Homo erectus out of Africa. Second is the ubiquity of genetic interchange between human populations, both in terms of recurrent gene flow constrained by geographical distance and of major population expansion events resulting in interbreeding, not replacement."

Pages 48 - 9

"The highest clade level inferences for five genes are range expansions out of Africa (mtDNA at 0.13Myr ago; Y-DNA at 0.09Myr ago; MC1R at 0.64Myr ago; and b-globin at 0.82Myr ago) and a range expansion of ambiguous origin (MS205 at 0.63Myr ago). Figure 3 shows tha gamma distributions associated with the ages of these expansion events. The B-globin inference has 5.6% of its probability mass at 1.7Myr ago or older, but all the other inferred range expansions have much less probability mass at 1.7Myr ago or older. Hence, there is no cross-validated inference of marking the original expansion of Homo erectus out of Africa. Figure 3 shows that the five inferences fall into two broadly overlapping classes; the mtDNA and Y-DNA that are tightly clustered around an expansion event out of Africa at about 100,000 years ago, and the three autosomal loci with means between 0.64 to 0.82Myr ago. To test the null hypothesis that all five loci are compatible with a single range expansion event, the lower age bound was found such that 0.1% of the B-globin probability distribution was above this age (this locus has the oldest inferred expansion event) and the upper age bound was found such that 0.1% of the Y-DNA probability distribution was below this age (this locus has the youngest inferred expansion event). Any age outside of this interval would be strongly rejected (at the 0.1% level) on ths basis of Y-DNA or B-globin alone. This interval spans between 0.0474 to 0.2906Myr ago and is shown in grey in Fig. 3. The probability that all five loci are detecting an event in this age interval is 0.003. Because the expansion event detected with MS205 is of ambiguous geographical origin, the calculation was repeated excluding that locus to focus specifcally upon out-of-Africa expansion events. With this exclusion, the hypothesis of a single out-of-Africa expansion event is rejected with P . 0:018."

Page 49

"The GEODIS analyses indicate that the most recent out-of-Africa expansion event was not a replacement event. If it had been, the three significant genetic signatures of the older expansion event (Fig. 3) and the six significant genetic signatures of older recurrent gene flow (Fig. 2) would have been wiped away. Although there is considerable error in dating any single inference from only one gene, an out-of-Africa replacement event would require that all nine significant inferences found in all eight bisexually inherited nuclear loci examined would have to be in error simultaneously. Moreover, the dating errors would have to be large in all nine cases and in the same direction. The hypothesis of a recent out-of-Africa replacement event is therefore strongly rejected."

Discussion

"The model of recent human evolution shown in Fig. 1 is dominated by genetic interchange and a special role for Africa. I consider first genetic interchange. African and Eurasian populations were linked by recurrent gene flow, certainly over the last half a million years, and probably longer. Overlaid upon this gene flow trellis are occasional major movements out of Africa and out of Asia that enhanced gene interchange through interbreeding. More recently, population expansions acted to extend the geographical range of the human species and to establish additional areas linked by gene flow. This model emphasizes that genetic interchange among human populations, facilitated both by gene flow and range expansions coupled with interbreeding, has been a major force in shaping the human species and its spatial pattern of genetic diversity. Second, Fig. 1 reveals the special role that African populations have played in human evolution. There were at least two major movements of peoples out of Africa after the original spread of Homo erectus. This inference is consistent with the archaeological record of cultural expansions out of Africa (Acheulean) in the middle Pleistocene. These Acheulean cultural expansions broadly overlap the time frame of the middle out-of-Africa expansion event shown in Fig. 1, indicating that this expansion involved both people and ideas coming out of Africa and interacting with local populations in Eurasia. This expansion is also compatible with the fossil data. After the initial expansion of Homo erectus out of Africa about 1.7Myr ago, there was little change in average brain size up to 700,000 years ago1. By 400,000 to 500,000 years ago, average cranial capacities had shown a substantial increase. The time period of this transition in cranial capacity overlaps extensively with the time period for the older out-of-Africa expansion event shown in Fig. 3.

"The most recent out-of-Africa expansion event shown in Figs 1 and 3 is also compatible with fossil evidence. Many `modern' traits (such as high, rounded skulls; small brow ridges; a vertical forehead; and a noticeable chin) first appear in Africa about 130,000 years ago, followed by an expansion out-of-Africa more than 90,000 years ago. This time frame overlaps extensively with the out-of-Africa expansion marked by the mtDNA and Y-DNA distributions in Fig. 3, implying that many of these traits could have been carried into Eurasia by this African population range expansion. Other traits, however, do not display any significant changes before, during or after this most recent expansion out of Africa. This later set of traits is difficult to reconcile with a population replacement, but is compatible with this most recent out-of-Africa expansion event being characterized by interbreeding. With interbreeding, mendelian inheritance allows some traits to spread while others do not. Moreover, living humans are still polymorphic for `modern' traits, and the frequencies of different `modern' traits show heterogeneity in their present geographical distributions1. The current spatial and frequency heterogeneity in `modern' traits undercuts the idea of a global replacement of an `archaic' type by a `modern' type but is consistent with a trait-based evolution of humans that is allowed under expansion with interbreeding. The model in Fig. 1 indicates the recent fossil evidence should be interpreted in terms of traits and not population types. The genetic impacts of Africa upon the entire human species is large because of at least three major expansions out of Africa, although the genetic impact is not as complete as it would be under total replacement. This model is similar to earlier models that have emphasized the role of out-of-Africa population expansion coupled with gene flow and not replacement, such as the assimilation model of Smith et al., the multiregional model with expansions followed by admixture ofWolpoff et al.50, and the `mostly out of Africa' model of Relethford. The predicted large genetic impact of African populations explains the results of Takahata et al. that about 90% of the haplotype trees in the nuclear genome appear to be rooted in Africa. These results also falsify a total replacement hypothesis, which predicts that all haplotype trees with coalescent times greater than 100,000 years must be rooted in Africa. All of the haplotype trees considered have expected coalescent times greater than 100,000 years, so 100% of such old trees should have African roots under complete replacement, and not the observed 90%. The results given here show the importance of examining many DNA regions with a common analytical technique in making phylogeographic inferences. Indeed, the clearest result from Tables 1 and 2 is how incomplete our view of human evolution would be if it were based upon just one locus or DNA region. As more DNA regions are examined, additional insights into human evolution are sure to follow. However, this current analysis already demonstrates the inadequacies of both the out-of-Africa replacement model and of a simple trellis model. Humans expanded again and again out of Africa, but these expansions resulted in interbreeding, not replacement, and thereby strengthened the genetic ties between human populations throughout the world."

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Wolpoff, M. 1999. Paleoanthropology. Boston: McGraw-Hill. (2nd)

Pages 553-4

"But the widespread distribution of a number of rare variations in nuclear DNA shows there cannot have been a severe bottleneck for them, or, Xiong Weijun and colleagues suggest, even a significant population reduction. If there had been, these rare variations would have disappeared. But many have not; some, according to F. Aala, reflect genetic structures so similar to chimpanzees that they must be ancient. Humans and chimpanzees share many common alleles for the major histocompatibility complex genes. Divergence times for some of these genes are at 6 myr, the time of the chimpanzee-human divergence. Ayala calculates certain of them such as the human leukocyte antigen could not have passed through bottlenecks of less than 100,000 copies. In a similar analysis, Li Wenhisung and L. Sadler compared nucleotide and protein diversity in human and Drosophila DNA. The levels of protein diversity are quite similar, but nucleotide diversity is much lower in humans. They attribute this difference to a small but stable population size through most of human prehistory, rather than a bottleneck. If there had been a severe bottleneck long after the hominid-chimpanzee split, most of these shared polymorphisms would have been lost. The population of the human species could never have been as small as some population geneticists studying past population expansions have proposed. In sum, some gene systems, for instance mtDNA and certain segments of the Y chromosome, have gone through bottlenecks, but others have not. This would be an impossible conclusion if human populations had gone through a recent bottleneck. Replacement models require that all but the most recently evolved genes have the same history as the population they are in. These data show that gene histories are by-in-large independent of population histories."

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Klein, J. & Takahata, N. 2002. Where do we come from ? The molecular evidence for human descent. New York: Springer

Pages 307-8

"The sequence, Lake Mungo 3 or LM3, was derived from a gracile individual who expired 62,000 +/- 6000 years ago...For those who do not read scientific reports, the journalists conveyed the message in no uncertain terms as a clear home run for the multiregionalists in their match against the uniregionalists. In reality, however, the LM3 sequence does not support any such conclusions. The position of the sequence on the phylogenetic tree depends on the choice of extant H. sapiens sequences included in the sample and on the tree drawing method used. In many trees, both the LM3 and the numt sequences position themselves within the cluster of contemporary human sequences and, as the authors themselves admit, "trees in which the LM3/Insert lineage branches before the MRCA of contemporary human sequences were not significantly more likely than trees in which this lineage diverged after the MRCA of contemporary human sequences." In other words, you can take the tree that you find most appealing and the authors obviously preferred the one showing the LM3/numt sequences to be outside the cluster of extant human sequences. However, even if one were to accept this placement as genuine, it would still not provide evidence for the multiregional and against the uniregional hypotheses. It could be interpreted alternatively as evidence that mtDNA lineages existed in prehistoric H. sapiens that no longer persist in contemporary humans. The extinct lineages may have been replaced by the ancestors of the currently existing lineages which spread through the human species either by random genetic drift or by selection acting on one or several of the genes borne by the nonrecombining mtDNA molecules. "Of course, the same reservations must also apply to the interpretations of the Neandertal sequences. Their position outside the cluster of modern human sequences is largely reproducible and independent both of sampling and the method used. Nevertheless, it by no means provides evidence that Neandertals did not contribute genes to the H. sapiens gene pool and hence that they were "replaced" by modern humans. The apparent absence of H. neanderthalensis mtDNA variants in the H. sapiens gene pool could reflect the possible extinction of Neandertal lineages by drift or selection following the initial mixing of the two gene pools. Moreover, in the collection of contemporary human sequences, there are pairs that differ from the Neandertal sequences: the minimum number of substitutions between Neandertal and contemporary human mtDNA is 13, whereas the maximum number of substitutions in comparisons between mtDNAs of living humans is 22. This observation is, of course, inconsistent with the conclusion that H. neanderthalensis and H. sapiens were two distinct, noninterbreeding species, because if they were, any overlap in mtDNA variation between them should have been removed by evolution subsequent to species divergence. Although the inconsistency can be explained by postulating multiple changes that obscure the phylogenetic signal at some nucleotide sites, it can be argued - as the proponents of the multiregional hypothesis indeed have done - that this explanation is an ad hoc postulate introduced to avert the downfall of the uniregional hypothesis. In all fairness, therefore, of the conclusions reached by Krings and coworkers and echoed by Ovchinnikov and his associates, only one is warranted: the sequences are most likely of Neandertal origins. Viewed objectively, neither the Neandertal nor the ancient Australian sequences resolve the controversy regarding the origin of modern H. sapiens. Indeed, it is doubtful that mtDNA studies ever will. Despite the fanfare that accompanied the publication of the sequences of Neandertal and other fossil mtDNA sequences, the actual contribution of these sequences to the resolution of scientific questions has thus far been minimal"

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Hammer, M. F., T. Karafet, A. Rasanayagam, E. T. Wood, T. K. Altheide, T. Jenkins, R. C. Griffiths, A. R. Templeton, and S. L. Zegura. 1998. Out of Africa and back again: nested cladistic analysis of human Y chromosome variation. Mol. Biol. Evol. 15:427­441

The article does not advocate a populational bottleneck bottleneck. Page 438: "Templeton's (1998b) reanlysis of Harding et al.'s (1997) B-globin data represents the only nested cladistic analysis of a human autosomal data set. The deepest clade in the B-globin gene tree makes it unlikely that this range expansion had anything to do with the out-of-Africa event detected by our Y chromosome data. On the other hand, this time frame is more conordant with the sudden appearance of the possibly African-derived Homo antecessor in Spain sometime before 780,000 years ago (Bermudez de Castro et al. 1997). Moving to less deep structures, all the midlevel (two-step) clades gave strong evidence for gene flow restricted via isolation by distance occurring more than 200,000 years ago throughout the Old World. Finally, two range expansions were detected at the one-step clade leven: (1) the aforementioned expansion from southeast Asia back to Africa, and (2) an out-of-Africa expansion that innvolved the oldest haplotypes by outgroup rooting, making the temporal framework of this expansion unclear (i.e. it may be a recent expansion or the same one detected at higher levels in the cladogram). This out-of-Africa expansion was not a replacement event, because it was nested within a two-step clade characterized by gene flow restricted via isolation by distance. In order to equate this out-of-Africa event with the one detected in our Y chromosome data, one would have to argue that perhaps Eurasian males were replaced but females were not. This is consistent with the demographic picture from the nested cladistic analyses of mtDNA data (Templeton 1993, 1997), in which females show no signs of replacement and gene flow rather than range expansion is the oldest inference. Therefore, the B-globin locus integrates aspects of both the mtDNA and Y chromosome analyses and provides support for the hypotheses of contrasting male and female population structure and demographic histories. Because there is evidence for restricted, recurrent gene flow throughout the Old World during the entire history of anatomically modern humans, as well as for range expansions out of Africa >100,000 years ago, the nested cladistic analysis results from these three types of data conform with genetic predictions based on human origin(s) models characterized by interbreeding between migrating and resident populations. Thus, the combined data add a new sex-specific component to the conceptual framework of both Brauer's (1989) African Hybridization and Replacement model and Smith, Falsetti, and Donnelly's (1989) Assimilation model: the possibility that the Old World female genetic component was preserved by hybridization, whereas the Eurasian male component was replaced by African Y chromosome."

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Templeton, A. 2002. Out of Africa again and again. Nature 416, 7 March 2002

Abstract: "The publication of a haplotype tree of human mitochondrial DNA variation in 1987 provoked a controversy about the details of recent human evolution that continues to this day. Now many haplotype trees are available, and new analytical techniques exist for testing hypotheses about recent evolutionary history using haplotype trees. Here I present formal statistical analysis of human haplotype trees for mitochondrial DNA, Y-chromosomal DNA, two X-linked regions and six autosomal regions. A coherent picture of recent human evolution emerges with two major themes. First is the dominant role that Africa has played in shaping the modern human gene pool through at least two - not one - major expansions after the original range extension of Homo erectus out of Africa. Second is the ubiquity of genetic interchange between human populations, both in terms of recurrent gene flow constrained by geographical distance and of major population expansion events resulting in interbreeding, not replacement."

Pages 48 - 9: "The highest clade level inferences for five genes are range expansions out of Africa (mtDNA at 0.13Myr ago; Y-DNA at 0.09Myr ago; MC1R at 0.64Myr ago; and b-globin at 0.82Myr ago) and a range expansion of ambiguous origin (MS205 at 0.63Myr ago). Figure 3 shows tha gamma distributions associated with the ages of these expansion events. The B-globin inference has 5.6% of its probability mass at 1.7Myr ago or older, but all the other inferred range expansions have much less probability mass at 1.7Myr ago or older. Hence, there is no cross-validated inference of marking the original expansion of Homo erectus out of Africa. Figure 3 shows that the five inferences fall into two broadly overlapping classes; the mtDNA and Y-DNA that are tightly clustered around an expansion event out of Africa at about 100,000 years ago, and the three autosomal loci with means between 0.64 to 0.82Myr ago. To test the null hypothesis that all five loci are compatible with a single range expansion event, the lower age bound was found such that 0.1% of the B-globin probability distribution was above this age (this locus has the oldest inferred expansion event) and the upper age bound was found such that 0.1% of the Y-DNA probability distribution was below this age (this locus has the youngest inferred expansion event). Any age outside of this interval would be strongly rejected (at the 0.1% level) on ths basis of Y-DNA or B-globin alone. This interval spans between 0.0474 to 0.2906 Myr ago and is shown in grey in Fig. 3. The probability that all five loci are detecting an event in this age interval is 0.003. Because the expansion event detected with MS205 is of ambiguous geographical origin, the calculation was repeated excluding that locus to focus specifcally upon out-of-Africa expansion events. With this exclusion, the hypothesis of a single out-of-Africa expansion event is rejected with P . 0:018."

Page 49: "The GEODIS analyses indicate that the most recent out-of-Africa expansion event was not a replacement event. If it had been, the three significant genetic signatures of the older expansion event (Fig. 3) and the six significant genetic signatures of older recurrent gene flow (Fig. 2) would have been wiped away. Although there is considerable error in dating any single inference from only one gene, an out-of-Africa replacement event would require that all nine significant inferences found in all eight bisexually inherited nuclear loci examined would have to be in error simultaneously. Moreover, the dating errors would have to be large in all nine cases and in the same direction. The hypothesis of a recent out-of-Africa replacement event is therefore strongly rejected."

Pages 49 - 50: The model of recent human evolution shown in Fig. 1 is dominated by genetic interchange and a special role for Africa. I consider first genetic interchange. African and Eurasian populations were linked by recurrent gene flow, certainly over the last half a million years, and probably longer. Overlaid upon this gene flow trellis are occasional major movements out of Africa and out of Asia that enhanced gene interchange through interbreeding. More recently, population expansions acted to extend the geographical range of the human species and to establish additional areas linked by gene flow. This model emphasizes that genetic interchange among human populations, facilitated both by gene flow and range expansions coupled with interbreeding, has been a major force in shaping the human species and its spatial pattern of genetic diversity. Second, Fig. 1 reveals the special role that African populations have played in human evolution. There were at least two major movements of peoples out of Africa after the original spread of Homo erectus. This inference is consistent with the archaeological record of cultural expansions out of Africa (Acheulean) in the middle Pleistocene. These Acheulean cultural expansions broadly overlap the time frame of the middle out-of-Africa expansion event shown in Fig. 1, indicating that this expansion involved both people and ideas coming out of Africa and interacting with local populations in Eurasia. This expansion is also compatible with the fossil data. After the initial expansion of Homo erectus out of Africa about 1.7Myr ago, there was little change in average brain size up to 700,000 years ago1. By 400,000 to 500,000 years ago, average cranial capacities had shown a substantial increase. The time period of this transition in cranial capacity overlaps extensively with the time period for the older out-of-Africa expansion event shown in Fig. 3.
The most recent out-of-Africa expansion event shown in Figs 1 and 3 is also compatible with fossil evidence. Many `modern' traits (such as high, rounded skulls; small brow ridges; a vertical forehead; and a noticeable chin) first appear in Africa about 130,000 years ago, followed by an expansion out-of-Africa more than 90,000 years ago. This time frame overlaps extensively with the out-of-Africa expansion marked by themtDNAand Y-DNAdistributions in Fig. 3, implying that many of these traits could have been carried into Eurasia by this African population range expansion. Other traits, however, do not display any significant changes before, during or after this most recent expansion out of Africa. This later set of traits is difficult to reconcile with a population replacement, but is compatible with this most recent out-of-Africa expansion event being characterized by interbreeding. With interbreeding, mendelian inheritance allows some traits to spread while others do not. Moreover, living humans are still polymorphic for `modern' traits, and the frequencies of different `modern' traits show heterogeneity in their present geographical distributions1. The current spatial and frequency heterogeneity in `modern' traits undercuts the idea of a global replacement of an `archaic' type by a `modern' type but is consistent with a trait-based evolution of humans that is allowed under expansion with interbreeding. The model in Fig. 1 indicates the recent fossil evidence should be interpreted in terms of traits and not population types. The genetic impacts of Africa upon the entire human species is large because of at least three major expansions out of Africa, although the genetic impact is not as complete as it would be under total replacement. This model is similar to earlier models that have emphasized the role of out-of-Africa population expansion coupled with gene flow and not replacement, such as the assimilation model of Smith et al., the multiregional model with expansions followed by admixture of Wolpoff et al. and the `mostly out of Africa' model of Relethford. The predicted large genetic impact of African populations explains the results of Takahata et al. that about 90% of the haplotype trees in the nuclear genome appear to be rooted in Africa. These results also falsify a total replacement hypothesis, which predicts that all haplotype trees with coalescent times greater than 100,000 years must be rooted in Africa. All of the haplotype trees considered have expected coalescent times greater than 100,000 years, so 100% of such old trees should have African roots under complete replacement, and not the observed 90%. The results given here show the importance of examining many DNA regions with a common analytical technique in making phylogeographic inferences. Indeed, the clearest result from Tables 1 and 2 is how incomplete our view of human evolution would be if it were based upon just one locus or DNA region. As more DNA regions are examined, additional insights into human evolution are sure to follow. However, this current analysis already demonstrates the inadequacies of both the out-of-Africa replacement model and of a simple trellis model. Humans expanded again and again out of Africa, but these expansions resulted in interbreeding, not replacement, and thereby strengthened the genetic ties between human populations throughout the world.
But the widespread distribution of a number of rare variations in nuclear DNA shows there cannot have been a severe bottleneck for them, or, Xiong Weijun and colleagues suggest, even a significant population reduction. If there had been, these rare variations would have disappeared. But many have not; some, according to F. Aala, reflect genetic structures so similar to chimpanzees that they must be ancient. Humans and chimpanzees share many common alleles for the major histocompatibility complex genes. Divergence times for some of these genes are at 6 myr, the time of the chimpanzee-human divergence. Ayala calculates certain of them such as the human leukocyte antigen could not have passed through bottlenecks of less than 100,000 copies. In a similar analysis, Li Wenhisung and L. Sadler compared nucleotide and protein diversity in human and Drosophila DNA. The levels of protein diversity are quite similar, but nucleotide diversity is much lower in humans. They attribute this difference to a small but stable population size through most of human prehistory, rather than a bottleneck. If there had been a severe bottleneck long after the hominid-chimpanzee split, most of these shared polymorphisms would have been lost. The population of the human species could never have been as small as some population geneticists studying past population expansions have proposed. In sum, some gene systems, for instance mtDNA and certain segments of the Y chromosome, have gone through bottlenecks, but others have not. This would be an impossible conclusion if human populations had gone through a recent bottleneck. Replacement models require that all but the most recently evolved genes have the same history as the population they are in. These data show that gene histories are by-in-large independent of population histories.

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Hawks, J., Hunley, K., Lee, S-H., Wolpoff, M. 2000. Population Bottlenecks and Pleistocene Human Evolution. Mol. Biol. Evol. 17(1):2–22

We review the anatomical and archaeological evidence for an early population bottleneck in humans and bracket the time when it could have occurred. We outline the subsequent demographic changes that the archaeological evidence of range expansions and contractions address, and we examine how inbreeding effective population size provides an alternative view of past population size change. This addresses the question of other, more recent, population size bottlenecks, and we review nonrecombining and recombining genetic systems that may reflect them. We examine how these genetic data constrain the possibility of significant population size bottlenecks (i.e., of sufficiently small size and/or long duration to minimize genetic variation in autosomal and haploid systems) at several different critical times in human history. Different constraints appear in nonrecombining and recombining systems, and among the autosomal loci most are incompatible with any Pleistocene population size expansions. Microsatellite data seem to show Pleistocene population size expansions, but in aggregate they are difficult to interpret because different microsatellite studies do not show the same expansion. The archaeological data are only compatible with a few of these analyses, most prominently with data from Alu elements, and we use these facts to question whether the view of the past from analysis of inbreeding effective population size is valid. Finally, we examine the issue of whether inbreeding effective population size provides any reasonable measure of the actual past size of the human species. We contend that if the evidence of a population size bottleneck early in the evolution of our lineage is accepted, most genetic data either lack the resolution to address subsequent changes in the human population or do not meet the assumptions required to do so validly. It is our conclusion that, at the moment, genetic data cannot disprove a simple model of exponential population growth following a bottleneck 2 MYA at the origin of our lineage and extending through the Pleistocene. Archaeological and paleontological data indicate that this model is too oversimplified to be an accurate reflection of detailed population history, and therefore we find that genetic data lack the resolution to validly reflect many details of Pleistocene human population change. However, there is one detail that these data are sufficient to address. Both genetic and anthropological data are incompatible with the hypothesis of a recent population size bottleneck. Such an event would be expected to leave a significant mark across numerous genetic loci and observable anatomical traits, but while some subsets of data are compatible with a recent population size bottleneck, there is no consistently expressed effect that can be found across the range where it should appear, and this absence disproves the hypothesis.

While it is clear that paleontological, archaeological, and genetic approaches are potentially rich sources of hypotheses about human demographic history, each alone has a considerable disadvantage when applied as a test of paleodemographic questions. The weaknesses of fossil and archeological approaches lie in their incompleteness and poor sampling. While paleoanthropologists have learned much about human phylogeny and adaptation, it has been a challenge to obtain any but the roughest estimates of past population size from site distributions, distributions of technologies or traits, or evidence of morphological evolution. Geographically clustered sampling and taphonomy bias the samples, and their sizes are very small. The weakness of genetic data is inaccuracy, especially in the sense of low levels of resolution, as there are many factors other than population size that affect genetic diversity and do so in ways that are largely not quantifiable. Perhaps the most significant of these is selection, and its main effect is to remove the element of predictability from these relationships because the details of past selection are unknown, and perhaps unknowable. All the currently available genetic, paleontological, and archaeological data are consistent with a bottleneck in our lineage more or less at about 2 MYA. At the moment, genetic data cannot disprove a simple model of exponential population growth following such a bottleneck and extending through the Pleistocene. Archaeological and paleontological data indicate that this model is too oversimplified to be an accurate reflection of detailed population history, and therefore we conclude that genetic data lack the resolution to validly reflect many details of Pleistocene human population change. However, there is one detail these data are suffi- cient to address. Both genetic and anthropological data are incompatible with the hypothesis of a recent population size bottleneck. Such an event would be expected to leave a significant mark across numerous genetic loci and observable anatomical traits. Genetic and anatomical traits, after all, are the raw data the hypothesized bottleneck is meant to explain. But while some subsets of data are compatible with a recent population size bottleneck, there is no consistently expressed effect that can be found across the range where it should appear, and this absence disproves the hypothesis. There are better ways to explain the data. Although significant population size fluctuations and contractions occurred, none has left a singular mark on our genetic heritage. Instead, while isolation by distance across the network of population interactions allowed differences to persist, and with selection, local adaptations were able to develop, evolution through selection, along with gene flow, has promoted the spread of morphological and behavioral changes across the human range. It is this pattern of shared ancestry that has left its signature in the variation that we observe today. We know this from many sources of data and argue that no single source can suffice. If the evidence of a population size bottleneck early in the evolution of our lineage is accepted, most genetic data by themselves either lack the resolution to address subsequent changes in the human population or do not meet the assumptions required to do so validly.


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