Complex speciation in primates (Mailund et al. 2012)

PLoS Genet 8(12): e1003125. doi:10.1371/journal.pgen.1003125

A New Isolation with Migration Model along Complete Genomes Infers Very Different Divergence Processes among Closely Related Great Ape Species

Thomas Mailund et al.

We present a hidden Markov model (HMM) for inferring gradual isolation between two populations during speciation, modelled as a time interval with restricted gene flow. The HMM describes the history of adjacent nucleotides in two genomic sequences, such that the nucleotides can be separated by recombination, can migrate between populations, or can coalesce at variable time points, all dependent on the parameters of the model, which are the effective population sizes, splitting times, recombination rate, and migration rate. We show by extensive simulations that the HMM can accurately infer all parameters except the recombination rate, which is biased downwards. Inference is robust to variation in the mutation rate and the recombination rate over the sequence and also robust to unknown phase of genomes unless they are very closely related. We provide a test for whether divergence is gradual or instantaneous, and we apply the model to three key divergence processes in great apes: (a) the bonobo and common chimpanzee, (b) the eastern and western gorilla, and (c) the Sumatran and Bornean orang-utan. We find that the bonobo and chimpanzee appear to have undergone a clear split, whereas the divergence processes of the gorilla and orang-utan species occurred over several hundred thousands years with gene flow stopping quite recently. We also apply the model to the Homo/Pan speciation event and find that the most likely scenario involves an extended period of gene flow during speciation.

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Longer time scale for human evolution (Hawks 2012)

Scally and Durbin published a recent review on the implications of a slower human autosomal mutation rate, and now John Hawks has a commentary on the same topic in PNAS (pdf; paywall). He goes through a lot of the evidence of early fossil hominins and ape and mentions several examples that harmonize with the slower mutation rate. As expected, he also finds a better agreement of the slow mutation rate with the evidence for Neandertals where 530,000 year old finds from Atapuerca show signs of belonging to the Neandertal lineage, a date that is inconsistent with a late divergence of modern humans and Neandertals. Finally, he has this to say about modern humans:

Across this same time scale, the archaic ancestors of today’s Africans had already developed an intricate population structure. Genomic investigation of African hunter–gatherers has opened new windows onto this deep genetic history of differentiation and introgression (14, 15), bringing the origin of modern African diversity into the population structure of the early Middle Pleistocene. A simple hypothesis of modern human origins in a bottlenecked population cannot account for this diverse genetic history.    

The mtDNA time scale now poses a hanging question. Mitochondrial mutations occur much more often than nuclear DNA mutations, with greater heterogeneity among sites (16). Still, our estimate of mtDNA substitution rates depends on our estimates of branch lengths of the primate phylogeny. Until now, mitochondrial comparisons have been the strongest evidence in favor of a short time scale for the dispersal and differentiation of non-African peoples, within the past 70,000 y (17). Some recent attempts to examine the relationships of non-African populations using nuclear genome data have led to time scales in excess of 100,000 y (18), and others favor more recent estimates (19). Despite the recency of this work, most authors have continued to use an outdated fast molecular clock and short generation time estimates. As we move forward, such results will need to be corrected or adjusted to enable comparisons with current work. 

There is a very interesting question here, which I've mentioned before, but is worth repeating: admixture between divergent lineages can inflate split times. Acceptance of the slow autosomal mutation rate will result in split times in excess of 100 thousand years for Africans vs. non-Africans, and perhaps 300 thousand years for African hunter-gatherers. On the other hand, the mtDNA clock (haplogroup L3 = 70ky), no matter how it is recalibrated is unlikely to match these old dates, and the Y-chromosome clock (current estimate of its root a little more than 100 ky, and of the dominant African lineage E on the cusp of the LSA) will certainly not match them.

In my opinion, it will slowly become apparent that the way to harmonize our picture of human origins is to accept a substantial degree of archaic admixture in Africa. Such admixture cannot be detected directly, because there are no archaic genomes from Africa, and the hot climate throughout much of the continent may make preservation of DNA more difficult than in northern parts of Eurasia (where Neandertal and Denisovan individuals were from). Nor can it always be detected with LD-based methods, since LD decays exponentially and really old admixture is indistinguishable from an excess of mutation in a large population size. But, its acceptance will simultaneously solve the riddle of excess polymorphism in Africans, remove the need for an Out-of-Africa bottleneck of biblical proportions, and resolve the discrepancy between autosomal and uniparental evidence.

Cultured orangutans

The is a long-standing debate about the origins of human uniqueness. Specific human adaptations (such as the use of sophisticated tools, fire, clothing, ornaments, etc.) seem to have occurred at different times. What seems to be most human, however, is language and culture. Our species, it turns out, is not the only one to have culture, i.e., transmission of know-how via non-genetic means, but we are certainly awfully good at it, aided by our ability to communicate with language.

One camp thinks that there was one or more genetic mutations that turned us from apes to humans. According to that point of view, we are genetically special, and our complex language and culture was made possible by our genetic endowment.

An alternative view is that humans are not that special genetically, or that their adaptations took hold long before the emergence of fully modern behavior during the Upper Paleolithic. According to that view, one can think of humans as kindling that took the spark of culture by accident, long after it was ready to receive it. As an analogy, we can say that Upper Paleolithic brains probably had the capacity to go to the Moon, but did not have the culture for it yet: settled agriculture, science, and the industrial revolution were needed first.

I tend to the latter view myself. If a Neandertal or even Homo heidelbergensis child were raised in a modern society, they would no doubt be able to function in it, even if they weren't very bright or if they talked/moved/looked funny. The fact that these species never developed the complex cultures that modern humans did is not in itself evidence that they were innately incapable to produce them.

In any case, the comparison of the modern human/Neandertal genomes, in conjunction with developmental studies/studies of pathological variants may yet shed more light on whether modern humans do have, after all, genetic mutations that acted as the great enablers of their cultural efflorescence.

The new study frames the debate by establishing that one part of "being human", cultural transmission across the generations isn't "only human".

Culture in Humans and Apes Has the Same Evolutionary Roots

ScienceDaily (Oct. 20, 2011) — Culture is not a trait that is unique to humans. By studying orangutan populations, a team of researchers headed by anthropologist Michael Krützen from the University of Zurich has demonstrated that great apes also have the ability to learn socially and pass them down through a great many generations. The researchers provide the first evidence that culture in humans and great apes has the same evolutionary roots, thus answering the contentious question as to whether variation in behavioral patterns in orangutans are culturally driven, or caused by genetic factors and environmental influences.

Current Biology, 10.1016/j.cub.2011.09.017

Culture and Geographic Variation in Orangutan Behavior

Michael Krützen et al.

Although geographic variation in an organism's traits is often seen as a consequence of selection on locally adaptive genotypes accompanied by canalized development [1], developmental plasticity may also play a role [2,3], especially in behavior [4]. Behavioral plasticity includes both individual learning and social learning of local innovations (“culture”). Cultural plasticity is the undisputed and dominant explanation for geographic variation in human behavior. It has recently also been suggested to hold for various primates and birds [5], but this proposition has been met with widespread skepticism [6,7,8]. Here, we analyze parallel long-term studies documenting extensive geographic variation in behavioral ecology, social organization, and putative culture of orangutans [9] (genus Pongo). We show that genetic differences among orangutan populations explain only very little of the geographic variation in behavior, whereas environmental differences explain much more, highlighting the importance of developmental plasticity. Moreover, variation in putative cultural variants is explained by neither genetic nor environmental differences, corroborating the cultural interpretation. Thus, individual and cultural plasticity provide a plausible pathway toward local adaptation in long-lived organisms such as great apes and formed the evolutionary foundation upon which human culture was built.

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Modern humans bite hard

From the paper:

Our findings offer an explanation for the apparently inconsistent presence of a dentition in H. sapiens that appears well adapted to resist high bite forces relative to other extant hominids, set in a cranium and mandible that are relatively gracile and characterized by less robust musculature. Thus, the teeth of humans need to be able to resist comparable bite reaction forces to those of other extant hominids, but, because considerably less muscle force is required to achieve any given bite reaction force in the human than in other hominids, less stress is produced.

...

We conclude that although humans are well adapted to produce high peak forces with the jaw moving in rotation, they may not be as well adapted to produce and maintain high bite forces with the jaw moving in translation. Thus, Homo sapiens may be comparable to other hominids in possessing an ability to access some relatively hard foods through the application of high transitory bite forces, however, our species may be less well adapted to consume tough or hard foods that require powerful, sustained chewing.

Proceedings of the Royal Society B doi: 10.1098/rspb.2010.0509

The craniomandibular mechanics of being human

Stephen Wroe et al.

Diminished bite force has been considered a defining feature of modern Homo sapiens, an interpretation inferred from the application of two-dimensional lever mechanics and the relative gracility of the human masticatory musculature and skull. This conclusion has various implications with regard to the evolution of human feeding behaviour. However, human dental anatomy suggests a capacity to withstand high loads and two-dimensional lever models greatly simplify muscle architecture, yielding less accurate results than three-dimensional modelling using multiple lines of action. Here, to our knowledge, in the most comprehensive three-dimensional finite element analysis performed to date for any taxon, we ask whether the traditional view that the bite of H. sapiens is weak and the skull too gracile to sustain high bite forces is supported. We further introduce a new method for reconstructing incomplete fossil material. Our findings show that the human masticatory apparatus is highly efficient, capable of producing a relatively powerful bite using low muscle forces. Thus, relative to other members of the superfamily Hominoidea, humans can achieve relatively high bite forces, while overall stresses are reduced. Our findings resolve apparently discordant lines of evidence, i.e. the presence of teeth well adapted to sustain high loads within a lightweight cranium and mandible.

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Strong apes and fast humans

The paper is freely accessible.

Current Anthropology doi:10.1086/592023

The Strength of Great Apes and the Speed of Humans

Alan Walker

Abstract

Cliff Jolly developed a causal model of human origins in his paper “The Seed‐Eaters,” published in 1970. He was one of the first to attempt this, and the paper has since become a classic. I do not have such grand goals; instead, I seek to understand a major difference between the living great apes and humans. More than 50 years ago, Maynard Smith and Savage (1956) showed that the musculoskeletal systems of mammals can be adapted for strength at one extreme and speed at the other but not both. Great apes are adapted for strength—chimpanzees have been shown to be about four times as strong as fit young humans when normalized for body size. The corresponding speed that human limb systems gain at the expense of power is critical for effective human activities such as running, throwing, and manipulation, including tool making. The fossil record can shed light on when the change from power to speed occurred. I outline a hypothesis that suggests that the difference in muscular performance between the two species is caused by chimpanzees having many fewer small motor units than humans, which leads them, in turn, to contract more muscle fibers earlier in any particular task. I outline a histological test of this hypothesis.

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