OBJECTIVES The ability to use visual signals to identify individuals is an important feature of primate social groups, including humans. Sheehan and Nachman (2014) showed that loci linked to facial morphology had elevated levels of diversity and interpreted this as evidence that the human face is under frequency-dependent selection to enhance individual recognition (Nature Communications 5). In our study, we tested whether this pattern is found in non-human ape species, to help understand whether individual recognition might also play a role in species other than humans. MATERIALS AND METHODS We examined levels of genetic diversity in an available population genomic dataset of humans, chimpanzees, bonobos, gorillas, and orangutans for three sets of loci, (1) loci linked to facial morphology, (2) loci linked to height, and (3) neutrally evolving regions. We tested whether loci linked to facial morphology were more variable than loci linked to height or neutrally evolving loci in each of these species. RESULTS We found significantly elevated diversity in loci linked to facial morphology in chimpanzees, gorillas, and Sumatran and Bornean orangutans. DISCUSSION Our findings closely parallel those of Sheehan and Nachman and are consistent with the idea that selection for facial diversity and individual recognition has not only shaped the evolution of the human face, but it has similarly shaped the evolution of most of our closest primate relatives. We also discuss alternative hypotheses for this pattern.

Natural selection, developmental constraint, and plasticity have all been invoked as explanations for intraspecific cranial variation in humans and apes. However, global patterns of human cranial variation are congruent with patterns of genetic variation, demonstrating that population history has influenced cranial variation in humans. Here we show that this finding is not unique to Homo sapiens but is also broadly evident across extant ape species. Specifically, taxa that exhibit greater intraspecific cranial shape variation also exhibit greater genetic diversity at neutral autosomal loci. Thus, cranial shape variation within hominoid taxa reflects the population history of each species. Our results suggest that neutral evolutionary processes such as mutation, gene flow, and genetic drift have played an important role in generating cranial variation within species. These findings are consistent with previous work on human cranial morphology and improve our understanding of the evolutionary processes that generate intraspecific cranial shape diversity within hominoids. This work has implications for the analysis of selective and developmental pressures on the cranium and for interpreting shape variation in fossil hominin crania.

There is a trade-off reflected in the contrasting phenotypes of elite long-distance runners, who are typically leaner, and elite sprinters, who are usually more heavily muscled. It is unclear, however, whether and how swimmers' bodies vary across event distances from the 50 m swim, which is about a 20–30 s event, to the 10 000 m marathon swim, which is about a 2 h event. We examined data from the 2012 Olympics to test whether swimmers’ phenotypes differed across event distances. We show that across all swimming event distances, from the 50 m sprint to the 10 000 m marathon, swimmers converge on a single optimal body mass index (BMI) in men's and women's events, in marked contrast with the strong inverse relationship between BMI and event distance found in runners. The absence of a speed–endurance trade-off in the body proportions of swimmers indicates a fundamental difference in design pressures and performance capability in terrestrial versus aquatic environments.

The Papionina is a geographically widespread subtribe of African cercopithecid monkeys whose evolutionary history is of particular interest to anthropologists. The phylogenetic relationships among arboreal mangabeys (Lophocebus), baboons (Papio), and geladas (Theropithecus) remain unresolved. Molecular phylogenetic analyses have revealed marked gene tree incongruence for these taxa, and several recent concatenated phylogenetic analyses of multilocus datasets have supported different phylogenetic hypotheses. To address this issue, we investigated the phylogeny of the Lophocebus + Papio + Theropithecus group using concatenation methods, as well as alternative methods that incorporate gene tree heterogeneity to estimate a 'species tree.' Our compiled DNA sequence dataset was ∼56 kb pairs long and included 57 independent partitions. All analyses of concatenated alignments strongly supported a Lophocebus + Papio clade and a basal position for Theropithecus. The Bayesian concordance analysis supported the same phylogeny. A coalescent-based Bayesian method resulted in a very poorly resolved species tree. The topological agreement between concatenation and the Bayesian concordance analysis offers considerable support for a Lophocebus + Papio clade as the dominant relationship across the genome. However, the results of the Bayesian concordance analysis indicate that almost half the genome has an alternative history. As such, our results offer a well-supported phylogenetic hypothesis for the Papio/Lophocebus/Theropithecus trichotomy, while at the same time providing evidence for a complex evolutionary history that likely includes hybridization among lineages.

Mammalian olfaction comprises two chemosensory systems: the odorant-detecting main olfactory system (MOS) and the pheromone-detecting vomeronasal system (VNS). Mammals are diverse in their anatomical and genomic emphases on olfactory chemosensation, including the loss or reduction of these systems in some orders. Despite qualitative evidence linking the genomic evolution of the olfactory systems to specific functions and phenotypes, little work has quantitatively tested whether the genomic aspects of the mammalian olfactory chemosensory systems are correlated to anatomical diversity. We show that the genomic and anatomical variation in these systems is tightly linked in both the VNS and the MOS, though the signature of selection is different in each system. Specifically, the MOS appears to vary based on absolute organ and gene family size while the VNS appears to vary according to the relative proportion of functional genes and relative anatomical size and complexity. Furthermore, there is little evidence that these two systems are evolving in a linked fashion. The relationships between genomic and anatomical diversity strongly support a role for natural selection in shaping both the anatomical and genomic evolution of the olfactory chemosensory systems in mammals.

Malaria is a disease caused by Plasmodium parasites and is responsible for high mortality in humans. This disease is caused by four different species of Plasmodium though the main source of mortality is Plasmodium falciparum. Humans have a number of genetic adaptations that act to combat Plasmodium. One adaptation is a deletion in the SLC4A1 gene that leads to Southeast Asian ovalocytosis (SAO). There is evidence that SAO erythrocytes are resistant to multiple Plasmodium species. Here we analyze SLC4A1 in 23 primates and mammals to test for differential selective pressures among different primate lineages. Because primates are infected with both human Plasmodium parasites and their relatives, this analysis can be used to test which human Plasmodium parasite is the likely target of SAO. A significantly different pattern of molecular evolution was found in humans and African apes, species that are infected by P. falciparum and its relatives. This effect was restricted to the cytosolic domain of the SLC4A1 gene. The evidence is consistent with a different selective regime operating on this gene domain in humans and African apes, when compared to other primates and mammals. Alternatively, this pattern is consistent with a relaxation of selection or weak adaptive evolution operating on a small number of amino acids. The adaptive interpretation of the results is consistent with the SAO allele of the SLC4A1 gene interacting with P. falciparum in humans, rather than other Plasmodium parasites. However, additional investigation of the relationship between SLC4A1 variants and Plasmodium in humans and African apes is required to test whether the different selective regime in humans and African apes is due to natural selection or relaxed constraint.

A long-standing problem in primate evolution is the discord between paleontological and molecular clock estimates for the time of crown primate origins: the earliest crown primate fossils are ∼56 million y (Ma) old, whereas molecular estimates for the haplorhine-strepsirrhine split are often deep in the Late Cretaceous. One explanation for this phenomenon is that crown primates existed in the Cretaceous but that their fossil remains have not yet been found. Here we provide strong evidence that this discordance is better-explained by a convergent molecular rate slowdown in early primate evolution. We show that molecular rates in primates are strongly and inversely related to three life-history correlates: body size (BS), absolute endocranial volume (EV), and relative endocranial volume (REV). Critically, these traits can be reconstructed from fossils, allowing molecular rates to be predicted for extinct primates. To this end, we modeled the evolutionary history of BS, EV, and REV using data from both extinct and extant primates. We show that the primate last common ancestor had a very small BS, EV, and REV. There has been a subsequent convergent increase in BS, EV, and REV, indicating that there has also been a convergent molecular rate slowdown over primate evolution. We generated a unique timescale for primates by predicting molecular rates from the reconstructed phenotypic values for a large phylogeny of living and extinct primates. This analysis suggests that crown primates originated close to the K–Pg boundary and possibly in the Paleocene, largely reconciling the molecular and fossil timescales of primate evolution.

Estimation of divergence times is usually done using either the fossil record or sequence data from modern species. We provide an integrated analysis of palaeontological and molecular data to give estimates of primate divergence times that utilize both sources of information. The number of preserved primate species discovered in the fossil record, along with their geological age distribution, is combined with the number of extant primate species to provide initial estimates of the primate and anthropoid divergence times. This is done by using a stochastic forwards-modeling approach where speciation and fossil preservation and discovery are simulated forward in time. We use the posterior distribution from the fossil analysis as a prior distribution on node ages in a molecular analysis. Sequence data from two genomic regions (CFTR on human chromosome 7 and the CYP7A1 region on chromosome 8) from 15 primate species are used with the birth-death model implemented in mcmctree in PAML to infer the posterior distribution of the ages of 14 nodes in the primate tree. We find that these age estimates are older than previously reported dates for all but one of these nodes. To perform the inference, a new approximate Bayesian computation (ABC) algorithm is introduced, where the structure of the model can be exploited in an ABC-within-Gibbs algorithm to provide a more efficient analysis.

According to recent taxonomic reclassification, the primate family Hylobatidae contains four genera (Hoolock, Nomascus, Symphalangus, and Hylobates) and between 14 and 18 species, making it by far the most species-rich group of extant hominoids. Known as the “small apes”, these small arboreal primates are distributed throughout Southeast, South and East Asia. Considerable uncertainty surrounds the phylogeny of extant hylobatids, particularly the relationships among the genera and the species within the Hylobates genus. In this paper we use parsimony, likelihood, and Bayesian methods to analyze a dataset containing nearly 14 kilobase pairs, which includes newly collected sequences from X-linked, Y-linked, and mitochondrial loci together with data from previous mitochondrial studies. Parsimony, likelihood, and Bayesian analyses largely failed to find a significant difference among phylogenies with any of the four genera as the most basal taxon. All analyses, however, support a tree with Hylobates and Symphalangus as most closely related genera. One strongly supported phylogenetic result within the Hylobates genus is that Hylobates pileatus is the most basal taxon. Multiple analyses failed to find significant support for any singular genus-level phylogeny. While it is natural to suspect that there might not be sufficient data for phylogenetic resolution (whenever that situation occurs), an alternative hypothesis relating to the nature of gibbon speciation exists. This lack of resolution may be the result of a rapid radiation or a sudden vicariance event of the hylobatid genera, and it is likely that a similarly rapid radiation occurred within the Hylobates genus. Additional molecular and paleontological evidence are necessary to better test among these, and other, hypotheses of hylobatid evolution.

The phylogenetic position of tarsiers within the primates has been a controversial subject for over a century. Despite numerous morphological and molecular studies, there has been weak support for grouping tarsiers with either strepsirrhine primates in a prosimian clade or with anthropoids in a haplorrhine clade. Here, we take advantage of the recently released whole genome assembly of the Philippine tarsier, Tarsius syrichta, in order to infer the phylogenetic relationship of Tarsius within the order Primates. We also present estimates of divergence times within the primates. Using a 1.26 million base pair multiple sequence alignment derived from 1078 orthologous genes, we provide overwhelming statistical support for the presence of a haplorrhine clade. We also present divergence date estimates using local relaxed molecular clock methods. The estimated time of the most recent common ancestor of extant Primates ranged from 64.9 Ma to 72.6 Ma, and haplorrhines were estimated to have a most recent common ancestor between 58.9 Ma and 68.6 Ma. Examination of rates of nucleotide substitution in the three major extant primate clades show that anthropoids have a slower substitution rate than either strepsirrhines or tarsiers. Our results provide the framework on which primate morphological, reproductive, and genomic features can be reconstructed in the broader context of mammalian phylogeny.