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Identifying the molecular underpinnings of the neural specializations that underlie human cognitive and behavioral traits has long been of considerable interest. Much research on human-specific changes in gene expression and epigenetic marks has focused on the prefrontal cortex, a brain structure distinguished by its role in executive functions. The cerebellum shows expansion in great apes and is gaining increasing attention for its role in motor skills and cognitive processing, including language. However, relatively few molecular studies of the cerebellum in a comparative evolutionary context have been conducted. Here, we identify human-specific methylation in the lateral cerebellum relative to the dorsolateral prefrontal cortex, in a comparative study with chimpanzees ( Pan troglodytes ) and rhesus macaques ( Macaca mulatta ). Specifically, we profiled genome-wide methylation levels in the three species for each of the two brain structures and identified human-specific differentially methylated genomic regions unique to each structure. We further identified which differentially methylated regions (DMRs) overlap likely regulatory elements and determined whether associated genes show corresponding species differences in gene expression. We found greater human-specific methylation in the cerebellum than the dorsolateral prefrontal cortex, with differentially methylated regions overlapping genes involved in several conditions or processes relevant to human neurobiology, including synaptic plasticity, lipid metabolism, neuroinflammation and neurodegeneration, and neurodevelopment, including developmental disorders. Moreover, our results show some overlap with those of previous studies focused on the neocortex, indicating that such results may be common to multiple brain structures. These findings further our understanding of the cerebellum in human brain evolution.

Color vision in primates is variable across species, and it represents a rare trait in which the genetic mechanisms underlying phenotypic variation are fairly well-understood. Research on primate color vision has largely focused on adaptive explanations for observed variation, but it remains unclear why some species have trichromatic or polymorphic color vision while others are red-green color blind. Lemurs, in particular, are highly variable. While some species are polymorphic, many closely-related species are strictly dichromatic. We provide the first characterization of color vision in a wild population of red-bellied lemurs (Eulemur rubriventer, Ranomafana National Park, Madagascar) with a sample size (87 individuals; NX chromosomes = 134) large enough to detect even rare variants (0.95 probability of detection at ≥ 3% frequency). By sequencing exon 5 of the X-linked opsin gene we identified opsin spectral sensitivity based on known diagnostic sites and found this population to be dichromatic and monomorphic for a long wavelength allele. Apparent fixation of this long allele is in contrast to previously published accounts of Eulemur species, which exhibit either polymorphic color vision or only the medium wavelength opsin. This unexpected result may represent loss of color vision variation, which could occur through selective processes and/or genetic drift (e.g., genetic bottleneck). To indirectly assess the latter scenario, we genotyped 55 adult red-bellied lemurs at seven variable microsatellite loci and used heterozygosity excess and M-ratio tests to assess if this population may have experienced a recent genetic bottleneck. Results of heterozygosity excess but not M-ratio tests suggest a bottleneck might have occurred in this red-bellied lemur population. Therefore, while selection may also play a role, the unique color vision observed in this population might have been influenced by a recent genetic bottleneck. These results emphasize the need to consider adaptive and nonadaptive mechanisms of color vision evolution in primates.

The greying of human head hair is arguably the most salient marker of human aging. In wild mammal populations, greying can change with life history or environmental factors (e.g., sexual maturity in silverback gorillas). Yet, whether humans are unique in our pattern of age-related hair depigmentation is unclear. We examined the relationship between pigmentation loss in facial hair (greying) to age, population, and sex in wild and captive chimpanzees (Pan troglodytes). Digital facial photographs representing three chimpanzee populations (N = 145; ages 1-60 years) were scored for hair greying on a scale of one [~100% pigmented] to six [~0% pigmented]. Our data suggest that chimpanzee head and facial hair generally greys with age prior to mid-life (~30 years old), but afterwards, greying ceases to increase incrementally. Our results highlight that chimpanzee pigmentation likely exhibits substantial variation between populations, and that both 'grey' and pigmented phenotypes exist across various age classes. Thus, chimpanzee facial hair greying is unlikely a progressive indicator of age beyond mid-life, and thus facial greying in chimpanzees seems different from the pattern observed in humans. Whether this reflects neutral differences in senescence, or potential differences in selection pressures (e.g. related to conspecific communication), is unclear and worthy of more detailed examination across populations and taxa.

The human apolipoprotein E (APOE) gene is polymorphic, with three primary alleles (E2, E3, E4) that differ at two key non-synonymous sites. These alleles are functionally different in how they bind to lipoproteins, and this genetic variation is associated with phenotypic variation for several medical traits, including cholesterol levels, cardiovascular health, Alzheimer's disease risk, and longevity. The relative frequencies of these alleles vary across human populations, and the evolution and maintenance of this diversity is much debated. Previous studies comparing human and chimpanzee APOE sequences found that the chimpanzee sequence is most similar to the human E4 allele, although the resulting chimpanzee protein might function like the protein coded for by the human E3 allele. However, these studies have used sequence data from a single chimpanzee and do not consider whether chimpanzees, like humans, show intra-specific and subspecific variation at this locus. To examine potential intraspecific variation, we sequenced the APOE gene of 32 chimpanzees. This sample included 20 captive individuals representing the western subspecies (P. troglodytes verus) and 12 wild individuals representing the eastern subspecies (P. t. schweinfurthii). Variation in our resulting sequences was limited to one non-coding, intronic SNP, which showed fixed differences between the two subspecies. We also compared APOE sequences for all available ape genera and fossil hominins. The bonobo APOE protein is identical to that of the chimpanzee, and the Denisovan APOE exhibits all four human-specific, non-synonymous changes and appears functionally similar to the human E4 allele. We found no coding variation within and between chimpanzee populations, suggesting that the maintenance of functionally diverse APOE polymorphisms is a unique feature of human evolution.

Facial phenotypes are significant in communication with conspecifics among social primates. Less is understood about the impact of such markers in heterospecific encounters. Through behavioral and physical phenotype analyses of domesticated dogs living in human households, this study aims to evaluate the potential impact of superficial facial markings on dogs’ production of human-directed facial expressions. That is, this study explores how facial markings, such as eyebrows, patches, and widow’s peaks, are related to expressivity toward humans. We used the Dog Facial Action Coding System (DogFACS) as an objective measure of expressivity, and we developed an original schematic for a standardized coding of facial patterns and coloration on a sample of more than 100 male and female dogs (N = 103), aged from 6 months to 12 years, representing eight breed groups. The present study found a statistically significant, though weak, correlation between expression rate and facial complexity, with dogs with plainer faces tending to be more expressive (r = −0.326, p ≤ 0.001). Interestingly, for adult dogs, human companions characterized dogs’ rates of facial expressivity with more accuracy for dogs with plainer faces. Especially relevant to interspecies communication and cooperation, within-subject analyses revealed that dogs’ muscle movements were distributed more evenly across their facial regions in a highly social test condition compared to conditions in which they received ambiguous cues from their owners. On the whole, this study provides an original evaluation of how facial features may impact communication in human–dog interactions.

The evolution of facial muscles in dogs has been linked to human preferential selection of dogs whose faces appear to communicate information and emotion. Dogs who convey, especially with their eyes, a sense of perceived helplessness can elicit a caregiving response from humans. However, the facial muscles used to generate such expressions may not be uniquely present in all dogs, but rather specifically cultivated among various taxa and individuals. In a preliminary, qualitative gross anatomical evaluation of 10 canid specimens of various species, we find that the presence of two facial muscles previously implicated in human-directed canine communication, the levator anguli occuli medialis (LAOM) and the retractor anguli occuli lateralis (RAOL), was not unique to domesticated dogs (Canis familiaris). Our results suggest that these aspects of facial musculature do not necessarily reflect selection via human domestication and breeding. In addition to quantitatively evaluating more and other members of the Canidae family, future directions should include analyses of the impact of superficial facial features on canine communication and interspecies communication between dogs and humans.

Gorillas are humans’ closest living relatives after chimpanzees, and are of comparable importance for the study of human origins and evolution. Here we present the assembly and analysis of a genome sequence for the western lowland gorilla, and compare the whole genomes of all extant great ape genera. We propose a synthesis of genetic and fossil evidence consistent with placing the human–chimpanzee and human–chimpanzee–gorilla speciation events at approximately 6 and 10 million years ago. In 30% of the genome, gorilla is closer to human or chimpanzee than the latter are to each other; this is rarer around coding genes, indicating pervasive selection throughout great ape evolution, and has functional consequences in gene expression. A comparison of protein coding genes reveals approximately 500 genes showing accelerated evolution on each of the gorilla, human and chimpanzee lineages, and evidence for parallel acceleration, particularly of genes involved in hearing. We also compare the western and eastern gorilla species, estimating an average sequence divergence time 1.75 million years ago, but with evidence for more recent genetic exchange and a population bottleneck in the eastern species. The use of the genome sequence in these and future analyses will promote a deeper understanding of great ape biology and evolution. The genome of a western lowland gorilla has been sequenced and analysed, completing the genome sequences of all great ape genera, and providing evidence for parallel accelerated evolution in chimpanzee, gorilla and human lineages at a number of loci. Hominid genomes: gorilla makes four The genome of the gorilla has been sequenced, making it possible to compare the DNA of the four surviving hominid genera: human, chimpanzee, gorilla and orang-utan. The data — mainly from a female western lowland gorilla named Kamilah, but also from other gorillas representing both the western lowland and eastern lowland sub-species — imply that in almost one-third of its genome, the gorilla is closer to the human or chimpanzee than the human and chimp are to each other. Around 500 genes show accelerated evolution in gorilla, human and chimpanzee lineages, and there is evidence for parallel acceleration, particularly in genes associated with hearing. On the basis of genetic and fossil evidence, the authors suggest that the human–chimpanzee and human–chimpanzee–gorilla speciation events occurred at around 6 million and 10 million years ago respectively, whereas the two gorilla species diverged around 1.75 million years ago.

Understanding trait evolution is essential for explaining modern biological diversity, and this is particularly exemplified by studies of coloration. Recent studies have applied evolutionary models to understand animal coloration, yet we have limited knowledge of how this trait evolves in mammals in a comparative context. Here we use phylogenetic methods to examine how different traits are associated with the evolutionary diversity of primate hair color. We hypothesize that hair color evolves independently across body regions, and that variation in biological and ecological traits influence patterns of hair color evolution. To test this, we quantify the phylogenetic signal of coloration for each body region, then compare the fit of three evolutionary models and a null, non-phylogenetic model to explain color variation across 94 primate species. We then test how trait optima and rate of color evolution covary with biological traits, clade membership, and habitat. Phylogenetic signal varies across regions, with head and forelimb coloration exhibiting the highest values. Head and forelimb coloration is best explained by an Ornstein-Uhlenbeck model, which could suggest stabilizing selection, whereas a null model best fits other body regions. Rates of hair color evolution and optimal color values vary across species with different visual systems, activity patterns, habitat types, and clade memberships. These results suggest that selective pressures are acting independently across body regions and across different primate taxa. Our results emphasize the importance of investigating patterns of trait evolution across regions of the body, as well as incorporating relevant biological and ecological traits into evolutionary models.

Aim: In 1833, C. L. Gloger observed that bird populations living in warm and wet habitats were darker than those found in dry, cool areas. However, this hypothesis has seldom been evaluated, particularly for mammals. Here, we test Gloger's rule using a dataset consisting of more than 100 primate species representing all major primate clades. Location: Africa, Madagascar, Asia and the Neotropics. Methods: We used museum skins, digital photography, and colour correction software to quantify the brightness of the dorsal and ventral pelage surface of each species. We utilized the mean actual evapotranspiration (AET) within the geographic range of each species as a proxy for habitat conditions and accounted for additional variables that may influence coloration. To analyse the data, we used a generalized linear model that simultaneously accounts for the effects of phylogenetic and spatial autocorrelation. Results: We found that increasing levels of AET were significantly related to increasing pelage darkness on the dorsal surface of species, while accounting for other effects. Main conclusions: Our finding provides further support for the applicability of Gloger's rule to mammals, and is the first broad-scale evaluation for primates. The mechanism driving Gloger's rule is not easy to discern, but may include increased background matching for species living in relatively light or dark habitats, increased resistance to keratin-degrading micro-organisms in hair with large amounts of eumelanin, and/or thermoregulation.

Methylation levels have been shown to change with age at sites across the human genome. Change at some of these sites is so consistent across individuals that it can be used as an ‘epigenetic clock’ to predict an individual's chronological age to within a few years. Here, we examined how the pattern of epigenetic ageing in chimpanzees compares with humans. We profiled genome-wide blood methylation levels by microarray for 113 samples from 83 chimpanzees aged 1–58 years (26 chimpanzees were sampled at multiple ages during their lifespan). Many sites (greater than 65 000) showed significant change in methylation with age and around one-third (32%) of these overlap with sites showing significant age-related change in humans. At over 80% of sites showing age-related change in both species, chimpanzees displayed a significantly faster rate of age-related change in methylation than humans. We also built a chimpanzee-specific epigenetic clock that predicted age in our test dataset with a median absolute deviation from known age of only 2.4 years. However, our chimpanzee clock showed little overlap with previously constructed human clocks. Methylation at CpGs comprising our chimpanzee clock showed moderate heritability. Although the use of a human microarray for profiling chimpanzees biases our results towards regions with shared genomic sequence between the species, nevertheless, our results indicate that there is considerable conservation in epigenetic ageing between chimpanzees and humans, but also substantial divergence in both rate and genomic distribution of ageing-associated sites. This article is part of the theme issue ‘Evolution of the primate ageing process'.