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  1. While low serotonergic activity is often associated with psychological disorders such as depression, anxiety, mood, and personality disorders, variations in serotonin also contribute to normal personality differences. In this study, we investigated the role of blood DNA methylation levels at individual CpG sites of two key serotonergic genes (serotonin receptor gene 1A, HTR1A; serotonin transporter gene, SLC6A4) in predicting the personalities of captive chimpanzees. We found associations between methylation at 9/48 CpG sites with four personality dimensions: Dominance, Reactivity/Dependability, Agreeableness, and Openness. Directionality of effects were CpG location-dependent and confirmed a role of serotonergic methylation in reducing anxiety (Dominance) and aggression-related personality (Reactivity/Undependability) while simultaneously promoting prosocial (Agreeableness) and exploratory personalities (Openness). Although early-life adversity has been shown to impact serotonergic methylation patterns in other species, here, atypical early social rearing experiences only had a modest impact on CpG methylation levels in this chimpanzee sample. The precise environmental factors impacting serotonergic methylation in chimpanzees remain to be identified. Nevertheless, our study suggests a role in shaping natural variation in animal personalities. The results of this study offer a basis for future hypothesis-driven testing in additional populations and species to better understand the impact of ecology and evolution on complex behavioral traits.

     
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  2. Gojobori, Takashi (Ed.)
    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. 
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  3. Abstract

    Joint attention (JA) is an important milestone in human infant development and is predictive of the onset of language later in life. Clinically, it has been reported that children at risk for or with a diagnosis of autism spectrum disorder (ASD) perform more poorly on measures of JA compared to neurotypical controls. JA is not unique to humans but has also been reported in great apes and to a lesser extent in more distantly related monkeys. Further, individual differences in JA among chimpanzees are associated with polymorphisms in the vasopressin and oxytocin genes,AVPR1AandOXTR. Here, we tested whether individual variation in DNA methylation ofOXTRandAVPR1Awere associated with performance on JA tasks in chimpanzees. We found that individual differences in JA performance was associated withAVPR1Amethylation, but notOXTRmethylation in the chimpanzees. The collective results provide further evidence of the role ofAVPR1Ain JA abilities in chimpanzees. The results further suggest that methylation values forAVPR1Amay be useful biomarkers for identifying individuals at risk for ASD or related neurodevelopmental disorders associated with impairments in JA abilities.

     
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  4. Abstract Objectives

    Hair (i.e., pelage/fur) is a salient feature of primate (including human) diversity and evolution—serving functions tied to thermoregulation, protection, camouflage, and signaling—but wild primate pelage evolution remains relatively understudied. Specifically, assessing multiple hypotheses across distinct phylogenetic scales is essential but is rarely conducted. We examine whole body hair color and density variation across Indriidae (Avahi,Indri,Propithecus)—a lineage that, like humans, exhibits vertical posture (i.e., their whole bodies are vertical to the sun).

    Materials and methods

    Our analyses consider multiple phylogenetic scales (family‐level, genus‐level) and hypotheses (e.g., Gloger's rule, the body cooling hypotheses). We obtain hair color and density from museum and/or wild animals, opsin genotypes from wild animals, and climate data from WorldClim. To analyze our data, we use phylogenetic generalized linear mixed models (PGLMM) using Markov chain Monte Carlo algorithms.

    Results

    Our results show that across the Indriidae family, darker hair is typical in wetter regions. However, withinPropithecus, dark black hair is common in colder forest regions. Results also show pelage redness increases in populations exhibiting enhanced color vision. Lastly, we find follicle density on the crown and limbs increases in dry and open environments.

    Discussion

    This study highlights how different selective pressures across distinct phylogenetic scales have likely acted on primate hair evolution. Specifically, our data acrossPropithecusmay implicate thermoregulation and is the first empirical evidence of Bogert's rule in mammals. Our study also provides rare empirical evidence supporting an early hypothesis on hominin hair evolution.

     
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  5. Abstract

    Studying genetic mechanisms underlying primate brain morphology can provide insight into the evolution of human brain structure and cognition. In humans, loss‐of‐function mutations in the gene coding for ASPM (Abnormal Spindle Microtubule Assembly) have been associated with primary microcephaly, which is defined by a significantly reduced brain volume, intellectual disability and delayed development. However, less is known about the effects of commonASPMvariation in humans and other primates. In this study, we characterized the degree of coding variation atASPMin a large sample of chimpanzees (N = 241), and examined potential associations between genotype and various measures of brain morphology. We identified and genotyped five non‐synonymous polymorphisms in exons 3 (V588G), 18 (Q2772K, K2796E, C2811Y) and 27 (I3427V). Using T1‐weighted magnetic resonance imaging of brains, we measured total brain volume, cerebral gray and white matter volume, cerebral ventricular volume, and cortical surface area in the same chimpanzees. We found a potential association betweenASPMV588G genotype and cerebral ventricular volume but not with the other measures. Additionally, we found that chimpanzee, bonobo, and human lineages each independently show a signature of acceleratedASPMprotein evolution. Overall, our results suggest the potential effects ofASPMvariation on cerebral cortical development, and emphasize the need for further functional studies. These results are the first evidence suggestingASPMvariation might play a role in shaping natural variation in brain structure in nonhuman primates.

     
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  6. Abstract

    Lemurs are among the world's most threatened mammals. The critically endangered black‐and‐white ruffed lemur (Varecia variegata), in particular, has recently experienced rapid population declines due to habitat loss, ecological sensitivities to habitat degradation, and extensive human hunting pressure. Despite this, a recent study indicates that ruffed lemurs retain among the highest levels of genetic diversity for primates. Identifying how this diversity is apportioned and whether gene flow is maintained among remnant populations will help to diagnose and target conservation priorities. We sampled 209 individuals from 19 sites throughout the remainingV. variegatarange. We used 10 polymorphic microsatellite loci and ~550 bp of mtDNAsequence data to evaluate genetic structure and population dynamics, including dispersal patterns and recent population declines. Bayesian cluster analyses identified two distinct genetic clusters, which optimally partitioned data into populations occurring on either side of theMangoro River. Localities north of the Mangoro were characterized by greater genetic diversity, greater gene flow (lower genetic differentiation) and higher mtDNAhaplotype and nucleotide diversity than those in the south. Despite this, genetic differentiation across all sites was high, as indicated by high averageFST(0.247) and ΦST(0.544), and followed a pattern of isolation‐by‐distance. We use these results to suggest future conservation strategies that include an effort to maintain genetic diversity in the north and restore connectivity in the south. We also note the discordance between patterns of genetic differentiation and current subspecies taxonomy, and encourage a re‐evaluation of conservation management units moving forward.

     
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