Structurally divergent and recurrently mutated regions of primate genomes.

We sequenced and assembled using multiple long-read sequencing technologies the genomes of chimpanzee, bonobo, gorilla, orangutan, gibbon, macaque, owl monkey, and marmoset. We identified 1,338,997 lineage-specific fixed structural variants (SVs) disrupting 1,561 protein-coding genes and 136,932 regulatory elements, including the most complete set of human-specific fixed differences. We estimate that 819.47 Mbp or ∼27% of the genome has been affected by SVs across primate evolution. We identify 1,607 structurally divergent regions wherein recurrent structural variation contributes to creating SV hotspots where genes are recurrently lost (e.g., CARD, C4, and OLAH gene families) and additional lineage-specific genes are generated (e.g., CKAP2, VPS36, ACBD7, and NEK5 paralogs), becoming targets of rapid chromosomal diversification and positive selection (e.g., RGPD gene family). High-fidelity long-read sequencing has made these dynamic regions of the genome accessible for sequence-level analyses within and between primate species.

Factors influencing terrestriality in primates of the Americas and Madagascar.

Among mammals, the order Primates is exceptional in having a high taxonomic richness in which the taxa are arboreal, semiterrestrial, or terrestrial. Although habitual terrestriality is pervasive among the apes and African and Asian monkeys (catarrhines), it is largely absent among monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines), which are mostly arboreal. Numerous ecological drivers and species-specific factors are suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and current environmental conditions may provide analogous scenarios to those transitional periods. Therefore, we investigated predominantly arboreal, diurnal primate genera from the Americas and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat canopy cover, predation risk, maximum temperature, precipitation, primate species richness, human population density, and distance to roads) or species-specific traits (body mass, group size, and degree of frugivory) associate with increased terrestriality. We collated 150,961 observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in the Americas. Multiple factors were associated with ground use in these otherwise arboreal species, including increased temperature, a decrease in canopy cover, a dietary shift away from frugivory, and larger group size. These factors mostly explain intraspecific differences in terrestriality. As humanity modifies habitats and causes climate change, our results suggest that species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift toward greater ground use.

Ecological and genetic variables co-vary with social group identity to shape the gut microbiome of a pair-living primate.

Primates exhibit diverse social systems that are intricately linked to their biology, behavior, and evolution, all of which influence the acquisition and maintenance of their gut microbiomes (GMs). However, most studies of wild primate populations focus on taxa with relatively large group sizes, and few consider pair-living species. To address this gap, we investigate how a primate's social system interacts with key environmental, social, and genetic variables to shape the GM in pair-living, red-bellied lemurs (Eulemur rubriventer). Previous research on this species suggests that social interactions within groups influence interindividual microbiome similarity; however, the impacts of other nonsocial variables and their relative contributions to gut microbial variation remain unclear. We sequenced the 16S ribosomal RNA hypervariable V4-V5 region to characterize the GM from 26 genotyped individuals across 11 social groups residing in Ranomafana National Park, Madagascar. We estimated the degree to which sex, social group identity, genetic relatedness, dietary diversity, and home range proximity were associated with variation in the gut microbial communities residing in red-bellied lemurs. All variables except sex played a significant role in predicting GM composition. Our model had high levels of variance inflation, inhibiting our ability to determine which variables were most predictive of gut microbial composition. This inflation is likely due to red-bellied lemurs' pair-living, pair-bonded social system that leads to covariation among environmental, social, and genetic variables. Our findings highlight some of the factors that predict GM composition in a tightly bonded, pair-living species and identify variables that require further study. We propose that future primate microbiome studies should simultaneously consider environmental, social, and genetic factors to improve our understanding of the relationships among sociality, the microbiome, and primate ecology and evolution.

Primate innate immune responses to bacterial and viral pathogens reveals an evolutionary trade-off between strength and specificity.

Despite their close genetic relatedness, apes and African and Asian monkeys (AAMs) differ in their susceptibility to severe bacterial and viral infections that are important causes of human disease. Such differences between humans and other primates are thought to be a result, at least in part, of interspecies differences in immune response to infection. However, because of the lack of comparative functional data across species, it remains unclear in what ways the immune systems of humans and other primates differ. Here, we report the whole-genome transcriptomic responses of ape species (human and chimpanzee) and AAMs (rhesus macaque and baboon) to bacterial and viral stimulation. We find stark differences in the responsiveness of these groups, with apes mounting a markedly stronger early transcriptional response to both viral and bacterial stimulation, altering the transcription of ∼40% more genes than AAMs. Additionally, we find that genes involved in the regulation of inflammatory and interferon responses show the most divergent early transcriptional responses across primates and that this divergence is attenuated over time. Finally, we find that relative to AAMs, apes engage a much less specific immune response to different classes of pathogens during the early hours of infection, up-regulating genes typical of anti-viral and anti-bacterial responses regardless of the nature of the stimulus. Overall, these findings suggest apes exhibit increased sensitivity to bacterial and viral immune stimulation, activating a broader array of defense molecules that may be beneficial for early pathogen killing at the potential cost of increased energy expenditure and tissue damage.

Subjective Reactions to First Coitus in Relation to Participant Sex, Partner Age, and Context in a German Nationally Representative Sample of Adolescents and Young Adults.

Analysis of a Finnish nationally representative student sample found that subjective reactions to first intercourse (mostly heterosexual; usually in adolescence) were highly positive for boys and mostly positive for girls, whether involved with peers or adults (Rind, 2022). The present study examined the generality of these findings by examining subjective reactions to first coitus (heterosexual intercourse) in a German nationally representative sample of young people (data collected in 2014). Most first coitus was postpubertal. Males reacted mostly positively and uncommonly negatively in similar fashion in all age pairings: boy-girl (71% positive, 13% negative); boy-woman (73% positive; 17% negative); man-woman (73% positive, 15% negative). Females' reactions were more mixed, similar in the girl-boy (48% positive; 37% negative) and woman-man (46% positive, 36% negative) groups, but less favorable in the girl-man group (32% positive, 47% negative). In logistic regressions, adjusting for other factors, rates of positive reactions were unrelated to age groups. These rates did increase, in order of importance, when participants were male, their partners were close, they expected the coitus to happen, and they affirmatively wanted it. Reaction rates were computed from the Finnish sample, restricting cases to first coitus occurring in the 2000s, and then compared to minors' reactions in the German sample. The Finns reacted more favorably, similarly in both minor-peer and minor-adult coitus, with twice the odds of reacting positively. It was argued that this discrepancy was due to cultural differences (e.g., Finnish culture is more sex-positive). To account for the reaction patterns shown in the adolescent-adult coitus, sizably at odds with expectations from mainstream professional thinking, an evolutionary framework was employed.

Evolution of regulatory signatures in primate cortical neurons at cell-type resolution.

The human cerebral cortex contains many cell types that likely underwent independent functional changes during evolution. However, cell-type-specific regulatory landscapes in the cortex remain largely unexplored. Here we report epigenomic and transcriptomic analyses of the two main cortical neuronal subtypes, glutamatergic projection neurons and GABAergic interneurons, in human, chimpanzee, and rhesus macaque. Using genome-wide profiling of the H3K27ac histone modification, we identify neuron-subtype-specific regulatory elements that previously went undetected in bulk brain tissue samples. Human-specific regulatory changes are uncovered in multiple genes, including those associated with language, autism spectrum disorder, and drug addiction. We observe preferential evolutionary divergence in neuron subtype-specific regulatory elements and show that a substantial fraction of pan-neuronal regulatory elements undergoes subtype-specific evolutionary changes. This study sheds light on the interplay between regulatory evolution and cell-type-dependent gene-expression programs, and provides a resource for further exploration of human brain evolution and function.

Archimetrosis: the evolution of a disease and its extant presentation : Pathogenesis and pathophysiology of archimetrosis (uterine adenomyosis and endometriosis).

PURPOSE: This article presents a novel concept of the evolution and, thus, the pathogenesis of uterine adenomyosis as well as peritoneal and peripheral endometriosis. Presently, no unifying denomination of this nosological entity exists. METHODS: An extensive search of the literature on primate evolution was performed. This included comparative functional morphology with special focus on the evolution of the birthing process that fundamentally differs between the haplorrhine primates and most of the other eutherian mammals. The data were correlated with the results of own research on the pathophysiology of human archimetrosis and with the extant presentation of the disease. RESULTS: The term Archimetrosis is suggested as a denomination of the nosological entity. Archimetrosis occurs in human females and also in subhuman primates. There are common features in the reproductive process of haplorrhine primates such as spontaneous ovulation and corpus luteum formation, spontaneous decidualization and menstruation. These have fused Müllerian ducts resulting in a uterus simplex. Following a usually singleton pregnancy, the fetus is delivered in the skull position. Some of these features are shared by other mammals, but not in that simultaneous fashion. In haplorrhine primates, with the stratum vasculare, a new myometrial layer has evolved during the time of the Cretaceous-Terrestrial Revolution (KTR) that subserves expulsion of the conceptus and externalization of menstrual debris in non-conceptive cycles. Hypercontractility of this layer has evolved as an advantage with respect to the survival of the mother and the birth of a living child during delivery and may be experienced as primary dysmenorrhea during menstruation. It may result in tissue injury by the sheer power of the contractions and possibly by the associated uterine ischemia. Moreover, the lesions at extra-uterine sites appear to be maintained by biomechanical stress. CONCLUSIONS: Since the pathogenesis of archimetrosis is connected with the evolution of the stratum vasculare, tissue injury and repair (TIAR) turns out to be the most parsimonious explanation for the development of the disease based on clinical, experimental and evolutionary evidence. Furthermore, a careful analysis of the published clinical data suggests that, in the risk population with uterine hypercontractility, the disease develops with a yet to be defined latency phase after the onset of the biomechanical injury. This opens a new avenue of prevention of the disease in potentially affected women that we consider to be primarily highly fertile.

The Pop-Gen Pipeline Platform: A Software Platform for Population Genomic Analyses.

The Pop-Gen Pipeline Platform (PPP) is a software platform for population genomic analyses. The PPP was designed as a collection of scripts that facilitate common population genomic workflows in a consistent and standardized Python environment. Functions were developed to encompass entire workflows, including input preparation, file format conversion, various population genomic analyses, and output generation. The platform has also been developed with reproducibility and extensibility of analyses in mind. The PPP is an open-source package that is available for download and use at https://ppp.readthedocs.io/en/latest/PPP_pages/install.html.

Functional and Adaptive Significance of Promoter Mutations That Affect Divergent Myocardial Expressions of TRIM72 in Primates.

Cis-regulatory elements play important roles in tissue-specific gene expression and in the evolution of various phenotypes, and mutations in promoters and enhancers may be responsible for adaptations of species to environments. TRIM72 is a highly conserved protein that is involved in energy metabolism. Its expression in the heart varies considerably in primates, with high levels of expression in Old World monkeys and near absence in hominids. Here, we combine phylogenetic hypothesis testing and experimentation to demonstrate that mutations in promoter are responsible for the differences among primate species in the heart-specific expression of TRIM72. Maximum likelihood estimates of lineage-specific substitution rates under local-clock models show that relative to the evolutionary rate of introns, the rate of promoter was accelerated by 78% in the common ancestor of Old World monkeys, suggesting a role for positive selection in the evolution of the TRIM72 promoter, possibly driven by selective pressure due to changes in cardiac physiology after species divergence. We demonstrate that mutations in the TRIM72 promoter account for the differential myocardial TRIM72 expression of the human and the rhesus macaque. Furthermore, changes in TRIM72 expression alter the expression of genes involved in oxidative phosphorylation, which in turn affects mitochondrial respiration and cardiac energy capacity. On a broader timescale, phylogenetic regression analyses of data from 29 mammalian species show that mammals with high cardiac expression of TRIM72 have high heart rate, suggesting that the expression changes of TRIM72 may be related to differences in the heart physiology of those species.

Diverse Molecular Mechanisms Contribute to Differential Expression of Human Duplicated Genes.

Emerging evidence links genes within human-specific segmental duplications (HSDs) to traits and diseases unique to our species. Strikingly, despite being nearly identical by sequence (>98.5%), paralogous HSD genes are differentially expressed across human cell and tissue types, though the underlying mechanisms have not been examined. We compared cross-tissue mRNA levels of 75 HSD genes from 30 families between humans and chimpanzees and found expression patterns consistent with relaxed selection on or neofunctionalization of derived paralogs. In general, ancestral paralogs exhibited greatest expression conservation with chimpanzee orthologs, though exceptions suggest certain derived paralogs may retain or supplant ancestral functions. Concordantly, analysis of long-read isoform sequencing data sets from diverse human tissues and cell lines found that about half of derived paralogs exhibited globally lower expression. To understand mechanisms underlying these differences, we leveraged data from human lymphoblastoid cell lines (LCLs) and found no relationship between paralogous expression divergence and post-transcriptional regulation, sequence divergence, or copy-number variation. Considering cis-regulation, we reanalyzed ENCODE data and recovered hundreds of previously unidentified candidate CREs in HSDs. We also generated large-insert ChIP-sequencing data for active chromatin features in an LCL to better distinguish paralogous regions. Some duplicated CREs were sufficient to drive differential reporter activity, suggesting they may contribute to divergent cis-regulation of paralogous genes. This work provides evidence that cis-regulatory divergence contributes to novel expression patterns of recent gene duplicates in humans.

Molecular diversity and phenotypic pleiotropy of ancient genomic regulatory loci derived from human endogenous retrovirus type H (HERVH) promoter LTR7 and HERVK promoter LTR5_Hs and their contemporary impacts on pathophysiology of Modern Humans.

Timelines of population-level effects of viruses on humans varied from the evolutionary scale of million years to contemporary spread of viral infections. Correspondingly, these events are exemplified by: (i) emergence of human endogenous retroviruses (HERVs) from ancient germline infections leading to stable integration of viral genomes into human chromosomes; and (ii) wide-spread viral infections reaching a global pandemic state such as the COVID-19 pandemic. Despite significant efforts, understanding of HERV's roles in governance of genomic regulatory networks, their impacts on primate evolution and development of human-specific physiological and pathological phenotypic traits remains limited. Remarkably, present analyses revealed that expression of a dominant majority of genes (1696 of 1944 genes; 87%) constituting high-confidence down-steam regulatory targets of defined HERV loci was significantly altered in cells infected with the SARS-CoV-2 coronavirus, a pathogen causing the global COVID-19 pandemic. This study focused on defined sub-sets of DNA sequences derived from HERVs that are expressed at specific stages of human preimplantation embryogenesis and exert regulatory actions essential for self-renewal and pluripotency. Evolutionary histories of LTR7/HERVH and LTR5_Hs/HERVK were charted based on evidence of the earliest presence and expansion of highly conserved (HC) LTR sequences. Sequence conservation analyses of most recent releases 17 primate species' genomes revealed that LTR7/HERVH have entered germlines of primates in Africa after the separation of the New World Monkey lineage, while LTR5_Hs/HERVK successfully colonized primates' germlines after the segregation of Gibbons' species. Subsequently, both LTR7 and LTR5_Hs undergo a marked ~ fourfold-fivefold expansion in genomes of Great Apes. Timelines of quantitative expansion of both LTR7 and LTR5_Hs loci during evolution of Great Apes appear to replicate the consensus evolutionary sequence of increasing cognitive and behavioral complexities of non-human primates, which seems particularly striking for LTR7 loci and 11 distinct LTR7 subfamilies. Consistent with previous reports, identified in this study, 351 human-specific (HS) insertions of LTR7 (175 loci) and LTR5_Hs (176 loci) regulatory sequences have been linked to genes implicated in establishment and maintenance of naïve and primed pluripotent states and preimplantation embryogenesis phenotypes. Unexpectedly, HS-LTRs manifest regulatory connectivity to genes encoding markers of 12 distinct cells' populations of fetal gonads, as well as genes implicated in physiology and pathology of human spermatogenesis, including Y-linked spermatogenic failure, oligo- and azoospermia. Granular interrogations of genes linked with 11 distinct LTR7 subfamilies revealed that mammalian offspring survival (MOS) genes seem to remain one of consistent regulatory targets throughout ~ 30 MYA of the divergent evolution of LTR7 loci. Differential GSEA of MOS versus non-MOS genes identified clearly discernable dominant enrichment patterns of phenotypic traits affected by MOS genes linked with LTR7 (562 MOS genes) and LTR5_Hs (126 MOS genes) regulatory loci across the large panel of genomics and proteomics databases reflecting a broad spectrum of human physiological and pathological traits. GSEA of LTR7-linked MOS genes identified more than 2200 significantly enriched records of human common and rare diseases and gene signatures of 466 significantly enriched records of Human Phenotype Ontology traits, including Autosomal Dominant (92 genes) and Autosomal Recessive (93 genes) Inheritance. LTR7 regulatory elements appear linked with genes implicated in functional and morphological features of central nervous system, including synaptic transmission and protein-protein interactions at synapses, as well as gene signatures differentially regulated in cells of distinct neurodevelopmental stages and morphologically diverse cell types residing and functioning in human brain. These include Neural Stem/Precursor cells, Radial Glia cells, Bergman Glia cells, Pyramidal cells, Tanycytes, Immature neurons, Interneurons, Trigeminal neurons, GABAergic neurons, and Glutamatergic neurons. GSEA of LTR7-linked genes identified significantly enriched gene sets encoding markers of more than 80 specialized types of neurons and markers of 521 human brain regions, most prominently, subiculum and dentate gyrus. Identification and characterization of 1944 genes comprising high-confidence down-steam regulatory targets of LTR7 and/or LTR5_Hs loci validated and extended these observations by documenting marked enrichments for genes implicated in neoplasm metastasis, intellectual disability, autism, multiple cancer types, Alzheimer's, schizophrenia, and other brain disorders. Overall, genes representing down-stream regulatory targets of ancient retroviral LTRs exert the apparently cooperative and exceedingly broad phenotypic impacts on human physiology and pathology. This is exemplified by altered expression of 93% high-confidence LTR targets in cells infected by contemporary viruses, revealing a convergence of virus-inflicted aberrations on genomic regulatory circuitry governed by ancient retroviral LTR elements and interference with human cells' differentiation programs.

A morphometric analysis of early Eocene Euprimate tarsals from Gujarat, India.

Early Eocene primate postcranial bones from the Vastan lignite mine of Gujarat, India, have proven useful for understanding the haplorhine and strepsirrhine divergence. Previous analyses of material assigned to Asiadapidae supported interpretations that these primates were generalized arboreal quadrupeds, while the omomyid Vastanomys was likely to have been more proficient leaper than asiadapids. More recent examinations of long bone cross-sectional properties and calcaneal elongation have complicated the behavioral interpretations of these fossils. This study examines whole talar and calcaneal morphology of the Vastan material to refine the locomotor reconstructions of these fossils. A comparative sample of extant primate species representing various locomotor behaviors was obtained by accessing surface models from MorphoSource.org. Surface models of fossil specimens attributed to Asiadapis cambayensis, Marcgodinotius indicus, and Vastanomys major were generated from micro-computed tomography scans. A morphological analysis was carried out using weighted spherical harmonics, a Fourier-based method that represents surfaces using coefficients associated with a common set of spherical harmonic functions. The coefficients describing each surface were then used as shape variables in a principal components analysis. Significant differences between locomotor groups were assessed using nonparametric tests. Results from extant comparative samples show that locomotor behavior can be predicted from both talar and calcaneal morphology when phylogenetic relationships are known. Consistent with previous analyses, our results indicate that Asiadapis cambayensis and Marcgodinotius indicus were likely arboreal quadrupeds with some leaping capabilities. Vastanomys major is reconstructed as an arboreal quadruped with greater leaping proficiency than its asiadapid counterparts based on its talar morphology.

Morphological integration and evolutionary potential of the primate shoulder: Variation among taxa and implications for genetic covariances with the basicranium, pelvis, and arm.

Within the primate order, the morphology of the shoulder girdle is immensely variable and has been shown to reflect the functional demands of the upper limb. The observed morphological variation among extant primate taxa consequently has been hypothesized to be driven by selection for different functional demands. Evolutionary analyses of the shoulder girdle often assess this anatomical region, and its traits, individually, therefore implicitly assuming independent evolution of the shoulder girdle. However, the primate shoulder girdle has developmental and functional covariances with the basicranium and pelvic girdle that have been shown to potentially influence its evolution. It is unknown whether these relationships are similar or even present across primate taxa, and how they may affect morphological variation among primates. This study evaluates the strength of covariance and evolutionary potential across four anatomical regions: shoulder girdle, basicranium, pelvis, and distal humerus. Measures of morphological integration and evolutionary potential (conditioned covariance and evolutionary flexibility) are assessed across eight anthropoid primate taxa. Results demonstrate a consistent pattern of morphological constraint within paired anatomical regions across primates. Differences in evolutionary flexibility are observed among primate genera, with humans having the highest evolutionary potential overall. This pattern does not follow functional differences, but rather a separation between monkeys and apes. Therefore, evolutionary hypotheses of primate shoulder girdle morphological variation that evaluate functional demands alone may not account for the effect of these relationships. Collectively, our findings suggest differences in genetic covariance among anatomical regions may have contributed to the observable morphological variation among taxa.

Morphological affinities of a fossil ulna (KNM-WS 65401) from Buluk, Kenya.

The morphological affinities of a primate proximal ulna (KNM-WS 65401) recovered from the late Early Miocene site Buluk, Kenya, are appraised. Nineteen three-dimensional landmarks on ulnae from 36 extant anthropoid species (n = 152 individuals) and KNM-WS 65401, as well as a subset of 14 landmarks on six ulnae belonging to other East African Miocene catarrhine taxa, were collected. To quantify ulnar shape, three-dimensional geometric morphometric techniques were used and linear dimensions commonly cited in the literature were derived from the landmark data. KNM-WS 65401 is situated between monkeys and hominoids in the principal components morphospace. KNM-WS 65401 shares features such as a short olecranon process, broad trochlear notch, and laterally oriented radial notch with extant hominoids, whereas features such as an anteriorly directed trochlear notch and flat, proximodistally elongated, and anteroposteriorly narrow radial notch are shared with extant monkeys. Principal component scores and linear metrics generally align KNM-WS 65401 with both suspensors and arboreal quadrupeds, but quadratic and linear discriminant analyses of principal component score data provide posterior probabilities of 80% and 83%, respectively, for assignment of KNM-WS 65401 to the suspensory group. Compared with fossil ulnae from other Miocene primates, KNM-WS 65401 is morphologically most distinct from KNM-LG 6, attributed to Dendropithecus macinnesi, and morphologically most similar to KNM-WK 16950R, attributed to Turkanapithecus kalakolensis. The KNM-WS 65401 individual likely possessed more enhanced capabilities for elbow joint extension, perhaps during suspensory behaviors, compared with other Miocene primates in the sample.

The sensory ecology of primate food perception, revisited.

Twenty years ago, Dominy and colleagues published "The sensory ecology of primate food perception," an impactful review that brought new perspectives to understanding primate foraging adaptations. Their review synthesized information on primate senses and explored how senses informed feeding behavior. Research on primate sensory ecology has seen explosive growth in the last two decades. Here, we revisit this important topic, focusing on the numerous new discoveries and lines of innovative research. We begin by reviewing each of the five traditionally recognized senses involved in foraging: audition, olfaction, vision, touch, and taste. For each sense, we provide an overview of sensory function and comparative ecology, comment on the state of knowledge at the time of the original review, and highlight advancements and lingering gaps in knowledge. Next, we provide an outline for creative, multidisciplinary, and innovative future research programs that we anticipate will generate exciting new discoveries in the next two decades.

Palaeoecological differences underlie rare co-occurrence of Miocene European primates.

BACKGROUND: The two main primate groups recorded throughout the European Miocene, hominoids and pliopithecoids, seldom co-occur. Due to both their rarity and insufficiently understood palaeoecology, it is currently unclear whether the infrequent co-occurrence of these groups is due to sampling bias or reflects different ecological preferences. Here we rely on the densely sampled primate-bearing sequence of Abocador de Can Mata (ACM) in Spain to test whether turnovers in primate assemblages are correlated with palaeoenvironmental changes. We reconstruct dietary evolution through time (ca. 12.6-11.4 Ma), and hence climate and habitat, using tooth-wear patterns and carbon and oxygen isotope compositions of enamel of the ubiquitous musk-deer Micromeryx. RESULTS: Our results reveal that primate species composition is strongly correlated with distinct environmental phases. Large-bodied hominoids (dryopithecines) are recorded in humid, densely-forested environments on the lowermost portion of the ACM sequence. In contrast, pliopithecoids inhabited less humid, patchy ecosystems, being replaced by dryopithecines and the small-bodied Pliobates toward the top of the series in gallery forests embedded in mosaic environments. CONCLUSIONS: These results support the view that pliopithecoid primates preferred less humid habitats than hominoids, and reveal that differences in behavioural ecology were the main factor underpinning their rare co-occurrence during the European Miocene. Our findings further support that ACM hominoids, like Miocene apes as a whole, inhabited more seasonal environments than extant apes. Finally, this study highlights the importance of high-resolution, local investigations to complement larger-scale analyses and illustrates that continuous and densely sampled fossiliferous sequences are essential for deciphering the complex interplay between biotic and abiotic factors that shaped past diversity.

Evidence for the loss and recovery of SLAMF9 during human evolution: implications on Dollo's law.

Signaling lymphocyte activation molecule family member 9 (SLAMF9) is a cell surface protein of the CD2/SLAM family of leukocyte surface receptors. It is conserved throughout mammals and has roles in the initiation of inflammatory responses and regulation of plasmacytoid dendritic cell function. Through comparison of reference sequences encoding SLAMF9 in human, mouse, and primate sequences, we have determined that the SLAMF9 gene underwent successive mutation events, resulting in the loss of the protein and subsequent recovery of a less stable version. The mutations included a single base pair deletion in the second exon and a change in the splice acceptor site of that same exon. These changes would have had the effect of creating and later repairing a frameshift in the coding sequence. These events took place since the divergence of the human lineage from the chimpanzee-human last common ancestor and represent the first known case of the functional loss and recovery of a gene within the human lineage.

Increased performance in juvenile baboons is consistent with ontogenetic changes in morphology.

OBJECTIVES: In many primates, the greater proportion of climbing and suspensory behaviors in the juvenile repertoire likely necessitates good grasping capacities. Here, we tested whether very young individuals show near-maximal levels of grasping strength, and whether such an early onset of grasping performance could be explained by ontogenetic variability in the morphology of the limbs in baboons. MATERIAL AND METHODS: We quantified a performance trait, hand pull strength, at the juvenile and adult stages in a cross-sectional sample of 15 olive baboons (Papio anubis). We also quantified bone dimensions (i.e., lengths, widths, and heights) of the fore- (n = 25) and hind limb (n = 21) elements based on osteological collections covering the whole development of olive baboons. RESULTS: One-year old individuals demonstrated very high pull strengths (i.e., 200% of the adult performance, relative to body mass), that are consistent with relatively wider phalanges and digit joints in juveniles. The mature proportions and shape of the forelimb elements appeared only at full adulthood (i.e., ≥4.5 years), whereas the mature hind limb proportions and shape were observed much earlier during development. DISCUSSION: These changes in limb performance and morphology across ontogeny may be explained with regard to behavioral transitions that olive baboons experience during their development. Our findings highlight the effect of infant clinging to mother, an often-neglected feature when discussing the origins of grasping in primates. The differences in growth patterns, we found between the forelimb and the hind limb further illustrate their different functional roles, having likely evolved under different ecological pressures (manipulation and locomotion, respectively).

Human exonization through differential nucleosome occupancy.

Nucleosomal modifications have been implicated in fundamental epigenetic regulation, but the roles of nucleosome occupancy in shaping changes through evolution remain to be addressed. Here we present high-resolution nucleosome occupancy profiles for multiple tissues derived from human, macaque, tree shrew, mouse, and pig. Genome-wide comparison reveals conserved nucleosome occupancy profiles across both different species and tissue types. Notably, we found significantly higher levels of nucleosome occupancy in exons than in introns, a pattern correlated with the different exon-intron GC content. We then determined whether this biased occupancy may play roles in the origination of new exons through evolution, rather than being a downstream effect of exonization, through a comparative approach to sequentially trace the order of the exonization and biased nucleosome binding. By identifying recently evolved exons in human but not in macaque using matched RNA sequencing, we found that higher exonic nucleosome occupancy also existed in macaque regions orthologous to these exons. Presumably, such biased nucleosome occupancy facilitates the origination of new exons by increasing the splice strength of the ancestral nonexonic regions through driving a local difference in GC content. These data thus support a model that sites bound by nucleosomes are more likely to evolve into exons, which we term the "nucleosome-first" model.

Mitogenomics of macaques (Macaca) across Wallace's Line in the context of modern human dispersals.

Wallace's Line demarcates a biogeographical boundary between the Indomalaya and Australasian ecoregions. Most placental mammalian genera, for example, occur to the west of this line, whereas most marsupial genera occur to the east. However, macaque monkeys are unusual because they naturally occur on both western and eastern sides. To further explore this anomalous distribution, we analyzed 222 mitochondrial genomes from ∼20 macaque species, including new genomes from 60 specimens. These comprise a population sampling of most Sulawesi macaques, Macaca fascicularis (long-tailed macaques) specimens that were collected by Alfred R. Wallace and specimens that were recovered during archaeological excavations at Liang Bua, a cave on the Indonesian island of Flores. In M. fascicularis, three mitochondrial lineages span the southernmost portion of Wallace's Line between Bali and Lombok, and divergences within these lineages are contemporaneous with, and possibly mediated by, past dispersals of modern human populations. Near the central portion of Wallace's Line between Borneo and Sulawesi, a more ancient dispersal of macaques from mainland Asia to Sulawesi preceded modern human colonization, which was followed by rapid dispersal of matrilines and was subsequently influenced by recent interspecies hybridization. In contrast to previous studies, we find no strong signal of recombination in most macaque mitochondrial genomes. These findings further characterize macaque evolution before and after modern human dispersal throughout Southeast Asia and point to possible effects on biodiversity of ancient human cultural diasporas.