Sexual selection acting on males through intrasexual competition for mates is a well-established driver of sexual size dimorphism (SSD) in primates. However, studies typically focus on within-group competition, overlooking the potential significance of competition arising from interactions between neighbouring social groups, particularly when home ranges overlap. Here, we analysed the relationships between SSD, mating system and different proxies of range use across up to 143 species of anthropoid and strepsirrhine primates. Contrary to expectations, mating system-a commonly used proxy for male competition-did not significantly predict SSD. Instead, male-biased SSD increased with home range overlap and encounter rate between social groups, even after accounting for mating system and body size allometry. This suggests that spatial pressures, such as the latent threat of competition from rival groups, impose stronger selection on male compared with female size. Home range overlap may select for larger males to deter rivals, defend resources or monopolize females across shared territories, potentially without frequent physical contests. Our work calls for renewed attention to how spatial competition, including resource defence and mate guarding across overlapping territories, influences trait evolution in primates and other social vertebrates and to re-evaluate proxies of sexual selection.

Lineages undergoing rapid evolutionary diversification may evolve a set of mixed traits as a result of hybrid speciation, gene flow, or incomplete lineage sorting (ILS). However, how best to quantify these alternative processes impacting phenotypic variation remains unclear. Here, we examined trait evolution in two sister genera of endangered Asian primates, Trachypithecus and Semnopithecus. By assembling a de novo genome of the Trachypithecus pileatus group, which is geographically located in a transitional zone between these two genera, our integrated phylogenomic analyses clarified the evolutionary relationship of the T. pileatus group with other Trachypithecus species. We also identified that morphological similarities shared between this species group and Semnopithecus are the result of ILS, rather than gene flow or hybrid speciation. Across all chromosomes of the T. pileatus group, ILS contributed 8.9% of whole genome segments. Across these segments, we distinguished 77 genes such as FGFBP1 and FOXO1 that are involved in pathways of bone development and osteoblast differentiation. Functional experiments indicate that FGFBP1 genotypes shared by species of the T. pileatus group and Semnopithecus appear to enhance osteogenic capability and mineralization, possibly resulting in larger body size and similarities in skull morphology compared with other species of Trachypithecus. The study reveals that ILS has shaped the evolution of mixed traits within gene-regulatory networks, driving phenotypic diversity during periods of rapid species divergence in this highly successful primate radiation. ILS appears to be more common than previously thought and represents a critical step in accurately assessing the phylogeny of closely related taxa.

>Sexual dimorphism, encompassing various differences between the sexes in a species, such as body size, canine length, coloration, and ornamentations(Figure 1A), has long been the center of academic focus in evolutionary biology and ecology since Darwin. In recent years, empirical and theoretical advances have enriched our understanding of the nature and evolution of dimorphic traits.

Sensory trade-offs between vision and olfaction in the evolution and radiation of primates have long been debated. However, insights have been limited by a lack of sensory gene sequences and accompanying functional predictions. Here we conduct large-scale functional analyses of visual and olfactory receptors and related brain regions across extant primates. Our results reveal a visual shift from ultraviolet to violet colour sensitivity in early haplorrhine primates, followed by acceleration in the rhodopsin retinal release rates at the origin of anthropoids, both of which are expected to greatly enhance visual acuity under brighter light conditions. Additionally, we find that the sensitivity of olfactory receptors shifted from narrowly to broadly tuned early in anthropoid evolution. In contrast, strepsirrhines appear to have retained sensitive dim-light vision and underwent functional enhancement of narrowly tuned olfactory receptors. Our models indicate that this would have enhanced odorant discrimination and facilitated olfaction-mediated physiology and behaviour. These differences in tuning patterns of olfactory receptors between major primate lineages mirror well-established morphological differences in external anatomy and brain structures, revealing new mechanisms of olfactory adaptation and evolutionary plasticity. Our multisystem analyses reveal patterns of co-evolution in genomic, molecular and neuroanatomical traits that are consistent with a sensory 'reallocation' rather than strict trade-offs.

The dual impact of climate change and human activities has led to a sharp decline in global primate biodiversity.China,which has the most diverse primate species in the northern hemisphere,faces severe eco-logical threats during its transition from an agricultural to a modern society due to the expansion of modern ag-riculture,over-exploitation and consumption of natural resources,and excessive land development.In re-sponse,China has implemented various ecological conservation measures,including habitat restoration and protection.These efforts have made substantial progress in biodiversity conservation,with certain regions see-ing an increase in primate populations.This study conducted a systematic review of historical documents and field research data related to Chinese primates,evaluating the endangered status of primate species in China.Despite improvements in the habitats of most primate species and some population growth,many species still face severe threats,including declining and small populations.Species such as the Myanmar snub-nosed mon-key(Rhinopithecus strykeri),eastern black crested gibbon(Nomascus nasutus),and Hainan gibbon(N.hainanus)remain particularly vulnerable due to their limited distribution ranges and extremely small popula-tions.Insufficient scientific data,fragmented information,and a lack of comprehensive studies in conservation biology further exacerbate these challenges.Additionally,there is a notable lack of detailed population monito-ring data for species such as the Bengal slow loris(Nycticebus bengalensis),Pygmy slow loris(N.pygmae-us),Indochinese gray langur(Trachypithecus crepusculus),Shortridge's langur(T.shortridgei),and capped langur(T.pileatus),hindering the development of practical and targeted conservation management strategies.Therefore,for national biodiversity conservation,there is an urgent need for specialized primate surveys,enhanced habitat protection and restoration,and increased focus on cross-border conservation strate-gies and regional cooperation.Establishing a comprehensive and systematic research database platform,con-ducting continuous and in-depth research in primate biology.Additionally,strengthening public awareness on wildlife conservation remains essential.Such integrated and systematic efforts will provide scientific support for the current and future conservation and management of primate species in China.

Golden snub-nosed monkeys (Rhinopithecus roxellana) live in multilevel societies of over 100 individuals. Despite exploiting low visibility high-altitude forests and home ranges of 14 km2, they maintain large and cohesive social networks that serve to coordinate travel and daily activities effectively. During traveling, foraging, and feeding, golden snub-nosed monkeys communicate using contact or coo calls. These contact calls are conspicuous (70–75 decibels), directional, and function to communicate affiliative intention, identity, and location. Based on social network analyses, we found that golden snub-nosed monkeys exchanged contact calls among individuals within their resident one-male multi-female unit (OMU) and with conspecifics from neighboring OMUs. Within each OMU, there were more frequent call exchanges among more spatially separated members than among closely located individuals. In the case of contact calls between OMUs, there were more frequent contact call exchanges among closely located leader males. These findings demonstrate that contact call exchanges communicate individual identity and location, promote social bonds, and contribute to OMU and inter-OMU coordinated behavior that is essential to a well-functioning multilevel or tiered social network. In addition, given that 34

The dynamics of animal social structures are heavily influenced by environmental patterns of competition and cooperation. In folivorous colobine primates, prevailing theories suggest that larger group sizes should be favored in rainforests with a year-round abundance of food, thereby reducing feeding competition. Yet, paradoxically, larger groups are frequently found in high-altitude or high-latitude montane ecosystems characterized by a seasonal scarcity of leaves. This contradiction is posited to arise from cooperative benefits in heterogeneous environments. To investigate this hypothesis, we carried out a six-year field study on two neighboring groups of golden snub-nosed monkey (Rhinopithecus roxellana), a species representing the northernmost distribution of colobine primates. Results showed that the groups adjusted their movement and habitat selection in response to fluctuating climates and spatiotemporal variability of resources, indicative of a dynamic foraging strategy. Notably, during the cold, resource-scarce conditions in winter, the large group occupied food-rich habitats but did not exhibit significantly longer daily travel distances than the smaller neighboring group. Subsequently, we compiled an eco-behavioral dataset of 52 colobine species to explore their evolutionary trajectories. Analysis of this dataset suggested that the increase in group size may have evolved via home range expansion in response to the cold and heterogeneous climates found at higher altitudes or latitudes. Hence, we developed a multi-benefits framework to interpret the formation of larger groups by integrating environmental heterogeneity. In cold and diverse environments, even smaller groups require larger home ranges to meet their dynamic survival needs. The spatiotemporal distribution of high-quality resources within these expanded home ranges facilitates more frequent interactions between groups, thereby encouraging social aggregation into larger groups. This process enhances the benefits of collaborative actions and reproductive opportunities, while simultaneously optimizing travel costs through a dynamic foraging strategy.

The Y chromosome usually plays a critical role in determining male sex and comprises sequence classes that have experienced unique evolutionary trajectories. Here we generated 19 new primate sex chromosome assemblies, analysed them with 10 existing assemblies and report rapid evolution of the Y chromosome across primates. The pseudoautosomal boundary has shifted at least six times during primate evolution, leading to the formation of a Simiiformes-specific evolutionary stratum and to the independent start of young strata in Catarrhini and Platyrrhini. Different primate lineages experienced different rates of gene loss and structural and chromatin change on their Y chromosomes. Selection on several Y-linked genes has contributed to the evolution of male developmental traits across the primates. Additionally, lineage-specific expansions of ampliconic regions have further increased the diversification of the structure and gene composition of the Y chromosome. Overall, our comprehensive analysis has broadened our knowledge of the evolution of the primate Y chromosome.

Although species can arise through hybridization, compelling evidence for hybrid speciation has been reported only rarely in animals. Here, we present phylogenomic analyses on genomes from 12 macaque species and show that the fascicularis group originated from an ancient hybridization between the sinica and silenus groups ~3.45 to 3.56 million years ago. The X chromosomes and low-recombination regions exhibited equal contributions from each parental lineage, suggesting that they were less affected by subsequent backcrossing and hence could have played an important role in maintaining hybrid integrity. We identified many reproduction-associated genes that could have contributed to the development of the mixed sexual phenotypes characteristic of the fascicularis group. The phylogeny within the silenus group was also resolved, and functional experimentation confirmed that all extant Western silenus species are susceptible to HIV-1 infection. Our study provides novel insights into macaque evolution and reveals a hybrid speciation event that has occurred only very rarely in primates.

Abstract Intrasexual competition among females has long been overshadowed by the focus on that in males. Apart from the studies on Callitrichidae, mechanisms beyond reproductive suppression are virtually uninvestigated. However, that females compete for breeding is likely ubiquitous across polygynous mating primates, where males are likely the limited resource for reproducing and/or offspring raring. As the northernmost distributed Asian colobine, golden snub-nosed monkey retained its ancestral one-male, multi-female unit, but evolved a multi-level society through social aggregation. As a result, the operational sex ratio (the ratio of sexually receptive males to sexually receptive females, hereafter OSR) is expected to be near one as numerous bachelor males shadow the breeding band for mating opportunities. Nevertheless, intrasexual competition was intense, at least in the two study units. The females copulated primarily with the residential males. Hormonal evidence indicates that they were receptive for only 70 days every two years, with only 1 to 3 ovulations. Finally, within units, 50% to 100% of their receptive periods overlapped with one another. Surprisingly, not a single case of aggression or reproductive suppression was observed. By the end of the breeding season, all receptive females showed signs of pregnancy, suggesting successful conceptions. Because staying in stable large units confers a competitive edge over resources through dominance, evolution might have provided strategies for avoiding costly mating competition within units. Further behavioral investigation tentatively reveals two such strategies: coordinating solicitation frequency through turn-taking and/or migrating to units where the intensity of intrasexual competition is low. Our future studies will address the nature and fitness consequences of them.

The biological mechanisms that underpin primate social evolution remain poorly understood. Asian colobines display a range of social organizations, which makes them good models for investigating social evolution. By integrating ecological, geological, fossil, behavioral, and genomic analyses, we found that colobine primates that inhabit colder environments tend to live in larger, more complex groups. Specifically, glacial periods during the past 6 million years promoted the selection of genes involved in cold-related energy metabolism and neurohormonal regulation. More-efficient dopamine and oxytocin pathways developed in odd-nosed monkeys, which may have favored the prolongation of maternal care and lactation, increasing infant survival in cold environments. These adaptive changes appear to have strengthened interindividual affiliation, increased male-male tolerance, and facilitated the stepwise aggregation from independent one-male groups to large multilevel societies.

Although the continual expansion of the brain during primate evolution accounts for our enhanced cognitive capabilities, the drivers of brain evolution have scarcely been explored in these ancestral nodes. Here, we performed large-scale comparative genomic, transcriptomic, and epigenomic analyses to investigate the evolutionary alterations acquired by brain genes and provide comprehensive listings of innovatory genetic elements along the evolutionary path from ancestral primates to human. The regulatory sequences associated with brain-expressed genes experienced rapid change, particularly in the ancestor of the Simiiformes. Extensive comparisons of single-cell and bulk transcriptomic data between primate and nonprimate brains revealed that these regulatory sequences may drive the high expression of certain genes in primate brains. Employing in utero electroporation into mouse embryonic cortex, we show that the primate-specific brain-biased gene BMP7 was recruited, probably in the ancestor of the Simiiformes, to regulate neuronal proliferation in the primate ventricular zone. Our study provides a comprehensive listing of genes and regulatory changes along the brain evolution lineage of ancestral primates leading to human. These data should be invaluable for future functional studies that will deepen our understanding not only of the genetic basis of human brain evolution but also of inherited disease.

Primates are highly successful mammals with significant morphological,behavioral,and physiological diversity.Studying the genomes of non-human primates,as the closest relative of humans,can provide insights into human evolution,genetic structure,and potential drug targets relevant to human health,thus making important contributions to medical research.Additionally,primate genome research can support ecological balance and resource conservation and promote sustainable development and human well-being.Despite the existence of more than 500 primate species belonging to 80 genera and 16 families worldwide,with new species still being discovered in recent years(Fan et al.,2017;Khanal et al.,2021;Roos et al.,2020),genome sequencing efforts have been limited to a relatively small number of species from only 22 genera(Ensembl v103).Notably,approximately 72％of primate genera remain unsequenced,leading to significant knowledge gaps in our understanding of their evolutionary history.This situation presents considerable challenges for the development,utilization,and protection of primate genetic resources.It is for these compelling reasons that we initiated the Primate Genome Project(PGP)(Wu et al.,2022).

Comparative analysis of primate genomes within a phylogenetic context is essential for understanding the evolution of human genetic architecture and primate diversity. We present such a study of 50 primate species spanning 38 genera and 14 families, including 27 genomes first reported here, with many from previously less well represented groups, the New World monkeys and the Strepsirrhini. Our analyses reveal heterogeneous rates of genomic rearrangement and gene evolution across primate lineages. Thousands of genes under positive selection in different lineages play roles in the nervous, skeletal, and digestive systems and may have contributed to primate innovations and adaptations. Our study reveals that many key genomic innovations occurred in the Simiiformes ancestral node and may have had an impact on the adaptive radiation of the Simiiformes and human evolution.

Lorises are a group of globally threatened strepsirrhine primates that exhibit many unusual physiological and behavioral features, including a low metabolic rate, slow movement, and hibernation. Here, we assembled a chromosome-level genome sequence of the pygmy loris (Xanthonycticebus pygmaeus) and resequenced whole genomes from 50 pygmy lorises and 6 Bengal slow lorises (Nycticebus bengalensis). We found that many gene families involved in detoxification have been specifically expanded in the pygmy loris, including theGSTAgene family, with many newly derived copies functioning specifically in the liver. We detected many genes displaying evolutionary convergence between pygmy loris and koala, includingPITRM1.Significant decreases in PITRM1 enzymatic activity in these two species may have contributed to their characteristic low rate of metabolism. We also detected many evolutionarily convergent genes and positively selected genes in the pygmy loris that are involved in muscle development. Functional assays demonstrated the decreased ability of one positively selected gene,MYOF,to up-regulate the fast-type muscle fiber, consistent with the lower proportion of fast-twitch muscle fibers in the pygmy loris. The protein product of another positively selected gene in the pygmy loris,PER2, exhibited weaker binding to the key circadian core protein CRY, a finding that may be related to this species’ unusual circadian rhythm. Finally, population genomics analysis revealed that these two extant loris species, which coexist in the same habitat, have exhibited an inverse relationship in terms of their demography over the past 1 million years, implying strong interspecies competition after speciation.

Various primate species, including golden snub-nosed monkeys, Rhinopithecus roxellana, form highly complex multilevel social systems. Breeding bands of snub-nosed monkeys maintain stability even though multiple one-male units (OMUs) within a band do not appear to engage in affiliative behaviours among units. As such, female dispersal within breeding bands may be a key factor related to social stability in these complex social systems. However, how individual and group behaviours influence both the formation of this complex social system and the maintenance of social stability within it remain to be fully elucidated. In the current study, based on 16 years of accumulated data, we investigated female dispersal in a wild population of golden snub-nosed monkeys in the Qinling Mountains of China. Using social network analysis and dynamic social modelling, we found that male take-over had no influence on the dominance rank of an OMU, whereas the number of breeding females within an OMU had a significant positive effect on rank. Both the number of breeding females and the number of females entering an OMU had significant positive effects on eigenvector centrality of an OMU. Female dispersal between OMUs decreased the clustering coefficient and reduced the risk of subgroup formation. In addition, female kinship matrices between units were not significantly correlated with association behaviour patterns. Thus, this study sheds light on the internal mechanisms that drive social stability in a complex primate social system.

A crucial step for understanding human evolution is to identify the genomic changes that occurred during primate evolution,thus allowing investigators to reconstruct the ancestral states preceding the human condition.In the past several decades,the primate clade has been a research focus in genome sequencing due to its unique phylogenetic position and key importance.Comparative genomic analyses of several primate lineages have radically expanded our knowledge on the tempo and mode of different features in primate genome evolution,revealing many genomic innovations contributing to the development and evolution of human phenotypes.

Papageorgiou and Farine [ 1. Papageorgiou D. Farine D. Multilevel societies in birds. Trends Ecol. Evol. 2020; (Published online October 29, 2020)https://doi.org/10.1016/j.tree.2020.10.008 Abstract Full Text Full Text PDF PubMed Scopus (1) Google Scholar ], in their comment on our recent synthesis of animal multilevel societies [ 2. Grueter C.C. et al. Multilevel organisation of animal sociality. Trends Ecol. Evol. 2020; 35: 834-847 Abstract Full Text Full Text PDF PubMed Scopus (14) Google Scholar ], provide several examples of nestedness in avian social systems and call for a fuller incorporation of birds into our theoretical framework. We focused mainly on mammals to construct our proposed framework because multilevel societies are best known from this taxonomic group. Papageorgiou and Farine [ 1. Papageorgiou D. Farine D. Multilevel societies in birds. Trends Ecol. Evol. 2020; (Published online October 29, 2020)https://doi.org/10.1016/j.tree.2020.10.008 Abstract Full Text Full Text PDF PubMed Scopus (1) Google Scholar ] point out several bird species that form nested social arrangements and argue that, by diving deeply into examples from birds, there may be variations in form that meet our criteria for a multilevel society: a social system with a stable core level and at least one recognizable upper level. Papageorgiou and Farine [ 1. Papageorgiou D. Farine D. Multilevel societies in birds. Trends Ecol. Evol. 2020; (Published online October 29, 2020)https://doi.org/10.1016/j.tree.2020.10.008 Abstract Full Text Full Text PDF PubMed Scopus (1) Google Scholar ] raise two questions: (i) whether the operational definition of multilevel societies should be relaxed to accommodate bird species that show more stability at higher levels of society; and (ii) whether societies with multiple tiers resulting solely from habitat preferences instead of social preferences should be classified as multilevel societies.

Collective decision-making is important for coordination and synchronization of the activities among group-living animals and the mechanisms guiding such procedure involve a great variety of characteristics of behavior and motivation. This study provides some evidence investigating collective movement initiation in a multi-level social band of the golden snub-nosed monkeys (Rhinopithecus roxellana) located in the Mts. Qinling, China. We collect 1223 datum records relevant to decision initiation from six OMUs. The results indicate that collective movement initiation could be divided into two continual but relatively independent processes: decisions on moving direction and movement implementation. In both processes, adult individuals are more likely to initiate the decision-making, while other adults vote on initiator’s preference, with a threshold, a supporting number required for a success. Thus, voting behavior and quorum fulfillment contribute to a successful decision-making. Adult individuals play important role in making decisions for moving direction and implementation. For a successful collective movement initiation, the individuals being more central in grooming network initiate decisions more frequently than the others, and attract voters more easily. Furthermore, following the initiation, at least four positive voters are required for a direction decision and at least three positive voters are needed for the decision on movement implementation, which could be considered as the threshold of quorum numbers required for a successful decision. This study has provided some very interesting information and scientific evidence in understanding social structure and behaviors of the nonhuman primates with a social structure very similar to humans’. Thus, some results can directly be referred to the comprehension of human social structure and behavior.