1 Introduction

Population genomics is a field of study that focuses on understanding the genetic composition of populations and how it changes over time due to various evolutionary forces such as mutation, selection, recombination, and genetic drift. This field is significant in evolutionary biology as it provides insights into the mechanisms driving genetic diversity and adaptation within and between species (Peter et al., 2016). Historically, advancements in genomic technologies, such as high-throughput DNA sequencing, have revolutionized our ability to analyze genetic variation at a genome-wide scale, enabling more precise estimates of genetic diversity and evolutionary dynamics (Osada, 2015). The integration of phylogenetics and population genetics, known as phylogenomics, has further enhanced our understanding of evolutionary histories and the functional elements within genomes (Siepel, 2009).

Primates hold a unique position in evolutionary biology due to their close genetic relationship to humans. Studying primate genomics is crucial for understanding human evolution, as it allows researchers to identify genetic differences and similarities that have shaped the phenotypic traits of humans and their closest relatives (Stone and Verrelli, 2006). Primates also exhibit a rich diversity in morphology, behavior, and ecological adaptations, making them an ideal group for studying the impact of genomic diversity on biological processes (Kuderna et al., 2023). Furthermore, many primate species are threatened with extinction due to anthropogenic effects, highlighting the importance of conservation genomics to inform population management and preserve biodiversity (Orkin et al., 2020).

This study is to summarize the current knowledge on primate population genomics, focusing on the diversity, population structure, and evolutionary dynamics of primate species. By synthesizing findings from recent genomic studies, this study will provide a comprehensive overview of the genetic variation within and between primate populations and the evolutionary forces shaping this diversity. Additionally, this study will explore the implications of these findings for understanding human evolution and for the conservation of primate species, and identify future research directions and challenges in the field of primate population genomics, emphasizing the need for continued advancements in genomic technologies and analytical methods.

2 Genetic Diversity in Primates

2.1 Intraspecific genetic variation

Genetic diversity within primate species varies significantly, influenced by factors such as population size, habitat fragmentation, and evolutionary history. For instance, rhesus macaques (Macaca mulatta) exhibit a high level of nucleotide diversity, approximately 2.5 times greater than that observed in humans. This diversity includes over 43.7 million single-nucleotide variants, which have implications for both functional and non-functional genomic regions (Xue et al., 2016).

Prado-Martinez et al. (2013) found that chimpanzees, particularly the common chimpanzee, display significant genetic diversity, with distinct genetic populations identified within the species. For example, the Nigeria-Cameroon/western and central/eastern populations of common chimpanzees are genetically distinct, highlighting the complex population history and gene flow within this species. In macaques, whole-genome sequencing has revealed extensive genetic variation, including numerous variants that affect protein sequences and gene regulation, underscoring the species’ utility as a model for human disease studies (Xue et al., 2016). Similarly, studies on lemurs have shown that even critically endangered species like the black and white ruffed lemur and Coquerel’s sifaka maintain high levels of genetic diversity, suggesting that conservation efforts can be effective if timely (Perry et al., 2012).

2.2 Interspecific genetic variation

Comparative genomic studies have provided insights into the genetic differences between various primate species. For instance, humans and chimpanzees, despite sharing 98.7% of their genomic DNA, exhibit significant differences in gene expression patterns, particularly in the brain, which may underlie the distinct cognitive and behavioral traits observed between the species (Enard et al., 2002). Additionally, the genetic diversity observed in great apes, including gorillas and orangutans, has been linked to their population history and varying levels of inbreeding, which affect their susceptibility to diseases and overall genetic health.

Great apes, such as chimpanzees and gorillas, show extensive genetic variation, with evidence of gene flow and distinct population structures within species. In contrast, New World monkeys and Old World monkeys exhibit different patterns of genetic diversity and evolutionary pressures. For example, the genetic diversity in rhesus macaques, an Old World monkey, is shaped by a large and fluctuating population size, which has led to higher levels of nucleotide diversity compared to humans (Xue et al., 2016). These differences highlight the varied evolutionary trajectories and selective pressures experienced by different primate lineages.

2.3 Factors influencing genetic diversity

Mutation, recombination, and genetic drift are fundamental forces shaping genetic diversity in primates. Mutations introduce new genetic variants, while recombination shuffles these variants, creating new combinations of alleles. Genetic drift, particularly in small populations, can lead to significant changes in allele frequencies over time. For example, the high level of genetic polymorphism observed in the common ancestor of the African ape clade (Homo-Pan-Gorilla) suggests that genetic drift played a significant role in shaping the genetic landscape of these species.

Population size, habitat fragmentation, and gene flow are critical factors influencing genetic diversity. Large populations tend to maintain higher levels of genetic diversity due to a greater number of breeding individuals and reduced effects of genetic drift. Conversely, habitat fragmentation can isolate populations, reducing gene flow and increasing the risk of inbreeding. For instance, the extensive inbreeding observed in eastern gorillas is likely a consequence of habitat fragmentation and reduced population sizes. Gene flow, on the other hand, can introduce new genetic variants into a population, enhancing genetic diversity and adaptive potential. The genetic distinctiveness of chimpanzee populations, for example, is partly due to historical gene flow events that have shaped their current genetic structure.

3 Population Structure in Primates

3.1 Geographical patterns of genetic structure

Geographical patterns of genetic structure in primates are influenced by various factors, including historical migrations, environmental barriers, and social behaviors. Studies have shown that genetic diversity and differentiation can vary significantly across different geographic regions. For instance, In gorillas, nucleotide diversity studies have shown that western lowland gorillas possess the highest levels of genetic diversity among African apes, which is about twice that of humans (Yu et al., 2004). This high diversity is indicative of substantial historical population sizes and migrations. In baboons, genome sequencing of six species has revealed multiple episodes of admixture and introgression, highlighting the complex evolutionary history and geographic structuring within the genus Papio (Figure 1) (Rogers et al., 2019).

Figure 1 Papio baboon species (Adopted from Rogers et al., 2019) Image caption: (A) The appearance and current distribution of each baboon species, and the locations of three well-documented active hybrid zones are also shown. x1: hybrid zone between P. hamadryas and P. anubis (Phillips-Conroy et al., 1991; Bergman et al., 2008); x2: hybrid zone between P. cynocephalus and P. anubis (Tung et al., 2008; Charpentier et al., 2012); x3: hybrid zone between P. kindae and P. ursinus (Jolly et al., 2011); Drawings of each species by S. Nash. (B) Distinguishing features of Papio species (Adopted from Rogers et al., 2019)

3.2 Social structure and genetic differentiation

Social organization plays a crucial role in shaping the genetic structure of primate populations. In species where males are the dispersing sex, such as baboons, social structure and behavior can predict molecular genetic measures of relatedness and reproductive success. For example, in Guinea baboons, female-biased gene flow has been observed, contrasting with the male-biased dispersal seen in other baboon species. This unique social system results in a lack of genetic-geographic structuring and higher genetic variation within demes (Kopp et al., 2013).

3.3 Historical demography

Reconstructing the historical demography of primates involves analyzing genetic data to infer past population sizes and migration events. For instance, studies on baboons have utilized ancient DNA to demonstrate long-term population continuity in southern Africa, providing insights into the demographic history of the species (Mathieson et al., 2020). Similarly, nucleotide diversity analyses in gorillas have been used to estimate long-term effective population sizes, shedding light on their historical population dynamics (Yu et al., 2004).

We can also apply similar methods to reconstruct the population history of other primate species. For example, analyzing mitochondrial and nuclear DNA sequences can reveal past population sizes, migration patterns, and the impact of historical events on genetic diversity. These insights are crucial for understanding the evolutionary dynamics and conservation needs of these primates.

4 Evolutionary Dynamics of Primates

4.1 Natural selection

Natural selection plays a crucial role in shaping the genetic architecture of primate populations. The detection of selection signatures in primate genomes involves identifying regions where genetic variation is influenced by selective pressures. Various methods have been developed to detect these signatures, including long-range haplotype methods and machine learning approaches, which can identify selective sweeps and other patterns indicative of selection (Hohenlohe et al., 2010; Liu et al., 2013; Kumar et al., 2022). For instance, the use of genome-wide scans has revealed widespread genomic signatures of natural selection in hominid evolution, highlighting the reduction in neutral sequence diversity near conserved features due to selection (McVicker et al., 2009). Additionally, balancing selection, which maintains genetic diversity within populations, has been increasingly recognized as a significant driver of diversity, with sophisticated methods now available to detect its signatures (Bitarello et al., 2023).

Adaptations to various environmental pressures, including diet and disease resistance, are evident in primate genomes. For example, genes associated with lactase persistence, skin pigmentation, and sickle cell anemia have been identified as targets of positive selection in human populations, reflecting adaptations to dietary changes and disease resistance (Rochus et al., 2018). Comparative genomics has also uncovered a role for positive Darwinian selection in genes involved in immune response, sensory perception, and reproduction, which are critical for survival and adaptation to environmental challenges (Ellegren, 2008). These findings underscore the importance of natural selection in driving the evolutionary dynamics of primates.

4.2 Genetic drift and bottlenecks

Genetic drift and demographic fluctuations, such as population bottlenecks, significantly impact genetic diversity in primate populations. Bottlenecks, which occur when populations experience a drastic reduction in size, can lead to a loss of genetic variation and an increase in inbreeding. This effect is particularly pronounced in island primates and endangered species, where limited population sizes exacerbate the impact of genetic drift (Siepel, 2009). The study of demographic history through genome sequencing has provided insights into how these fluctuations shape genetic diversity and influence evolutionary trajectories (Ellegren, 2008).

Island primates, such as those found in Madagascar, often experience severe genetic bottlenecks due to their isolated habitats and small population sizes. These bottlenecks can lead to reduced genetic diversity and increased vulnerability to environmental changes and diseases. Similarly, endangered primate species, such as certain great apes, face significant genetic challenges due to habitat loss and human activities. Understanding the genetic consequences of these bottlenecks is crucial for conservation efforts and for maintaining the evolutionary potential of these species (Ellegren, 2008; Siepel, 2009).

4.3 Gene flow and hybridization

Gene flow, the transfer of genetic material between populations, plays a vital role in shaping genetic diversity in primates. It can introduce new genetic variants into populations, enhancing genetic diversity and potentially facilitating adaptation to changing environments. Gene flow can also counteract the effects of genetic drift and inbreeding, maintaining genetic health in small populations (Ellegren, 2008; Siepel, 2009).

Hybrid zones, where different primate species or subspecies interbreed, provide valuable insights into the role of gene flow in evolution. For example, hybrid zones in macaques have been studied to understand how gene flow influences genetic diversity and adaptation. Similarly, introgression, the incorporation of genetic material from one species into the gene pool of another through hybridization, has been observed in baboons. These examples highlight the complex interplay between gene flow and hybridization in shaping the evolutionary dynamics of primates (Ellegren, 2008; Siepel, 2009).

By examining these evolutionary dynamics, we gain a deeper understanding of the processes that drive genetic diversity and adaptation in primate populations. This knowledge is essential for both evolutionary biology and conservation efforts, as it informs strategies to preserve the genetic health and evolutionary potential of primate species.

5 Genomic Tools and Approaches

5.1 High-throughput sequencing

Advances in high-throughput sequencing technologies have significantly transformed the field of primate genomics, enabling comprehensive studies of genetic diversity, population structure, and evolutionary dynamics. Whole-genome sequencing (WGS) has become a cornerstone of these efforts, providing detailed insights into the genetic makeup of various primate species. For instance, the sequencing of whole genomes from non-model organisms has revealed patterns of recombination rates, adaptive evolution, and gene family expansions that are crucial for understanding evolutionary biology (Ellegren, 2014). Additionally, the decreasing cost of sequencing has made it feasible to sequence entire primate genomes at the population level, which is essential for conservation genomics (Orkin et al., 2020).

Exome sequencing, which focuses on the protein-coding regions of the genome, has also been employed to uncover the molecular basis of phenotypic differences among primates. This approach has identified genes under positive selection that are involved in the conversion of epithelial cells in skin, hair, and nails to keratin, highlighting the power of targeted capture methods in comparative genomics (George et al., 2011). RNA sequencing (RNA-seq) has further expanded our understanding by revealing substantial genetic variation and gene expression differences among endangered primates, providing insights into species-specific adaptations and evolutionary forces (Perry et al., 2012).

5.2 Genomic data analysis

The analysis of genomic data in population genomics involves a variety of computational tools designed to infer population structure, demographic history, and selection pressures. Population structure analysis helps in understanding the genetic differentiation among populations, while demographic inference provides insights into historical population sizes and migration patterns. For example, a comprehensive overview of current population genomics methods has highlighted more than 100 state-of-the-art tools that can handle whole-genome data, facilitating the integration of selection into historical frameworks (Bourgeois and Warren, 2021).

Selection scans are another critical aspect of genomic data analysis, aiming to identify regions of the genome that have been subject to natural selection. These scans have been instrumental in uncovering genes involved in adaptation and speciation. For instance, the identification of genes under positive selection in primate exomes has provided valuable information on the evolutionary history and phenotypic diversity of these species (George et al., 2011). Additionally, the “Simple Fool’s Guide to Population Genomics via RNA-seq” offers a user-friendly protocol for analyzing high-throughput sequencing data, making these advanced techniques more accessible to population biologists (Wit et al., 2012).

5.3 Comparative genomics

Comparative genomics involves the analysis of genome sequences from different species to understand their evolutionary relationships and functional genomics. Genome alignments and phylogenomic analyses are fundamental tools in this field, allowing researchers to reconstruct the evolutionary history of primates and identify conserved and divergent genomic regions. For example, genome assemblies for various primate species have provided new insights into the evolutionary origins of the human genome and the processes involved (Rogers and Gibbs, 2014). Phylogenomics, which combines phylogenetic and genomic data, has been essential in unlocking valuable information about evolutionary history and genomic function, despite challenges posed by variation in ancestral populations (Siepel, 2009).

Functional genomics approaches, such as the analysis of gene expression and regulatory elements, have further enriched our understanding of primate evolution. Comparative RNA sequencing has revealed genetic variation and gene expression differences that are consistent with positive selection, shedding light on the genetic basis of species-specific adaptations (Perry et al., 2012). Moreover, the creation of a global catalog of whole-genome diversity from 233 primate species has provided a comprehensive resource for studying the impact of genomic diversity on biological processes, evolutionary divergence, and conservation efforts (Kuderna et al., 2023).

6 Case Studies in Primate Population Genomics

6.1 Population genomics of African great apes (chimpanzees, bonobos, and gorillas)

Research on the population genomics of African great apes, including chimpanzees, bonobos, and gorillas, has revealed significant insights into their genetic diversity, structure, and evolutionary dynamics.

Chimpanzees and bonobos exhibit complex demographic histories with evidence of ancient admixture. For instance, de Manuel et al. found that gene flow occurred from bonobos into the ancestors of central and eastern chimpanzees between 200,000 and 550,000 years ago, contributing less than 1% to the central chimpanzee genomes (Manuel et al., 2016). Additionally, studies have shown that chimpanzees have a nucleotide diversity (pi) of 0.134%, which is higher than that of humans but lower than previously thought (Yu et al., 2003). Gorillas, on the other hand, exhibit the highest nucleotide diversity among African apes, with a (pi) value of 0.158% (Yu et al., 2004).

The genetic structure of chimpanzee populations has been extensively studied, revealing three distinct populations: western, central, and eastern chimpanzees, with little evidence of gene flow between them (Becquet et al., 2007). Furthermore, Chaisson et al. (2018) systematically discovered structural changes (length>50 base pairs) through improved sequence adjacency and detected 614186 primate deletions, insertions, and reversals, each assigned to a specific primate lineage (Figure 2), providing deeper insights into their evolutionary trajectories.

Figure 2 SMRT assemblies and SV analyses (Adopted from Chaisson et al., 2018) Image caption: (Top) Contiguity of the de novo assemblies. (Bottom, left to right) For each ape, SVdetection was done against the human reference genome as represented by a dot plot of an inversion). Human-specific SVs, identified by comparing ape SVs and population genotyping (0/0, homozygous reference),were compared to single-cell gene expression differences [range: low (dark blue) to high (dark red)] in primary and organoid tissues. Each heatmap row is a gene that intersects an insertion or deletion (green), duplication (cyan), or inversion (light green) (Adopted from Chaisson et al., 2018)

6.2 Genomic studies on Asian primates (orangutans)

Genomic studies on Asian primates, particularly orangutans, have provided valuable insights into their population history and adaptive evolution. For example, high-quality genome assemblies of orangutans have enabled the identification of lineage-specific genetic variations and structural changes (Chaisson et al., 2018). These studies have highlighted the importance of structural variations in shaping the genetic landscape of orangutans and their adaptive evolution.

Comparative analyses have also shown that orangutans possess unique genetic features that distinguish them from other great apes. These features include specific structural variants and gene expression patterns that have evolved over millions of years (Stone and Verrelli, 2006). Such findings underscore the significance of genomic studies in understanding the evolutionary dynamics and population history of Asian primates.

6.3 Population genomics of New World monkeys (capuchins, howler monkeys, and marmosets)

New World monkeys, such as capuchins (genus Cebus), howler monkeys (genus Alouatta), and marmosets (genus Callithrix), have been studied to understand their genetic diversity and evolutionary dynamics. Capuchins, known for their intelligence and complex behaviors, exhibit significant genetic diversity across their range (Aristide et al., 2013). Howler monkeys, with their distinct vocalizations and folivorous diet, show genetic differentiation that corresponds with their geographic distribution. Marmosets, small and socially complex primates, provide insights into the genetic basis of social behavior and adaptation.

7 Implications for Conservation

7.1 Genetic monitoring and management

The use of genomic data in conservation planning has become increasingly feasible and essential due to advancements in sequencing technologies and the decreasing cost of genomic analyses. Genomic data can provide precise estimates of effective population size, inbreeding levels, demographic history, and population structure, which are critical for conservation efforts (Steiner et al., 2013; Hohenlohe et al., 2020). For instance, genomic tools can identify genetic loci responsible for inbreeding depression or adaptation to changing environments, thereby informing strategies to manage adaptive variation and enhance the evolutionary potential of populations (Harrisson et al., 2014; Hohenlohe et al., 2020).

Genomic data can be used to identify and introduce genetic diversity into small, inbred populations to reduce inbreeding depression and increase fitness. This approach has been successfully applied in various species, where the introduction of individuals from a related subspecies increased genetic diversity and improved population viability (Steiner et al., 2013).

Genomic data can also help manage captive breeding programs by ensuring that genetic diversity is maintained, which is crucial for the long-term survival of species. For example, genomic analyses have been used to manage the genetic diversity of captive primate populations, ensuring that they retain the evolutionary potential to adapt to future environmental changes (Supple et al., 2018; Orkin et al., 2020).

7.2 Identifying conservation units

Defining management units based on genetic data is crucial for effective conservation planning. Genomic data can reveal fine-scale population structure and historical isolation, which are often not apparent from morphological or ecological data alone (Coates et al., 2018; Supple et al., 2018). This information can be used to delineate conservation units that represent unique genetic diversity and evolutionary potential.

Genomic studies have identified distinct genetic populations within endangered primate species, such as lemurs and lorisoids, which were previously considered a single management unit. For example, the black and white ruffed lemur and the Coquerel’s sifaka, despite being critically endangered, were found to harbor considerable genetic diversity, suggesting the presence of multiple conservation units within these species (Perry et al., 2012). This information is vital for developing targeted conservation strategies that preserve the genetic integrity of each unit.

7.3 Addressing challenges in conservation genomics

While the potential of genomic tools in conservation is immense, there are several ethical considerations and practical challenges that need to be addressed. Ethical considerations include the potential for genomic data to be misused, the need for equitable access to genomic technologies, and the importance of involving local communities in conservation decisions (Allendorf et al., 2010; Steiner et al., 2013). It is essential to develop guidelines that ensure the ethical use of genomic data in conservation. This includes protecting the privacy of genetic information, obtaining informed consent from local communities, and ensuring that the benefits of genomic research are shared equitably (Steiner et al., 2013).

Implementing genomic tools in conservation requires overcoming challenges related to computational resources, sampling constraints, and the interpretation of complex genomic data. Strategies to address these challenges include investing in capacity building, developing user-friendly computational tools, and fostering collaborations between conservation biologists, geneticists, and policymakers (Allendorf et al., 2010; Supple et al., 2018).

By addressing these challenges and leveraging the power of genomic data, conservation efforts can be more precisely targeted and effective, ultimately contributing to the preservation of biodiversity and the resilience of ecosystems.

8 Future Directions and Challenges

8.1 Emerging technologies

The field of primate genomics is poised to benefit significantly from emerging technologies that promise to enhance our understanding of primate diversity, structure, and evolutionary dynamics. One such technology is CRISPR, which allows for precise genome editing and has the potential to elucidate gene function and evolutionary adaptations in primates (Orkin et al., 2020). Single-cell genomics is another promising technology, enabling the study of genetic variation at the cellular level, which can provide insights into cellular heterogeneity and the development of complex traits (Housman and Gilad, 2020). Additionally, environmental DNA (eDNA) techniques offer non-invasive methods to collect genetic material from primate habitats, facilitating the study of elusive or endangered species without the need for direct sampling (Orkin et al., 2020).

8.2 Integrative approaches

Combining genomics with other disciplines such as ecology, behavior, and physiology is crucial for a holistic understanding of primate evolution and adaptation. Integrative approaches can reveal how genetic variations influence phenotypic traits and how these traits interact with environmental factors. For instance, combining genomic data with ecological and behavioral studies can help identify the genetic basis of adaptive traits and their evolutionary significance (Bamba et al., 2018). Interdisciplinary research is essential for addressing complex questions about primate biology and for developing effective conservation strategies.

8.3 Addressing knowledge gaps

Despite significant advancements, there remain substantial knowledge gaps in primate genomics. One major challenge is the study of rare and cryptic species, which are often difficult to sample and study due to their elusive nature and low population densities (Orkin et al., 2020). Additionally, there is a need for more comprehensive genomic data across a broader range of primate species to fully understand their evolutionary histories and genetic diversity (Perelman et al., 2011). Addressing these gaps will require innovative sampling methods, increased collaboration among researchers, and the development of new analytical tools to handle complex genomic data.

9 Concluding Remarks

The systematic review of population genomics in primates has revealed significant insights into genetic diversity, population structure, and evolutionary dynamics. Comparative genomic studies have highlighted substantial genetic variation across primate species, including endangered ones, with some species like the black and white ruffed lemur and Coquerel’s sifaka showing high genetic diversity despite their endangered status. Advances in genome sequencing have provided comprehensive data on primate genome content and dynamics, offering valuable information about evolutionary origins and processes. Phylogenomic approaches have underscored the importance of considering ancestral population variation in understanding sequence divergence and evolutionary histories. Studies have also shown that genetic methods can illuminate long-term evolutionary processes and population dynamics that are not easily observable. Furthermore, research on gene regulation has expanded to include a wider range of species, providing insights into the evolutionary processes that govern gene regulatory evolution and phenotypic diversity.

Population genomics studies are crucial for understanding primate evolution and conservation. They provide a detailed view of genetic diversity and population structure, which are essential for reconstructing evolutionary histories and identifying adaptive traits. These studies also offer insights into the genetic basis of species-specific adaptations and the evolutionary forces shaping genetic variation, such as mutation, selection, recombination, and drift. Understanding these dynamics is vital for conservation efforts, as it helps identify populations with significant genetic diversity that may be more resilient to environmental changes. Additionally, population genomics can inform strategies for preserving genetic diversity and managing endangered species, ensuring their long-term survival.

The field of primate population genomics is rapidly advancing, driven by new technologies and collaborative efforts. Future research should focus on expanding genomic studies to include more primate species, particularly those that are critically endangered or have limited genomic data available. High-throughput sequencing and functional genomics approaches will enhance our understanding of genotype-phenotype relationships and the evolutionary processes underlying primate diversity. Collaborative efforts across disciplines and institutions will be essential for generating comprehensive genomic data and developing effective conservation strategies. Continued research in this field will not only deepen our understanding of primate evolution but also contribute to the broader knowledge of genetic diversity and evolutionary dynamics in other species. Encouraging ongoing research and fostering international collaborations will be key to unlocking the full potential of population genomics in primates and ensuring the conservation of these remarkable species.

Acknowledgments

The author thanks the two anonymous peer reviewers for their thorough review of this study and for their valuable suggestions for improvement.

Conflict of Interest Disclosure

The authors affirm that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

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