A global catalog of whole-genome diversity from 233 primate species

Abstract

The rich diversity of morphology and behavior displayed across primate species provides an informative context in which to study the impact of genomic diversity on fundamental biological processes. Analysis of that diversity provides insight into long-standing questions in evolutionary and conservation biology and is urgent given severe threats these species are facing. Here, we present high-coverage whole-genome data from 233 primate species representing 86% of genera and all 16 families. This dataset was used, together with fossil calibration, to create a nuclear DNA phylogeny and to reassess evolutionary divergence times among primate clades. We found within-species genetic diversity across families and geographic regions to be associated with climate and sociality, but not with extinction risk. Furthermore, mutation rates differ across species, potentially influenced by effective population sizes. Lastly, we identified extensive recurrence of missense mutations previously thought to be human specific. This study will open a wide range of research avenues for future primate genomic research.

Fig. 1.. Genetic diversity in primates across geographic regions and families.

(A) Sampling range of species analyzed in this project. Each point represents the approximate species range centroid of all sampled species with available ranges. Points are repelled to avoid overplotting. (B) Heterozygosity stratified by geographic region. Solid black circles and whiskers represent median values and interquartile range. (C) Median species heterozygosity by family. Solid circles and whiskers represent median and interquartile range. Solid gray line denotes primate-wide median heterozygosity; dashed and dotted lines denote human heterozygosity for African and bottlenecked out-of-Africa populations, respectively. Points are colored according to the family a species belongs to, as denoted on the x axis of (C).

Fig. 2.. Runs of homozygosity and impact of extinction risk on diversity

(A) Relationship between IUCN extinction risk categories and heterozygosity. Solid black circles and bars denote median and IQR. (B) Partition into threatened (T: VU, EN, CR) and nonthreatened (N: LC, NT) categories for all families with more than one species in either partition. Significant differences (p < 0.05, one-sided rank-sum test) are marked with an asterisk. (C) Median number of tracts of homozygosity versus median proportion of the genome in runs of homozygosity per species. Species with a fraction over 1/3 are highlighted. Solid black dots within highlights denote threatened species (VU, EN, CR).

Fig. 3.. Fossil-calibrated nuclear time tree.

Concentric background circles mark 10-million-year intervals; solid gray circles in internal nodes show fossil calibration points (36); species marked with solid circles at tips show paraphyly or polyphyly when including additional individuals to estimate the topology.

Fig. 4.. Estimates of mutation rates and effective population size.

(A) Distribution of estimates of the per-generation mutation rate across primate families (μ). Large solid circles denote median, and horizontal bars denote the interquartile range. The gray line denotes the primate-wide median. (B) Distribution of N_e estimates across primate families. Species with effective population size above 3 × 10⁵ are highlighted. (C) Comparison of pedigree-based estimates of μ for great apes (79, 80), olive baboon (81), rhesus macaque (82), and common marmoset (83) show a high correlation between the two estimates (Spearman’s r = 0.85, p = 0.02). The open circle denotes the estimate for the mouse lemur (84), which was excluded from the comparison as an outlier (16). Data for trio estimates were derived from (85). (D) Positive correlation between estimates of per-generation mutation rates and generation times (g) (Pearson’s r = 0.53, p = 2.1 × 10⁻¹⁷). (E) Inverse relationship between yearly mutation rate and generation time. Circles in (D) and (E) are colored by the effective population size N_e (Pearson’s r = −0.34, p = 3.1 × 10⁻⁷). (F) Relationship between per-generation mutation rate, adjusted by first regressing the effects of generation time, and effective population size. The relationship is highly significant after phylogenetic correction (r² = 0.45, p < 0.001).

Fig. 5.. Recurrent putative high-frequency human-specific missense changes.

Each bar on the x axis represents a high-frequency human-specific missense change with the same allele found in a different species. Color schemes are the same as presented in Figs. 1 and 2.