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Abstract The aye-aye (Daubentonia madagascariensis) is one of the 25 most endangered primate species in the world, maintaining amongst the lowest genetic diversity of any primate measured to date. Characterizing patterns of genetic variation within aye-aye populations, and the relative influences of neutral and selective processes in shaping that variation, is thus important for future conservation efforts. In this study, we performed the first whole-genome scans for positive and balancing selection in the species, utilizing high-coverage population genomic data from newly sequenced individuals. We generated null thresholds for our genomic scans by creating an evolutionarily appropriate baseline model that incorporates the demographic history of this aye-aye population, and identified a small number of candidate genes. Most notably, a suite of genes involved in olfaction—a key trait in these nocturnal primates—were identified as experiencing long-term balancing selection. We also conducted analyses to quantify the expected statistical power to detect positive and balancing selection in this population using site frequency spectrum–based inference methods, once accounting for the potentially confounding contributions of population history, mutation and recombination rate variation, as well as purifying and background selection. This work, presenting the first high-quality, genome-wide polymorphism data across the functional regions of the aye-aye genome, thus provides important insights into the landscape of episodic selective forces in this highly endangered species. 

The nocturnal aye-aye, Daubentonia madagascariensis, is one of the most elusive lemurs on the island of Madagascar. The timing of its activity and arboreal lifestyle has generally made it difficult to obtain accurate assessments of population size using traditional census methods. Therefore, alternative estimates provided by population genetic inference are essential for yielding much needed information for conservation measures and for enabling ecological and evolutionary studies of this species. Here, we utilize genomic data from 17 individuals—including 5 newly sequenced, high-coverage genomes—to estimate this history. Essential to this estimation are recently published annotations of the aye-aye genome which allow for variation at putatively neutral genomic regions to be included in the estimation procedures, and regions subject to selective constraints, or in linkage to such sites, to be excluded owing to the biasing effects of selection on demographic inference. By comparing a variety of demographic estimation tools to develop a well-supported model of population history, we find strong support for two demes, separating northern Madagascar from the rest of the island. Additionally, we find that the aye-aye has experienced two severe reductions in population size. The first occurred rapidly, ∼3,000 to 5,000 years ago, and likely corresponded with the arrival of humans to Madagascar. The second occurred over the past few decades and is likely related to substantial habitat loss, suggesting that the species is still undergoing population decline and remains at great risk for extinction. 

The rate of input of new genetic mutations, and the rate at which that variation is reshuffled, are key evolutionary processes shaping genomic diversity. Importantly, these rates vary not just across populations and species, but also across individual genomes. Despite previous studies having demonstrated that failing to account for rate heterogeneity across the genome can bias the inference of both selective and neutral population genetic processes, mutation and recombination rate maps have to date only been generated for a relatively small number of organisms. Here, we infer such fine-scale maps for the aye-aye (Daubentonia madagascariensis) – a highly endangered strepsirrhine that represents one of the earliest splits in the primate clade, and thus stands as an important outgroup to the more commonly-studied haplorrhines – utilizing a recently released fully-annotated genome combined with high-quality population sequencing data. We compare our indirectly inferred rates to previous pedigree-based estimates, finding further evidence of relatively low mutation and recombination rates in aye-ayes compared to other primates. 

The aye-aye (Daubentonia madagascariensis) is one of the 25 most endangered primate species in the world, maintaining amongst the lowest genetic diversity of any primate measured to date. Characterizing patterns of genetic variation within aye-aye populations, and the relative influences of neutral and selective processes in shaping that variation, is thus important for future conservation efforts. In this study, we performed the first whole-genome scans for recent positive and balancing selection in the species, utilizing high-coverage population genomic data from newly sequenced individuals. We generated null thresholds for our genomic scans by creating an evolutionarily appropriate baseline model that incorporates the demographic history of this aye-aye population, and identified a small number of candidate genes. Most notably, a suite of genes involved in olfaction — a key trait in these nocturnal primates — were identified as experiencing long-term balancing selection. We also conducted analyses to quantify the expected statistical power to detect positive and balancing selection in this population using site frequency spectrum-based inference methods, once accounting for the potentially confounding contributions of population history, recombination and mutation rate variation, and purifying and background selection. This work, presenting the first high-quality, genome-wide polymorphism data across the functional regions of the aye-aye genome, thus provides important insights into the landscape of episodic selective forces in this highly endangered species. 

Abstract Despite being an important biomedical model species for social behavior, the natural population history of the coppery titi monkey (Plecturocebus cupreus) remains largely uncharacterized, in part due to the scarcity of genomic resources available for the species. Apart from the inherent interest in the demographic dynamics of this abundant platyrrhine native to the Amazon forest of Brazil and Peru, this quantification will also serve as a central component of future genotype-to-phenotype studies, given the ability of historical population size change and structure to generate genetic associations. In this study, we deep-sequenced the genomes of six unrelated individuals and inferred a baseline demographic model based on observed levels and patterns of variation in the non-coding regions of the genome. In characterizing these demographic dynamics, we found that estimated population size changes correspond well to previously described speciation times as well as to large-scale climatic changes relating to glaciation patterns. 

ABSTRACT The rate of input of new genetic mutations, and the rate at which that variation is reshuffled, are key evolutionary processes shaping genomic diversity. Importantly, these rates vary not just across populations and species but also across individual genomes. Despite previous studies having demonstrated that failing to account for rate heterogeneity across the genome can bias the inference of both selective and neutral population genetic processes, mutation and recombination rate maps have to date only been generated for a relatively small number of organisms. Here, we infer such fine‐scale maps for the aye‐aye (Daubentonia madagascariensis)—a highly endangered strepsirrhine that represents one of the earliest splits in the primate clade and thus stands as an important outgroup to the more commonly studied haplorrhines—utilizing a recently released fully annotated genome combined with high‐quality population sequencing data. We compare our indirectly inferred rates to previous pedigree‐based estimates, finding further evidence of relatively low mutation and recombination rates in aye‐ayes compared to other primates. 

ABSTRACT Despite being a primate of considerable biomedical interest, particularly as a model for social behavior and neurobiology, the evolutionary processes shaping genetic variation in the coppery titi monkey (Plecturocebus cupreus) remain largely uncharacterized. Utilizing divergence and polymorphism data together with a recently published high-quality, annotated genome, we here infer the first fine-scale maps of mutation and recombination rates in this platyrrhine. We find a mean genome-wide mutation rate of between 0.93 × 10^-8and 1.61 × 10^-8per site per generation and a mean genome-wide recombination rate of 0.975 cM/Mb, in line with fine-scale rates estimated in other primates. In addition to providing novel biological insights into the mutation and recombination rates in this emerging model species for behavioral research, these fine-scale maps also improve our understanding of how the processes of mutation and recombination shape genetic variation in the coppery titi monkey genome, and their incorporation into evolutionary models will be a necessary aspect of future downstream inference of other evolutionary processes required to elucidate the genetic factors underlying the phenotypic traits studied in this species. 

ABSTRACT As a major model for biomedical research, the rhesus macaque (Macaca mulatta) is one of the most important and heavily studied nonhuman primates. Despite this importance, the level of population structure and subspecific division in this species remains relatively unclear; for example, the number of proposed subspecies in the literature ranges from one to six within China, with additional populations found across India. Motivated by an interest in comparing recombination rate landscapes between rhesus macaque subspecies, we re‐evaluated the demographic history of this group using a previously published data set from 79 wild‐born individuals sampled across 17 regions in China. In so doing, we found that previously published demographic models utilizing five subspecies did not well reproduce empirical levels or patterns of genomic variation. Thus, we re‐performed demographic inference, finding instead multiple lines of support for a single, interbreeding population (i.e., an absence of population structuring), as well as a population size‐change history linking periods of population growth and contraction to historical patterns of glaciation. Finally, utilizing this well‐fitting population history, we inferred a genome‐wide, fine‐scale recombination rate map for this population, finding mean rates consistent with those estimated in other closely related populations and species. However, we also observed notable difference in the fine‐scale landscape between rhesus macaques of Chinese and Indian origin – two populations widely used as models in biomedical research – highlighting the importance of accounting for population‐specific demographic history and recombination rate variation in future population genomic studies of this species. 

ABSTRACT We here present high‐quality, population‐level sequencing data from the X chromosome of the highly‐endangered aye‐aye,Daubentonia madagascariensis. Using both polymorphism‐ and divergence‐based inference approaches, we quantify fine‐scale mutation and recombination rate maps, study the demographic and selective processes additionally shaping variation on the X chromosome, and compare these estimates to those recently inferred from the autosomes in this species. Results suggest that an equal sex ratio is most consistent with observed patterns of variation, and that no sex‐specific demographic patterns are needed to fit the empirical site frequency spectrum. Further, reduced rates of recombination were observed relative to the autosomes as would be expected, whereas mutation rates were inferred to be similar. Utilizing the estimated population history together with the mutation and recombination rate maps, we evaluated evidence for both recent and recurrent selective sweeps as well as balancing selection across the X chromosome, finding no significant evidence supporting the action of these episodic processes. Overall, these analyses provide new insights into the evolution of the X chromosome in this species, which represents one of the earliest splits in the primate clade. 

Abstract Isolation by environment (IBE) is a population genomic pattern that arises when ecological barriers reduce gene flow between populations. Although current evidence suggests IBE is common in nature, few studies have evaluated the underlying mechanisms that generate IBE patterns. In this study, we evaluate five proposed mechanisms of IBE (natural selection against immigrants, sexual selection against immigrants, selection against hybrids, biased dispersal, environment-based phenological differences) that may give rise to host-associated differentiation within a sympatric population of the redheaded pine sawfly, Neodiprion lecontei, a species for which IBE has previously been detected. We first characterize the three pine species used by N. lecontei at the site, finding morphological and chemical differences among the hosts that could generate divergent selection on sawfly host-use traits. Next, using morphometrics and ddRAD sequencing, we detect modest phenotypic and genetic differentiation among sawflies originating from different pines that is consistent with recent, in situ divergence. Finally, via a series of laboratory assays – including assessments of larval performance on different hosts, adult mate and host preferences, hybrid fitness, and adult eclosion timing – we find evidence that multiple mechanisms contribute to IBE in N. lecontei. Overall, our results suggest IBE can emerge quickly, possibly due to multiple mechanisms acting in concert to reduce migration between different environments.