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Simulation is a key tool in population genetics for both methods development and empirical research, but producing simulations that recapitulate the main features of genomic data sets remains a major obstacle. Today, more realistic simulations are possible thanks to large increases in the quantity and quality of available genetic data, and to the sophistication of inference and simulation software. However, implementing these simulations still requires substantial time and specialized knowledge. These challenges are especially pronounced for simulating genomes for species that are not well-studied, since it is not always clear what information is required to produce simulations with a level of realism sufficient to confidently answer a given question. The community-developed frameworkstdpopsimseeks to lower this barrier by facilitating the simulation of complex population genetic models using up-to-date information. The initial version ofstdpopsimfocused on establishing this framework using six well-characterized model species (Adrion et al., 2020). Here, we report on major improvements made in the new release ofstdpopsim(version 0.2), which includes a significant expansion of the species catalog and substantial additions to simulation capabilities. Features added to improve the realism of the simulated genomes include non-crossover recombination and provision of species-specific genomic annotations. Through community-driven efforts, we expanded the number of species in the catalog more than three-fold and broadened coverage across the tree of life. During the process of expanding the catalog, we have identified common sticking points and developed best practices for setting up genome-scale simulations. We describe the input data required for generating a realistic simulation, suggest good practices for obtaining the relevant information from the literature, and discuss common pitfalls and major considerations. These improvements tostdpopsimaim to further promote the use of realistic whole-genome population genetic simulations, especially in non-model organisms, making them available, transparent, and accessible to everyone.

Several bat species act as asymptomatic reservoirs for many viruses that are highly pathogenic in other mammals. Here, we have characterized the functional diversification of the protein kinase R (PKR), a major antiviral innate defense system. Our data indicate that PKR has evolved under positive selection and has undergone repeated genomic duplications in bats in contrast to all studied mammals that have a single copy of the gene. Functional testing of the relationship between PKR and poxvirus antagonists revealed how an evolutionary conflict with ancient pathogenic poxviruses has shaped a specific bat host-virus interface. We determined that duplicated PKRs of the Myotis species have undergone genetic diversification, allowing them to collectively escape from and enhance the control of DNA and RNA viruses. These findings suggest that viral-driven adaptations in PKR contribute to modern virus-bat interactions and may account for bat-specific immunity.

Understanding the impacts of selection pressures influencing modern-day genomic diversity is a major goal of evolutionary genomics. In particular, the contribution of selective sweeps to adaptation remains an open question, with persistent statistical limitations on the power and specificity of sweep detection methods. Sweeps with subtle genomic signals have been particularly challenging to detect. While many existing methods powerfully detect specific types of sweeps and/or those with strong signals, their power comes at the expense of versatility. We present Flex-sweep, a machine learning-based tool designed to detect sweeps with a variety of subtle signals, including those thousands of generations old. It is especially valuable for non-model organisms, for which we have neither expectations about the overall characteristics of sweeps nor outgroups with population-level sequencing to otherwise facilitate detecting very old sweeps. We show that Flex-sweep has the power to detect sweeps with subtle signals, even in the face of demographic model misspecification, recombination rate heterogeneity, and background selection. Flex-sweep detects sweeps up to 0.125 * 4Negenerations old, including those that are weak, soft, and/or incomplete; it can also detect strong, complete sweeps up to 0.25 * 4Negenerations old. We apply Flex-sweep to the 1000 Genomes Yoruba data set and, in addition to recovering previously identified sweeps, show that sweeps disproportionately occur within genic regions and close to regulatory regions. In addition, we show that virus-interacting proteins (VIPs) are strongly enriched for selective sweeps, recapitulating previous results that demonstrate the importance of viruses as a driver of adaptive evolution in humans.

Several bat species act as asymptomatic reservoirs for many viruses that are instead highly pathogenic in other mammals. Here, we have characterized the functional diversification of the Protein kinase R (PKR), a major antiviral innate defense system. Our data indicate that PKR has evolved under positive selection and has undergone repeated genomic duplications in bats, in contrast to all studied mammals that possess a single copy of the gene. Functional testing of the relationship between PKR and poxvirus antagonists revealed how an evolutionary conflict with ancient pathogenic poxviruses has shaped a specific bat host-virus interface. More importantly, we determined that duplicated PKRs of the Myotis species have undergone functional diversification allowing them to collectively escape from and enhance control of DNA and RNA viruses. These findings suggest that viral-driven adaptations in PKR contribute to modern virus-bat interactions and may account for bat specific immunity.

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.

Advances in genome sequencing have improved our understanding of the genetic basis of human diseases, and thousands of human genes have been associated with different diseases. Recent genomic adaptation at disease genes has not been well characterized. Here, we compare the rate of strong recent adaptation in the form of selective sweeps between mendelian, non-infectious disease genes and non-disease genes across distinct human populations from the 1000 Genomes Project. We find that mendelian disease genes have experienced far less selective sweeps compared to non-disease genes especially in Africa. Investigating further the possible causes of the sweep deficit at disease genes, we find that this deficit is very strong at disease genes with both low recombination rates and with high numbers of associated disease variants, but is almost non-existent at disease genes with higher recombination rates or lower numbers of associated disease variants. Because segregating recessive deleterious variants have the ability to interfere with adaptive ones, these observations strongly suggest that adaptation has been slowed down by the presence of interfering recessive deleterious variants at disease genes. These results suggest that disease genes suffer from a transient inability to adapt as fast as the rest of the genome.

Despite the widespread notion that animal-mediated seed dispersal led to the evolution of fruit traits that attract mutualistic frugivores, the dispersal syndrome hypothesis remains controversial, particularly for complex traits such as fruit scent. Here, we test this hypothesis in a community of mutualistic, ecologically important neotropical bats (Carolliaspp.) and plants (Piperspp.) that communicate primarily via chemical signals. We found greater bat consumption is significantly associated with scent chemical diversity and presence of specific compounds, which fit multi-peak selective regime models inPiper. Through behavioural assays, we foundCarolliaprefer certain compounds, particularly 2-heptanol, which evolved as a unique feature of twoPiperspecies highly consumed by these bats. Thus, we demonstrate that volatile compounds emitted by neotropicalPiperfruits evolved in tandem with seed dispersal by scent-orientedCarolliabats. Specifically, fruit scent chemistry in somePiperspecies fits adaptive evolutionary scenarios consistent with a dispersal syndrome hypothesis. While other abiotic and biotic processes likely shaped the chemical composition of ripe fruit scent inPiper, our results provide some of the first evidence of the effect of bat frugivory on plant chemical diversity.

Bitter taste facilitates the detection of potentially harmful substances and is perceived via bitter taste receptors (TAS2Rs) expressed on the tongue and oral cavity in vertebrates. In primates, TAS2R16 specifically recognizes β-glucosides, which are important in cyanogenic plants' use of cyanide as a feeding deterrent. In this study, we performed cell-based functional assays for investigating the sensitivity of TAS2R16 to β-glucosides in three species of bamboo lemurs ( Prolemur simus, Hapalemur aureus and H. griseus ), which primarily consume high-cyanide bamboo. TAS2R16 receptors from bamboo lemurs had lower sensitivity to β-glucosides, including cyanogenic glucosides, than that of the closely related ring-tailed lemur ( Lemur catta ). Ancestral reconstructions of TAS2R16 for the bamboo-lemur last common ancestor (LCA) and that of the Hapalemur LCA showed an intermediate sensitivity to β-glucosides between that of the ring-tailed lemurs and bamboo lemurs. Mutagenetic analyses revealed that P. simus and H. griseus had separate species - specific substitutions that led to reduced sensitivity. These results indicate that low sensitivity to β-glucosides at the cellular level—a potentially adaptive trait for feeding on cyanogenic bamboo—evolved independently after the Prolemur – Hapalemur split in each species.

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SummaryThe current SARS-CoV-2 pandemic has emphasized the vulnerability of human populations to novel viral pressures, despite the vast array of epidemiological and biomedical tools now available. Notably, modern human genomes contain evolutionary information tracing back tens of thousands of years, which may help identify the viruses that have impacted our ancestors – pointing to which viruses have future pandemic potential. Here, we apply evolutionary analyses to human genomic datasets to recover selection events involving tens of human genes that interact with coronaviruses, including SARS-CoV-2, that likely started more than 20,000 years ago. These adaptive events were limited to the population ancestral to East Asian populations. Multiple lines of functional evidence support an ancient viral selective pressure, and East Asia is the geographical origin of several modern coronavirus epidemics. An arms race with an ancient coronavirus, or with a different virus that happened to use similar interactions as coronaviruses with human hosts, may thus have taken place in ancestral East Asian populations. By learning more about our ancient viral foes, our study highlights the promise of evolutionary information to better predict the pandemics of the future. Importantly, adaptation to ancient viral epidemics in specific human populations does not necessarily imply any difference in genetic susceptibility between different human populations, and the current evidence points toward an overwhelming impact of socioeconomic factors in the case of COVID-19.

Gene duplication is a key source of evolutionary innovation, and multigene families evolve in a birth-death process, continuously duplicating and pseudogenizing through time. To empirically test hypotheses about adaptive expansion and contraction of multigene families across species, models infer gene gain and loss in light of speciation events and these inferred gene family expansions may lead to interpretations of adaptations in particular lineages. While the relative abundance of a gene subfamily in the subgenome may reflect its functional importance, tests based on this expectation can be confounded by the complex relationship between the birth-death process of gene subfamily evolution and the species phylogeny. Using simulations, we confirmed tree heterogeneity as a confounding factor in inferring multi-gene adaptation, causing spurious associations between shifts in birth-death rate and lineages with higher branching rates. We then used the olfactory receptor (OR) repertoire, the largest gene family in the mammalian genome, of different bat species with divergent diets to test whether expansions in olfactory receptors are associated with shifts to frugivorous diets. After accounting for tree heterogeneity, we robustly inferred that certain OR subfamilies exhibited expansions associated with dietary shifts to frugivory. Taken together, these results suggest ecological correlates of individual OR gene subfamilies can be identified, setting the stage for detailed inquiry into within-subfamily functional differences.

The current severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic has emphasized the vulnerability of human populations to novel viral pressures, despite the vast array of epidemiological and biomedical tools now available. Notably, modern human genomes contain evolutionary information tracing back tens of thousands of years, which may help identify the viruses that have impacted our ancestors—pointing to which viruses have future pandemic potential. Here, we apply evolutionary analyses to human genomic datasets to recover selection events involving tens of human genes that interact with coronaviruses, including SARS-CoV-2, that likely started more than 20,000 years ago. These adaptive events were limited to the population ancestral to East Asian populations. Multiple lines of functional evidence support an ancient viral selective pressure, and East Asia is the geographical origin of several modern coronavirus epidemics. An arms race with an ancient coronavirus, or with a different virus that happened to use similar interactions as coronaviruses with human hosts, may thus have taken place in ancestral East Asian populations. By learning more about our ancient viral foes, our study highlights the promise of evolutionary information to better predict the pandemics of the future. Importantly, adaptation to ancient viral epidemics in specific human populations does not necessarily imply any difference in genetic susceptibility between different human populations, and the current evidence points toward an overwhelming impact of socioeconomic factors in the case of coronavirus disease 2019 (COVID-19)., Graphical abstract, Souilmi et al. find that strong genetic adaptation occurred in human East Asian populations, at multiple genes that interact with coronaviruses, including SARS-CoV-2. The adaptation started 25,000 years ago, and functional analysis of the adapting genes supports the occurrence of a corona- or related virus epidemic around that time in East Asia.

In non-model species, targeted gene capture (selective enrichment of specific genomic regions of interest) applications in molecular ecology have been limited by the practicalities of capture design. Currently, the minimal requirement for designing capture probes is a transcriptome, or established reference genome for the species of interest. When an established, annotated reference genome is unavailable, one common approach is to design probes from annotated reference genomes (or transcriptomes) of related species. Unfortunately, as divergence between probes and the genome of interest increases, such as occurs during directional selection, capture performance decreases. Here I introduce orthoCapture, a tool to overcome such limitations by mining unannotated whole-genome sequence (WGS) data from non-model species and/or their close relatives to allow probe design using multiple genomic sources. orthoCapture finds orthologs in WGS data from multiple related species to create a set of exon sequences that encompasses the diversity of the exons of interest. These “design sequences” can then be used to design capture probes for the species of interest. orthoCapture thus eliminates the need for transcriptome or whole-genome sequencing for bait capture experiments, making this technique accessible for molecular ecology and conservation studies. Use of orthoCapture is via command-line interface on Unix systems, and requires the input of a gene sequence from an unrelated annotated genome and a fasta database from a target, unannotated genome (e.g., whole-genome shotgun contigs). The output, sequence templates from the nonannotated genomic data, allows probe creation by any commercial company providing gene capture services.

Animals rely on multiple sensory modalities to perform even the simplest ecological tasks (Burkhardt 1989; Siemers and Schnitzler 2000; Holland et al. 2005; Knaden and Graham 2016). One of the main goals of behavioral and sensory ecology lies in understanding the ability of different species to employ and modulate their sensory modes in the context of different environmental cues, and how the resulting behavioral decisions ultimately affect their ecology and evolution. Frugivores use various cues, including components of fruit color (Burkhardt 1989; Hiramatsu et al. 2008; Melin et al. 2008; Osorio and Vorobyev 2008; Valenta et al. 2013), shape (Von Helversen and Von Helversen 1999; Kalko and Condon 1998), and scent (Sanchez et al. 2006; Valenta et al. 2013) to find and select ripe fruit, and exhibit corresponding sensory specializations in their visual, auditory, and/or olfactory systems to target those cues (Catania 1999; Muller et al. 2007; Vanderelst et al. 2010). Little is known, however, about what scenarios facilitate or constrain sensory use and modulation during fruit location, selection, and acquisition in vertebrate frugivores. Insight into these processes would provide mechanistic understanding of the behaviors underlying their foraging ecology. Frugivorous and omnivorous Neotropical leaf-nosed bats (Phyllostomidae) use three major senses, echolocation, olfaction, and vision, for navigation and foraging (e.g., Reiger and Jakob 1988; Gutierrez et al. 2018; Thiele and Winter 2005; Kalko and Condon 1998), which makes these organisms an exceptional system for investigating the relative role of different sensory modes during ecologically important tasks. Although there has been some work on phyllostomid vision, including comparisons of their short- and long-wave opsins (Muller et al. 2007, 2009; Kries et al. 2018; Sadier et al. 2018; Gutierrez et al. 2018), the importance of vision in ripe fruit location and selection has not been experimentally tested in phyllostomids. By contrast, experimental evidence strongly suggests that omnivorous phyllostomids rely primarily on echolocation to locate fruits (Kalko and Condon 1998), and specialized frugivores employ either olfaction or a combination of olfaction and echolocation to locate ripe fruit (Kalko and Schnitzler 1993; Korine and Kalko 2005; Hodgkison et al. 2007, 2013). The relative importance of different sensory modes for fruit detection may depend on which plant cues can be readily perceived within a specific environmental context. To date, little is known about whether and how frugivorous phyllostomids integrate their primary sensory modes (echolocation and olfaction) conditional on which plant cues are present. While plant scents can travel over short or long distances (Riffell et al. 2014), they are rarely directional and may be difficult to detect in saturated scent environments such as rainforests. Conversely, echolocation allows for highly precise prey detection (Schnitzler and Kalko 2001; Brinklov et al. 2009; Jakobsen et al. 2013), but phyllostomids emit short, high frequency, and low intensity calls (Thies et al. 1998; Korine and Kalko 2005). The echoes from these calls provide information about size, shape, texture, range, and position of an object in space relative to the bat (Simmons et al. 1975, 1983; Simmons and Stein 1980; Neuweiler 1989; Schmidt et al. 2000; Schnitzler and Kalko 2001), but these types of information are only effective at very short distances because low intensity, high frequency calls attenuate rapidly in warm, humid environments (e.g., 45–90 kHz attenuate at 1.4–4 dB/m at 25°C and 80% humidity; Jakobsen et al. 2013). Additionally, surrounding foliage can produce acoustic masking effects that may complicate fruit detection (Arlettaz et al. 2001; Korine and Kalko 2005). Therefore, flexibility in olfaction versus echolocation use could be highly beneficial for frugivorous bats given the limitations of each sensory mode within complex forest environments. Here, we study the primary plant cues from vegetation and fruits and how they relate to the roles of echolocation and olfaction for fruit detection and localization in the chestnut short-tailed fruit bat, Carollia castanea, a highly abundant frugivore and ecologically important seed disperser that inhabits forests in Central and South America (Bonaccorso 1979; Fleming 1991; Fig. 1). This research builds upon the seminal work of Thies et al. (1998), which demonstrated the importance of olfaction for fruit detection in Carollia; here we investigate the relative contributions of vegetative and fruit scent cues that drive C. castanea’s foraging decisions, and how varying foraging scenarios (i.e., changing of plant scent cues) may affect the relative reliance of these bats on olfaction versus echolocation for fruit detection. Evaluating the effect of vegetative scents on frugivore foraging behavior is particularly important because background scents from neighboring plants can impact the ability of animals to discriminate fruit or flower odors (Riffell et al. 2014) or, if vegetative scents are from the same plant, they can amplify the scent of the food source and make it more potent (e.g., Raguso and Willis 2005; Rusch et al. 2016; Stutz et al. 2016; McArthur et al. 2019). Open in a separate window Fig. 1 Study organisms, Carollia castanea (left) and Piper sancti-felicis (right). Photo credit: S.E. Santana.

Several taxonomically distinct mammalian groups—certain microbats and cetaceans (e.g., dolphins)—share both morphological adaptations related to echolocation behavior and strong signatures of convergent evolution at the amino acid level across seven genes related to auditory processing. Aye-ayes (Daubentonia madagascariensis) are nocturnal lemurs with a specialized auditory processing system. Aye-ayes tap rapidly along the surfaces of trees, listening to reverberations to identify the mines of wood-boring insect larvae; this behavior has been hypothesized to functionally mimic echolocation. Here we investigated whether there are signals of convergence in auditory processing genes between aye-ayes and known mammalian echolocators. We developed a computational pipeline (Basic Exon Assembly Tool) that produces consensus sequences for regions of interest from shotgun genomic sequencing data for nonmodel organisms without requiring de novo genome assembly. We reconstructed complete coding region sequences for the seven convergent echolocating bat–dolphin genes for aye-ayes and another lemur. We compared sequences from these two lemurs in a phylogenetic framework with those of bat and dolphin echolocators and appropriate nonecholocating outgroups. Our analysis reaffirms the existence of amino acid convergence at these loci among echolocating bats and dolphins; some methods also detected signals of convergence between echolocating bats and both mice and elephants. However, we observed no significant signal of amino acid convergence between aye-ayes and echolocating bats and dolphins, suggesting that aye-aye tap-foraging auditory adaptations represent distinct evolutionary innovations. These results are also consistent with a developing consensus that convergent behavioral ecology does not reliably predict convergent molecular evolution.