Biology subjects

Terbot, J. W.

Publications and source records attributed to Terbot, J. W..

12 recordsLinked to original sources

bioRxiv2026

Inferring the demographic history of Chinese and Indian rhesus macaque (Macaca mulatta) populations from PacBio HiFi long-read sequencing data

The rhesus macaque (Macaca mulatta) is one of the most widely used animal models in biomedical research, both as it resembles humans in key biological aspects and as it is characterized by a broad geographic range. Most of the individuals housed in U.S. research colonies have been sampled from either China or India, though notably the source population of these animals has significantly shifted over time. Given the substantial genetic and immunological differences between these populations, a deeper understanding of the underlying population structure is critically important for biomedical interpretation. Despite this, the demographic histories of these two populations remain poorly resolved. Here, we present an analysis of whole-genome, PacBio HiFi long-read sequencing data from ten unrelated individuals of each population, applying four related model- and non-model based demographic inference approaches, in order to reconstruct their ancestral history. We evaluated the fit of the subsequently estimated models against the empirical data, and incorporated underlying uncertainty in the mutation rates used for scaling. We inferred a well-fitting population history characterized by substantial structure between Chinese and Indian populations, with a split time [~]140,000 generations ago from an ancestral population of [~]65,000 individuals. We additionally inferred the subsequent history of size change within, and gene flow between, these populations, reaching the current estimated sizes of [~]220,000 individuals in the Chinese population and [~]14,000 individuals in the Indian population. The robust baseline demographic model established in this study will serve as a valuable resource for future research on this species, including for improved fine-scale recombination mapping, selection inference, and association studies.

evolutionary biology↗

bioRxiv2026

Inferring patterns of purifying, positive and balancing selection in the coppery titi monkey (Plecturocebus cupreus) utilizing a well-fit evolutionary baseline model

Despite the coppery titi monkey (Plecturocebus cupreus) being a model system for the study of neurodevelopment and behavior, the evolutionary forces shaping observed levels and patterns of genetic variation in the species have remained poorly studied. In order to illuminate the pervasive eCects of purifying and background selection, we have fit a distribution of fitness eCects of newly arising exonic mutations, utilizing patterns of polymorphism and divergence based on a recently published high-quality genome assembly. To further characterize episodically acting selective processes, we additionally performed the first whole-genome scans for recent positive and balancing selection in this species, reducing false-positive rates by incorporating the demographic history of the population into an evolutionary null model. These scans identified a small number of biomedically-relevant genes with strong statistical support for having experienced recent selective sweeps or long-term balancing selection. In addition, we identified four genomic deletions bearing the signatures of balancing selection. Taken together, this study provides the first insights into patterns of persistent and episodic selective processes in this species.

evolutionary biology↗

bioRxiv2026

Inferring fine-scale rates of mutation and recombination in the coppery titi monkey (Plecturocebus cupreus)

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 x 10-8 and 1.61 x 10-8 per 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.

evolutionary biology↗

bioRxiv2026

Inferring the demographic history of coppery titi monkeys (Plecturocebus cupreus) from high-quality, whole-genome, population-level data

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.

evolutionary biology↗

bioRxiv2025

Interpreting patterns of X chromosomal relative to autosomal diversity in aye-ayes(Daubentonia madagascariensis)

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.

evolutionary biology↗

bioRxiv2024

Inferring fine-scale mutation and recombination rate maps in aye-ayes (Daubentonia madagascariensis)

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.

evolutionary biology↗

bioRxiv2024

Inferring the demographic history of aye-ayes (Daubentonia madagascariensis) from high-quality, whole-genome, population-level data

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 unrelated 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 the species to consist of 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, approximately 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.

evolutionary biology↗

bioRxiv2024

A whole-genome scan for evidence of recent positive and balancing selection in aye-ayes (Daubentonia madagascariensis) utilizing a well-fit evolutionary baseline model

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.

evolutionary biology↗

bioRxiv2023

A simulation framework for modeling the within-patient evolutionary dynamics of SARS-CoV-2

The global impact of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) has led to considerable interest in detecting novel beneficial mutations and other genomic changes that may signal the development of variants of concern (VOCs). The ability to accurately detect these changes within individual patient samples is important in enabling early detection of VOCs. Such genomic scans for positive selection are best performed via comparison of empirical data to simulated data wherein evolutionary factors, including mutation and recombination rates, reproductive and infection dynamics, and purifying and background selection, can be carefully accounted for and parameterized. While there has been work to quantify these factors in SARS-CoV-2, they have yet to be integrated into a baseline model describing intra-host evolutionary dynamics. To construct such a baseline model, we develop a simulation framework that enables one to establish expectations for underlying levels and patterns of patient-level variation. By varying eight key parameters, we evaluated 12,096 different model-parameter combinations and compared them to existing empirical data. Of these, 592 models ([~]5%) were plausible based on the resulting mean expected number of segregating variants. These plausible models shared several commonalities shedding light on intra-host SARS-CoV-2 evolutionary dynamics: severe infection bottlenecks, low levels of reproductive skew, and a distribution of fitness effects skewed towards strongly deleterious mutations. We also describe important areas of model uncertainty and highlight additional sequence data that may help to further refine a baseline model. This study lays the groundwork for the improved analysis of existing and future SARS-CoV-2 within-patient data. Significance StatementDespite its tremendous impact on human health, a comprehensive evolutionary baseline model has yet to be developed for studying the within-host population genomics of SARS-CoV-2. Importantly, such modeling would enable improved analysis and provide insights into the key evolutionary dynamics governing SARS-CoV-2 evolution. Given this need, we have here quantified a set of plausible baseline models via large-scale simulation. The commonly shared features of these relevant models - including severe infection bottlenecks, low levels of progeny skew, and a high rate of strongly deleterious mutations - lay the foundation for sophisticated analyses of SARS-CoV-2 evolution within patients using these baseline models.

evolutionary biology↗

bioRxiv2023

Multiple mechanisms contribute to isolation-by-environment in the redheaded pine sawfly, Neodiprion lecontei

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.

evolutionary biology↗

bioRxiv2022

Body size as a magic trait in two plant-feeding insect species

When gene flow accompanies speciation, recombination can decouple divergently selected loci and loci conferring reproductive isolation. This barrier to sympatric divergence disappears when assortative mating and disruptive selection involve the same "magic" trait. Although magic traits could be widespread, the relative importance of different types of magic traits to speciation remains unclear. Because body size frequently contributes to host adaptation and assortative mating in plant-feeding insects, we evaluated several magic trait predictions for this trait in a pair of sympatric Neodiprion sawfly species adapted to different pine hosts. A large morphological dataset revealed that sawfly adults from populations and species that use thicker-needled pines are consistently larger than those that use thinner needled-pines. Fitness data from recombinant backcross females revealed that egg size is under divergent selection between the preferred pines. Lastly, mating assays revealed strong size-assortative mating within and between species in three different crosses, with the strongest prezygotic isolation between populations that have the greatest interspecific size differences. Together, our data support body size as a magic trait in pine sawflies and possibly many other plant-feeding insects. Our work also demonstrates how intraspecific variation in morphology and ecology can cause geographic variation in the strength of prezygotic isolation.

evolutionary biology↗

bioRxiv2019

Mother knows best: maternal egg-clutch size predicts larval group size in pine sawflies (genus Neodiprion)

Evolutionary conflicts are pervasive in nature and have the potential to drive antagonistic coevolution of conflict-related traits. However, when such conflicts are weak or idiosyncratic, phenotypic signatures of coevolutionary arms races may be absent. Here, we ask whether variation in group-living traits among pine-sawfly species in the genus Neodiprion is consistent with a history of parent-offspring conflict. To address this question, we compile data on adult female clutch size, larval aggregation behavior, and larval group size for a monophyletic group of 19 eastern North American Neodiprion species from field observations, laboratory assays, and published descriptions. We then evaluate the extent to which each trait exhibits phylogenetic signal and, based on these results, examine correlations between group-size traits both with and without phylogenetic correction. Although female oviposition behavior and larval grouping behavior varies among species and variation in these traits is decoupled from phylogeny, we find no evidence of antagonistic coevolution between these traits. Furthermore, while larvae are physically capable of dispersal, female clutch size is a strong predictor of larval colony size, indicating that larvae do not substantially alter initial group size after hatching. Thus, although theoretical work demonstrates the potential for parent-offspring conflict over group size in animals that lack parental care, our data suggest that this type of conflict is not likely to be a long-term driver of phenotypic evolution.

evolutionary biology↗