Biology subjects

Payseur, B. A.

Publications and source records attributed to Payseur, B. A..

12 recordsLinked to original sources

bioRxiv2026

Evolution of mutational fitness effects in island populations

The distribution of fitness effects (DFE) quantifies the selective consequences of newly arising mutations. Theoretical and empirical investigations of the DFE suggest that it is highly context-specific, shaped by both intrinsic properties of an organism (e.g., biological complexity) and extrinsic properties of a population (e.g., environment). Despite recent comparisons of the DFE between populations and species, little is known about how this distribution changes over shorter evolutionary timescales. Islands provide a powerful framework for understanding the impact of recent shifts in selection on the DFE, as founding populations often experience abrupt environmental changes. Using whole-genome, population-level sequence data, we investigate how such extreme transitions shape the DFE in two island radiations of Peromyscus mice: white-footed mice (P. leucopus) in Massachusettss Boston Harbor and deer mice (P. maniculatus) in the Gulf Islands of British Columbia. To measure the extent to which the selective effects of mutations have diverged between island and mainland populations, we leverage recent advances that extend DFE inference to multiple populations. By reconstructing the "joint DFE", we estimate both the strength of selection acting on distinct mutational classes and the correlation in mutational fitness effects between populations. We find that mutational fitness effects have diverged between island and mainland populations, despite the relative recency of these radiations. Comparisons between island populations, which reveal higher fitness effect correlations, suggest that this feature of the joint DFE captures broad-scale divergence in the environment populations inhabit. Together, our discoveries provide a rare empirical example of divergent environments shaping genome-wide patterns of fitness-affecting genetic variation in natural populations.

evolutionary biology↗

bioRxiv2025

Elevated mutation near crossovers inhibits the evolution of recombination

Recombination diversifies offspring genomes and helps ensure chromosome segregation during meiosis. Mutation rates are elevated near crossovers due to the induction of double-strand breaks and their imperfect repair, a byproduct of recombination typically ignored by theory designed to explain its evolution. To examine the evolutionary role of recombination-associated mutation, we analyze a population genetic model in which a modifier locus controls both the rate of recombination between two loci experiencing viability selection and the rate of mutation at those loci. Analytical and numerical results demonstrate that the advantage of recombination conferred by its capacity to remove epistatic, deleterious mutations is overcome by the selective cost of even small increases in the mutation rate. Simulations of finite populations show that recombination-associated mutation also decreases the probability of fixation of modifier alleles in the absence of epistasis. By incorporating the mutagenic effects of recombination, our analysis extends a rich body of theory to incorporate a molecular feature inherent in the formation of crossovers. Our findings suggest that higher recombination rate evolves by altering steps in the crossover pathway that are less likely to inflict mutational damage.

evolutionary biology↗

bioRxiv2025

The genomic imprint of chromosomal inversions and demographic history in island populations of deer mice

Populations that colonize islands experience novel selective pressures, fluctuations in size, and changes to their connectivity. Owing to their unique geographic setting, islands can function as natural laboratories in which to examine the interactions between demographic history and natural selection replicated across isolated populations. We used whole genome sequences of wild-caught deer mice (Peromyscus maniculatus) from two islands (Saturna and Pender) and one mainland location (Maple Ridge) in the Gulf Islands region of coastal British Columbia to investigate two primary determinants of genome-wide diversity: chromosomal inversions and non-equilibrium demographic history. We found that segregating inversions produce characteristic, large-scale distortions in allele frequencies and linkage disequilibrium that make it possible to identify and characterize them from short-read sequence data. Patterns of variation within and between karyotypes indicate that six inversion polymorphisms have been maintained by a shared history of balancing selection in both island and mainland populations. Whereas the estimated timing of contemporary population splits is consistent with the isolation of island populations from each other following the Last Glacial Maximum, ancestral island and mainland lineages are inferred to have diverged much earlier. These aspects of demographic history suggest that shared inversions existed long ago in a common ancestor or spread via limited gene flow between ancestral island and mainland lineages. Our results raise the possibility that inversions segregating among Gulf Islands populations are on similar evolutionary trajectories, providing a contrast to previous findings in mainland P. maniculatus and contributing to the emerging portrait of inversion evolution in this species.

evolutionary biology↗

bioRxiv2025

Population history across timescales in an urban archipelago

Contemporary patterns of genetic variation reflect the cumulative history of a population. Population splitting, migration, and changes in population size leave genomic signals that enable their characterization. Existing methods aimed at reconstructing these features of demographic history are often restricted in their temporal resolution, leaving gaps about how basic evolutionary parameters change over time. To illustrate the prospects for extracting insights about dynamic population histories, we turn to a system that has undergone dramatic changes on both geological and contemporary timescales - an urbanized, near-shore archipelago. Using whole genome sequences, we employed both common and novel summaries of variation to infer the demographic history of three populations of endemic white-footed mice (Peromyscus leucopus) in Massachusetts Boston Harbor. We find informative contrasts among the inferences drawn from these distinct patterns of diversity. While demographic models that fit the joint site frequency spectrum (jSFS) coincide with the known geological history of the Boston Harbor, patterns of linkage disequilibrium reveal collapses in population size on contemporary timescales that are not recovered by our candidate models. Historical migration between populations is also absent from best-fitting models for the jSFS, but rare variants show unusual clustering along the genome within individual mice, a pattern that is reproduced by simulations of recent migration. Together, our findings indicate that these urban archipelago populations have been shaped by both ancient geological processes and recent human influence. More broadly, our study demonstrates that the temporal resolution of demographic history can be extended by examining multiple facets of genomic variation. Significance StatementDetailed information about a populations history can be obtained by studying patterns of genomic variation, but these insights can be limited in their temporal scope. Our investigation of white-footed mice in the urban Boston Harbor archipelago demonstrates how combining multiple summaries of genomic variation enables a more complete reconstruction of population history over both the recent and distant past.

evolutionary biology↗

bioRxiv2025

Phenotypic and Developmental Dissection of an Instance of the Island Rule

Organismal body weight correlates with morphology, life history, physiology, and behavior, making it perhaps the most telling single indicator of an organisms evolutionary and ecological profile. Island populations provide an exceptional opportunity to study body weight evolution. In accord with the "island rule," insular small-bodied vertebrates often evolve larger sizes, whereas insular large-bodied vertebrates evolve smaller sizes. To understand how island populations evolve extreme sizes, we adopted a developmental perspective and compared a suite of traits with established connections to body size in the worlds largest wild house mice from Gough Island and mice from a smaller-bodied mainland strain. We pinpoint 24-hour periods during the third and fifth week of age in which Gough mice gain exceptionally more weight than mainland mice. We show that Gough mice accumulate more visceral fat beginning early in postnatal development. During a burst of weight gain, Gough mice shift toward carbohydrates and away from fat as fuel, despite being more active than and consuming equivalent amounts of food as mainland mice. Our findings showcase the value of developmental phenotypic characterization for discovering how body weight evolves in the context of broader patterns of trait evolution.

evolutionary biology↗

bioRxiv2025

Comparative Patterns of Variation on the X Chromosome and Autosomes: The Role of the Breeding Sex Ratio

In many populations, unequal numbers of females and males reproduce each generation. This imbalance in the breeding sex ratio (BSR) shapes patterns of genetic variation on the sex chromosomes and the autosomes in distinct ways. Despite recognition of this phenomenon, effects of the BSR on some aspects of variation remain unclear, especially for populations with non-equilibrium demographic histories. To address this gap in the field, we used coalescent simulations to examine relative patterns of variation at X-linked loci and autosomal loci in populations spanning the range of BSR with historical changes in population size. Shifts in BSR away from 1:1 reduce nucleotide diversity and the number of unique haplotypes and increase linkage disequilibrium and the frequency of the most common haplotype, with contrasting effects on X-linked loci and autosomal loci. Strong population bottlenecks transform relationships between the BSR, the site frequency spectrum, and linkage disequilibrium while relationships between the BSR, nucleotide diversity, and haplotype characteristics are broadly conserved. Our findings indicate that evolutionary interpretations of variation on the X chromosome should consider the combined effects of the BSR and demographic history. The genomic signatures we report could be used to reconstruct these fundamental population parameters from genomic data in natural populations. Significance StatementThe breeding sex ratio is a fundamental evolutionary parameter, but genomic analyses routinely assume it is 1:1. Our research characterizes the relationships between the breeding sex ratio and multiple facets of genomic variation and shows how these relationships change in the context of dynamic demographic histories. In doing so, we provide increasingly realistic expectations for patterns of X-linked and autosomal variation in population genomic datasets collected from natural populations.

evolutionary biology↗

bioRxiv2025

Population Genomics of Giant Mice from the Faroe Islands: Hybridization, Colonization, and a Novel Challenge to Identifying Genomic Targets of Selection

Populations that colonize islands provide unique insights into demography, adaptation, and the spread of invasive species. House mice on the Faroe Islands evolved exceptionally large bodies after colonization, generating interest from biologists since Darwin. To reconstruct the evolutionary history of these mice, we sequenced genomes of population samples from three Faroe Islands (Sandoy, Nolsoy, and Mykines) and Norway as a mainland comparison. Mice from the Faroe Islands are hybrids between the subspecies Mus musculus domesticus and M. m. musculus, with ancestry alternating along the genome. Analyses based on the site frequency spectrum of single nucleotide polymorphisms and the ancestral recombination graph (ARG) indicate that mice arrived on the Faroe Islands on a timescale consistent with transport by Norwegian Vikings, with colonization of Sandoy likely preceding colonization of Nolsoy. Substantial reductions in nucleotide diversity and effective population size associated with colonization suggest that mice on the Faroe Islands evolved large body size during periods of heightened genetic drift. Genomic scans for positive selection uncover windows with unusual site frequency spectra, but this pattern is mostly generated by clusters of singletons in individual mice. Variants showing evidence of selection in both Nolsoy and Sandoy based on the ARG are enriched for genes with neurological functions. Our findings reveal a dynamic evolutionary history for the enigmatic mice from Faroe Island and emphasize the challenges that accompany population genomic inferences in island populations. Significance StatementPopulations that colonize islands are expected to have unusual histories compared to their mainland counterparts. Using population genomic data, we conclude that giant mice living on the Faroe Islands originated from hybrids, invaded the islands on a timescale consistent with transport by Vikings, and persisted despite drastic reductions in population size. We also uncover a novel challenge to scanning genomes for genes involved in adaptation.

evolutionary biology↗

bioRxiv2024

Genetic background affects the strength of crossover interference in house mice

Meiotic recombination is required for faithful chromosome segregation in most sexually reproducing organisms and shapes the distribution of genetic variation in populations. Both the overall rate and the spatial distribution of crossovers vary within and between species. Adjacent crossovers on the same chromosome tend to be spaced more evenly than expected at random, a phenomenon known as crossover interference. Although interference has been observed in many taxa, the factors that influence the strength of interference are not well understood. We used house mice (Mus musculus), a well-established model system for understanding recombination, to study the effects of genetics and age on recombination rate and interference in the male germline. We analyzed crossover positions in 503 progeny from reciprocal F1 hybrids between inbred strains representing the three major subspecies of house mice. Consistent with previous studies, autosomal alleles from M. m. musculus tend to increase recombination rate, while inheriting a M. m. musculus X chromosome decreases recombination rate. Old males transmit an average of 0.6 more crossovers per meiosis (5.0%) than young males, though the effect varies across genetic backgrounds. We show that the strength of crossover interference depends on genotype, providing a rare demonstration that interference evolves over short timescales. Differences between reciprocal F1s suggest that X-linked factors modulate the strength of interference. Our findings motivate additional comparisons of interference among recently diverged species and further examination of the role of paternal age in determining the number and positioning of crossovers.

genetics↗

bioRxiv2021

Background selection under evolving recombination rates

Background selection (BGS), the effect that purifying selection exerts on sites linked to deleterious alleles, is expected to be ubiquitous across eukaryotic genomes. The effects of BGS reflect the interplay of the rates and fitness effects of deleterious mutations with recombination. A fundamental assumption of BGS models is that recombination rates are invariant over time. However, in some lineages recombination rates evolve rapidly, violating this central assumption. Here, we investigate how recombination rate evolution affects genetic variation under BGS. We show that recombination rate evolution modifies the effects of BGS in a manner similar to a localised change in the effective population size, potentially leading to an underestimation of the genome-wide effects of selection. Furthermore, we find evidence that recombination rate evolution in the ancestors of modern house mice may have impacted inferences of the genome-wide effects of selection in that species.

evolutionary biology↗

bioRxiv2021

Statistical inference in population genomics

The field of population genomics has grown rapidly in response to the recent advent of affordable, large-scale sequencing technologies. As opposed to the situation during the majority of the 20th century, in which the development of theoretical and statistical population-genetic insights out-paced the generation of data to which they could be applied, genomic data are now being produced at a far greater rate than they can be meaningfully analyzed and interpreted. With this wealth of data has come a tendency to focus on fitting specific (and often rather idiosyncratic) models to data, at the expense of a careful exploration of the range of possible underlying evolutionary processes. For example, the approach of directly investigating models of adaptive evolution in each newly sequenced population or species often neglects the fact that a thorough characterization of ubiquitous non-adaptive processes is a prerequisite for accurate inference. We here describe the perils of these tendencies, present our consensus views on current best practices in population genomic data analysis, and highlight areas of statistical inference and theory that are in need of further attention. Thereby, we argue for the importance of defining a biologically relevant baseline model tuned to the details of each new analysis, of skepticism and scrutiny in interpreting model-fitting results, and of carefully defining addressable hypotheses and underlying uncertainties.

evolutionary biology↗

bioRxiv2020

Evolution of Boldness and Exploratory Behavior in Giant Mice from Gough Island

Island populations are hallmarks of extreme phenotypic evolution. Radical changes in resource availability and predation risk accompanying island colonization drive changes in behavior, which Darwin likened to tameness in domesticated animals. Although many examples of animal boldness are found on islands, the heritability of observed behaviors, a requirement for evolution, remains largely unknown. To fill this gap, we profiled anxiety and exploration in island and mainland inbred strains of house mice raised in a common laboratory environment. The island strain was descended from mice on Gough Island, the largest wild house mice on record. Experiments utilizing open environments across two ages showed that Gough Island mice are bolder and more exploratory, even when a shelter is provided. Concurrently, Gough Island mice retain an avoidance response to predator urine. F1 offspring from crosses between these two strains behave more similarly to the mainland strain for most traits, suggesting recessive mutations contributed to behavioral evolution on the island. Our results provide a rare example of novel, inherited behaviors in an island population and demonstrate that behavioral evolution can be specific to different forms of perceived danger. Our discoveries pave the way for a genetic understanding of how island populations evolve unusual behaviors.

evolutionary biology↗

bioRxiv2019

Disrupted gene networks in subfertile hybrid house mice

The Dobzhansky-Muller model provides a widely accepted mechanism for the evolution of reproductive isolation: incompatible substitutions disrupt interactions between genes. To date, few candidate incompatibility genes have been identified, leaving the genes driving speciation mostly uncharacterized. The importance of interactions in the Dobzhansky-Muller model suggests that gene coexpression networks provide a powerful framework to understand disrupted pathways associated with postzygotic isolation. Here, we perform Weighted Gene Coexpression Network Analysis (WGCNA) to infer gene interactions in hybrids of two recently diverged European house mouse subspecies, Mus mus domesticus and M. m. musculus, which commonly show hybrid male sterility or subfertility. We use genome-wide testis expression data from 467 hybrid mice from two mapping populations: F2s from a laboratory cross between wild-derived pure subspecies strains and offspring of natural hybrids captured in the Central Europe hybrid zone. This large data set enabled us to build a robust consensus network using hybrid males with fertile phenotypes. We identify several expression modules, or groups of coexpressed genes, that are disrupted in subfertile hybrids, including modules functionally enriched for spermatogenesis, cilium and sperm flagellum organization, chromosome organization and DNA repair, and including genes expressed in spermatogonia, spermatocytes and spermatids. Our network-based approach enabled us to hone in on specific hub genes likely to be influencing module-wide gene expression and hence potentially driving Dobzhansky-Muller incompatibilities. A total of 69 (24.6%) of these genes lie in sterility loci identified previously in these mapping populations, and represent promising candidate barrier genes and targets for future functional analysis.

evolutionary biology↗