Bret A Payseur's research while affiliated with University of Wisconsin–Madison and other places
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Publications (123)
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 rat...
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 outpaced the generation of data to which they could be applie...
Some of the most compelling examples of morphological evolution come from island populations. Alterations in the size and shape of the mandible have been repeatedly observed in murid rodents following island colonization. Despite this pattern and the significance of the mandible for dietary adaptation, the genetic basis of island-mainland divergenc...
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 rat...
Meiotic recombination affects fertility, shuffles genomes, and modulates the effectiveness of natural selection. Despite conservation of the recombination pathway, the rate of recombination varies among individuals and along chromosomes. Recombination rate also differs among cells from the same organism, but this form of variation has received less...
The field of population genomics has grown rapidly with 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, genomi...
Demographic factors such as migration rate and population size can impede or facilitate speciation. In hybrid zones, reproductive boundaries between species are tested and demography mediates the opportunity for admixture between lineages that are partially isolated. Genomic ancestry is a powerful tool for revealing the history of admixed populatio...
Natural hybrid zones offer a powerful framework for understanding the genetic basis of speciation in progress because ongoing hybridization continually creates unfavorable gene combinations. Evidence indicates that postzygotic reproductive isolation is often caused by epistatic interactions between mutations in different genes that evolved independ...
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...
In most species that reproduce sexually, successful gametogenesis requires recombination during meiosis. The number and placement of crossovers (COs) vary among individuals, with females and males often presenting the most striking contrasts. Despite the recognition that the sexes recombine at different rates (heterochiasmy), existing data fail to...
A key challenge in understanding how organisms adapt to their environments is to identify the mutations and genes that make it possible. By comparing patterns of sequence variation to neutral predictions across genomes, the targets of positive selection can be located. We applied this logic to house mice that invaded Gough Island, an unusual popula...
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...
Although meiotic recombination is required for successful gametogenesis in most species that reproduce sexually, the rate of crossing over varies among individuals. Differences in recombination rate between females and males are perhaps the most striking form of this variation. To determine how sex shapes the evolution of recombination, we directly...
Island populations repeatedly evolve extreme body sizes, but the genomic basis of this pattern remains largely unknown. To understand how organisms on islands evolve gigantism, we compared genome-wide patterns of gene expression in Gough Island mice, the largest wild house mice in the world, and mainland mice from the WSB/EiJ wild-derived inbred st...
Positive selection and purifying selection reduce levels of variation at linked neutral loci. One consequence of these processes is that the amount of neutral diversity and the meiotic recombination rate are predicted to be positively correlated across the genome - a prediction met in some species but not others. To better document the prevalence o...
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-...
Through recombination, genes are freed to evolve more independently of one another, unleashing genetic variance hidden in the linkage disequilibrium that accumulates through selection combined with drift. Yet crossover numbers are evolutionarily constrained, with at least one and not many more than one crossover per bivalent in most taxa. Crossover...
Meiotic recombination shapes evolution and helps to ensure proper chromosome segregation in most species that reproduce sexually. Recombination itself evolves, with species showing considerable divergence in the rate of crossing‐over. However, the genetic basis of this divergence is poorly understood. Recombination events are produced via a complic...
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-...
The synaptonemal complex (SC) is a proteinaceous scaffold required for synapsis and recombination between homologous chromosomes during meiosis. Although the SC has been linked to differences in genome-wide crossover rates, the genetic basis of standing variation in SC structure remains unknown. To investigate the possibility that recombination evo...
Despite being linked to the fundamental processes of chromosome segregation and offspring diversification, meiotic recombination rates vary within and between species. Recent years have seen progress in quantifying recombination rate evolution across multiple temporal and genomic scales. Nevertheless, the level of variation in recombination rate wi...
Since their arrival approximately 200 years ago, the house mice (Mus musculus) on Gough Island (GI) rapidly increased in size to become the largest wild house mice on record. Along with this extreme increase in body size, GI mice adopted a predatory diet, consuming significant quantities of seabird chicks and eggs. We studied this natural experimen...
A recent article reassessing the Neutral Theory of Molecular Evolution claims that it is no longer as important as is widely believed (Kern & Hahn 2018). The authors argue that “the neutral theory was supported by unreliable theoretical and empirical evidence from the beginning, and that in light of modern, genome‐scale data, we can firmly reject i...
Hybrids between new species are often sterile. To understand the causes of this reproductive barrier, Schwahn et al. examined testis histology in a large number of hybrids between two nascent species of house mice...
Hybrid sterility is a common form of reproductive isolation between nascent species. Although hybrid sterility is routinely documente...
The initial drivers of reproductive isolation between species are poorly characterized. In cases where partial reproductive isolation exists, genomic patterns of variation in hybrid zones may provide clues about the barriers to gene flow which arose first during the early stages of speciation. Purifying selection against incompatible substitutions...
Sex chromosomes are peculiar. In contrast to their autosomal counterparts, sex chromosomes are inherited differently in females and males, can harbor distinct sets of genes with unusual expression profiles, often experience reduced recombination, and may degenerate relatively quickly over evolutionary time. These characteristics and others have man...
Genomes sampled from hybrid zones between nascent species provide important clues into the speciation process. With advances in genome sequencing and single nucleotide polymorphism (SNP) genotyping, it is now feasible to measure variation in gene flow with high genomic resolution. This progress motivates the development of conceptual and analytical...
Meiotic recombination is necessary for successful gametogenesis in most sexually reproducing organisms and is a fundamental genomic parameter, influencing the efficacy of selection and the fate of new mutations. The molecular and evolutionary functions of recombination should impose strong selective constraints on the range of recombination rates....
In some species, meiotic recombination is concentrated in small genomic regions. These "recombination hotspots" leave signatures in fine-scale patterns of linkage disequilibrium, raising the prospect that the genomic landscape of hotspots can be characterized from sequence variation. This approach has led to the inference that hotspots evolve rapid...
Recombination rate is a heritable quantitative trait that evolves despite the fundamentally conserved role that recombination plays in meiosis. Differences in recombination rate can alter the landscape of the genome and the genetic diversity of populations. Yet our understanding of the genetic basis of recombination rate evolution in nature remains...
Organisms on islands often undergo rapid morphological evolution, providing a platform for understanding mechanisms of phenotypic change. Many examples of evolution on islands involve the vertebrate skeleton. Although the genetic basis of skeletal variation has been studied in laboratory strains, especially in the house mouse Mus musculus domesticu...
Recombination rate is a heritable trait that varies among individuals. Despite the major impact of recombination rate on patterns of genetic diversity and the efficacy of selection, natural variation in this phenotype remains poorly characterized. We present a comparison of genetic maps, sampling 1,212 meioses, from a unique population of wild hous...
Hybridization among diverging lineages is common in nature. Genomic data provide a special opportunity to characterize the history of hybridization and the genetic basis of speciation. We review existing methods and empirical studies to identify recent advances in the genomics of hybridization, as well as issues that need to be addressed. Notable p...
Genetic background effects have long been recognized and, in some cases studied, but they are often viewed as a nuisance by molecular biologists. We suggest that genetic variation currently represents a critical frontier for molecular studies. Human genetics has seen a surge of interest in genetic variation and its contributions to disease, but ins...
Genome-wide scans for natural selection (GWSS) have become increasingly common over the last fifteen years due to increased availability of genome-scale genetic data. Here, we report a representative survey of GWSS from 1999 to present and find that: (1) between 1999-2009, 37 of 50 (74%) GWSS focused on human while from 2010-present only 38 of 84 (...
Hybrids between species are often sterile or inviable. This form of reproductive isolation is thought to evolve via the accumulation of mutations that interact to reduce fitness when combined in hybrids. Mathematical formulations of this "Dobzhansky-Muller model" predict an accelerating buildup of hybrid incompatibilities with divergence time (the...
Organisms on islands provide a revealing window into the process of adaptation. Populations that colonize islands often evolve substantial differences in body size from their mainland relatives. Although the ecological drivers of this phenomenon have received considerable attention, its genetic basis remains poorly understood. We use house mice (su...
The genome-wide scan for selection is an important method for identifying loci involved in adaptive evolution. However, theory that underlies standard scans for selection assumes a simple mutation model. In particular, recurrent mutation of the selective target is not considered. Although this assumption is reasonable for single nucleotide variants...
Long dinucleotide repeats found in exons present a substantial mutational hazard: mutations at these loci occur often and generate frameshifts. Here, we provide clear and compelling evidence that exonic dinucleotides experience strong selective constraint. In humans, only 18 exonic dinucleotides have repeat lengths greater than six, which contrasts...
Adaptation requires genetic variation. A complete understanding of this key evolutionary process includes identification of the mutations that confer adaptive change. High-resolution genetic dissection of particular adaptive phenotypes can pinpoint these mutations, but this is a challenging task and the resulting conclusions are restricted to the t...
Island populations provide natural laboratories for studying key contributors to evolutionary change, including natural selection, population size, and the colonization of new environments. The demographic histories of island populations can be reconstructed from patterns of genetic diversity. House mice (Mus musculus) inhabit islands throughout th...
Hybrid dysfunction, a common feature of reproductive barriers between species, is often caused by negative epistasis between loci ("Dobzhansky-Muller incompatibilities"). The nature and complexity of hybrid incompatibilities remain poorly understood because identifying interacting loci that affect complex phenotypes is difficult. With subspecies in...
The Dobzhansky-Muller model of speciation posits that defects in hybrids between species are the result of negative epistatic interactions between alleles that arose in independent genetic backgrounds. Tests of one important prediction from this model, that incompatibilities "snowball," have relied on comparisons of the number of incompatibilities...
The European Journal of Human Genetics is the official Journal of the European Society of Human Genetics, publishing high-quality, original research papers, short reports, News and Commentary articles and reviews in the rapidly expanding field of human genetics and genomics.
Population genetics theory supplies powerful predictions about how natural selection interacts with genetic linkage to sculpt the genomic landscape of nucleotide polymorphism. Both the spread of beneficial mutations and the removal of deleterious mutations act to depress polymorphism levels, especially in low-recombination regions. However, empiric...
Abstract The Dobzhansky-Muller model of speciation posits that defects in hybrids between species are the result of negative epistatic interactions between alleles that arose in independent genetic backgrounds. Tests of one important prediction from this model, that ...
We use genotype data from the Marshfield Clinical Research Foundation Personalized Medicine Research Project to investigate genetic similarity and divergence between Europeans and the sampled population of European Americans in Central Wisconsin, USA. To infer recent genetic ancestry of the sampled Wisconsinites, we train support vector machines (S...
The ability to survey polymorphism on a genomic scale has enabled genome-wide scans for the targets of natural selection. Theory that connects patterns of genetic variation to evidence of natural selection most often assumes a diallelic locus and no recurrent mutation. Although these assumptions are suitable to selection that targets single nucleot...
The pseudoautosomal region (PAR) is essential for the accurate pairing and segregation of the X and Y chromosomes during meiosis. Despite its functional significance, the PAR shows substantial evolutionary divergence in structure and sequence between mammalian species. An instructive example of PAR evolution is the house mouse Mus musculus domestic...
Despite advances in genetic mapping of quantitative traits and in phylogenetic comparative approaches, these two perspectives are rarely combined. The joint consideration of multiple crosses among related taxa (whether species or strains) not only allows more precise mapping of the genetic loci (called quantitative trait loci, QTL) that contribute...
Comparative genetic mapping provides insights into the evolution of the reproductive barriers that separate closely related species. This approach has been used to document the accumulation of reproductive incompatibilities over time, but has only been applied to a few taxa. House mice offer a powerful system to reconstruct the evolution of reprodu...
Recently diverged taxa may continue to exchange genes. A number of models of speciation with gene flow propose that the frequency of gene exchange will be lower in genomic regions of low recombination and that these regions will therefore be more differentiated. However, several population-genetic models that focus on selection at linked sites also...
We report genome sequences of 17 inbred strains of laboratory mice and identify almost ten times more variants than previously known. We use these genomes to explore the phylogenetic history of the laboratory mouse and to examine the functional consequences of allele-specific variation on transcript abundance, revealing that at least 12% of transcr...
GenBank staff is unable to verify sequence and/or annotation provided by the submitter.
Reproductive isolation between species is often caused by deleterious interactions among loci in hybrids. Finding the genes involved in these incompatibilities provides insight into the mechanisms of speciation. With recently diverged subspecies, house mice provide a powerful system for understanding the genetics of reproductive isolation early in...
Relative mRNA transcript abundance for candidate genes within 1.5 LOD units of the X chromosome QTL peak at 33 cM. Expression levels were assayed via real-time quantitative PCR and standardized to levels of β-actin transcript abundance. Expression levels were compared between (A) 4 high versus 4 low mean MLH1 count F2s, (B) inbred CAST versus PWD s...
The rate of meiotic recombination varies markedly between species and among individuals. Classical genetic experiments demonstrated a heritable component to population variation in recombination rate, and specific sequence variants that contribute to recombination rate differences between individuals have recently been identified. Despite these adv...
Although growing numbers of single nucleotide polymorphisms (SNPs) and microsatellites (short tandem repeat polymorphisms or STRPs) are used to infer population structure, their relative properties in this context remain poorly understood. SNPs and STRPs mutate differently, suggesting multi-locus genotypes at these loci might differ in ability to d...
Rapid advances in DNA sequencing and genotyping technologies are beginning to reveal the scope and pattern of human genomic variation. Although single nucleotide polymorphisms (SNPs) have been intensively studied, the extent and form of variation at other types of molecular variants remain poorly understood. Polymorphism at the most variable loci i...
Theoretical work focused on microsatellite variation has produced a number of important results, including the expected distribution of repeat sizes and the expected squared difference in repeat size between two randomly selected samples. However, closed-form expressions for the sampling distribution and frequency spectrum of microsatellite variati...
Although very closely related species can differ in their fine-scale patterns of recombination hotspots, variation in the average genomic recombination rate among recently diverged taxa has rarely been surveyed. We measured recombination rates in eight species that collectively represent several temporal scales of divergence within a single rodent...
The rate of recombination is a key genomic parameter that displays considerable variation among taxa. Species comparisons have demonstrated that the rate of evolution in recombination rate is strongly dependent on the physical scale of measurement. Individual recombination hotspots are poorly conserved among closely related taxa, whereas genomic-sc...
Hybrids between species provide information about the evolutionary processes involved in divergence. In addition to creating hybrids in the laboratory, biologists can take advantage of natural hybrid zones to understand the factors that shape gene flow between divergent lineages. In the early stages of speciation, most regions of the genome continu...
ABSTRACT : The high genomic density of the single-nucleotide polymorphism (SNP) sets that are typically surveyed in genome-wide association studies (GWAS) now allows the application of haplotype-based methods. Although the choice of haplotype-based vs. individual-SNP approaches is expected to affect the results of association studies, few empirical...
We have leveraged the reference sequence of a boxer to construct the first complete linkage map for the domestic dog. The new map improves access to the dog's unique biology, from human disease counterparts to fascinating evolutionary adaptations. The map was constructed with approximately 3000 microsatellite markers developed from the reference se...
Recombination rate within large and small loci. The 2.5% largest loci (blue) have a significantly lower recombination rate as compared to the 2.5% smallest loci (red) (p<0.00001), suggesting the minimum description length principle partitioned the genome in a biologically informative manner.
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Fine-scale phylogenetic discordance. The posterior probability of each topology is mapped throughout the genome to characterize fine-scale patterns of discordance. Position along the chromosomes is indicated on the x-axis (Mb) and the posterior probability of each topology is on the y-axis. Colors correspond to the three topologies.
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Genomic locations and posterior probabilities of the 14,081 loci (computed with a prior probability of gene tree concordance set at α = 1).
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Varied starting interval sizes for the minimum description length partitioning. A range of SNP intervals was applied to the partitioning of chromosomes 18 and 19. There are no significant differences in the concordance factors between the first three starting intervals: 25, 50, or 100 SNPs. Colors correspond to the three topologies. Error bars are...
Distribution of locus sizes. Using a minimum description length principle, the genome was partitioned into 14,081 loci with a median size of 98,238 bp (SD 312,637 bp) and a maximum locus size of 7.21 Mb. Loci greater than 1 Mb in size are not shown.
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Median locus size for each of the three topologies. Median locus size for each topology parallels the rank order of the concordance factors on both the autosomes and the X chromosome. Colors correspond to the three topologies.
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Maximum and minimum penalties against breakpoints for the minimum description length partitioning. Both the maximum (3) and minimum (0.9039) penalties were applied to the partitioning of chromosomes 18, 19, and X. Using a minimum penalty roughly doubles the number of loci on each chromosome, but the chromosome-wide concordance factors remain simila...
Phylogenetic discordance and long-branch attraction. The rat sequence was randomly shuffled to erase any phylogenetic signal between rat and house mice on chromosomes 18 and 19. Without the sequence shuffled (A), topologies significantly deviate from a 1/3, 1/3, 1/3 ratio. With the rat sequence shuffled (B), the topologies converge to a 1/3, 1/3, 1...
Single locus posterior probabilities. 84.9% of loci are supported by a high posterior probability (>0.9) from the single-locus Bayesian phylogenetic analyses, suggesting the minimum description length principle partitioned the genome in a phylogenetically informative manner.
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Population genetic theory predicts discordance in the true phylogeny of different genomic regions when studying recently diverged species. Despite this expectation, genome-wide discordance in young species groups has rarely been statistically quantified. The house mouse subspecies group provides a model system for examining phylogenetic discordance...
Despite rapid advances in the complementary fields of speciation genetics and molecular phylogenetics, little attention has been devoted to understanding how genetic changes associated with reproductive isolation accumulate across clades of species. We argue that comparative analyses of reproductive isolation QTL (quantitative trait loci) can gener...
We used a large panel of pedigreed, genetically admixed house mice to study patterns of recombination rate variation in a leading mammalian model system. We found considerable inter-individual differences in genomic recombination rates and documented a significant heritable component to this variation. These findings point to clear variation in rec...
Patterns of population structure provide insights into evolutionary processes and help identify groups of individuals for genotype-phenotype association studies. With increasing availability of polymorphic molecular markers across genomes, the examination of population structure using large numbers of unlinked loci has become a common practice in e...
Hybridization between genetically divergent populations is common in nature. By comparing the rate of gene flow throughout the genome, loci that impede genetic mixing, and therefore underlie reproductive isolation, can be identified, providing key insights into the process of speciation. In a previous issue of Molecular Ecology, Geraldes et al. (20...
The house mouse is one of the most successful mammals and the premier research animal in mammalian biology. The classical inbred strains of house mice have been artificially modified to facilitate identification of the genetic factors underlying phenotypic variation among these strains. Despite their widespread use in basic and biomedical research,...
Patterns of linkage disequilibrium (LD) reveal the action of evolutionary processes and provide crucial information for association mapping of disease genes. Although recent studies have described the landscape of LD among single nucleotide polymorphisms (SNPs) from across the human genome, associations involving other classes of molecular variatio...