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Searle, J. B.

Publications and source records attributed to Searle, J. B..

8 recordsLinked to original sources

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↗

The genomic landscape, causes, and consequences of extensive phylogenomic discordance in Old World mice and rats

A species tree is a central concept in evolutionary biology whereby a single branching phylogeny reflects relationships among species. However, the phylogenies of different genomic regions often differ from the species tree. Although tree discordance is often widespread in phylogenomic studies, we still lack a clear understanding of how variation in phylogenetic patterns is shaped by genome biology or the extent to which discordance may compromise comparative studies. We characterized patterns of phylogenomic discordance across the murine rodents (Old World mice and rats) - a large and ecologically diverse group that gave rise to the mouse and rat model systems. Combining new linked-read genome assemblies for seven murine species with eleven published rodent genomes, we first used ultra-conserved elements (UCEs) to infer a robust species tree. We then used whole genomes to examine finer-scale patterns of discordance and found that phylogenies built from proximate chromosomal regions had similar phylogenies. However, there was no relationship between tree similarity and local recombination rates in house mice, suggesting that genetic linkage influences phylogenetic patterns over deeper timescales. This signal may be independent of contemporary recombination landscapes. We also detected a strong influence of linked selection whereby purifying selection at UCEs led to less discordance, while genes experiencing positive selection showed more discordant and variable phylogenetic signals. Finally, we show that assuming a single species tree can result in high error rates when testing for positive selection under different models. Collectively, our results highlight the complex relationship between phylogenetic inference and genome biology and underscore how failure to account for this complexity can mislead comparative genomic studies.

evolutionary biology↗

Resource competition drives an invasion-replacement event among shrew species on an island

O_LIInvasive mammals are responsible for the majority of native species extinctions on islands. While most of these extinction events will be due to novel interactions between species (e.g. exotic predators and naive prey), it is more unusual to find incidences where a newly invasive species causes the decline/extinction of a native species on an island when they normally coexist elsewhere in their overlapping mainland ranges. C_LIO_LIWe investigated if resource competition between two insectivorous small mammals was playing a significant role in the rapid replacement of the native pygmy shrew (Sorex minutus) in the presence of the recently invading greater white-toothed shrew (Crocidura russula) on the island of Ireland. C_LIO_LIWe used DNA metabarcoding of gut contents from >300 individuals of both species to determine each species diet and measured the size of individuals (weight and length) during different stages of the invasion in Ireland (before, during and after the species come into contact with one another) and on a French island where both species have long coexisted (acting as a natural control site). Dietary composition, niche width and overlap and size were compared in these different stages. C_LIO_LIThe size of the invasive C. russula and composition of its diet changes between when it first invades an area and after it becomes established. Individuals are larger and they consume larger invertebrates at the invasion front, before switching towards the smaller prey taxa that are more essential for the survival of the native species after establishment. As a result, the level of interspecific dietary overlap increases from between 11-14% when they first come into contact with each other to between 39-46% after the invasion. C_LIO_LIHere we show that an invasive species can quickly alter its dietary niche in a new environment, leading to negative impacts that were not previously predicted based on the coexistence of these species in other parts of their mainland ranges. As well as causing the replacement of a native small mammal, the invasive shrew may be rapidly exhausting local resources of larger invertebrate species. These subsequent changes in terrestrial invertebrate communities could have severe impacts further downstream on ecosystem functioning and services. C_LI

ecology↗

Population structure and inbreeding in wild house mice (Mus musculus) at different geographic scales

House mice (Mus musculus) have spread globally as a result of their commensal relationship with humans. In the form of laboratory strains, both inbred and outbred, they are also among the most widely-used model organisms in biomedical research. Although the general outlines of house mouse dispersal and population structure are well known, details have been obscured by either limited sample size or small numbers of markers. Here we examine ancestry, population structure and inbreeding using SNP microarray genotypes in a cohort of 814 wild mice spanning five continents and all major subspecies of Mus, with a focus on M. m. domesticus. We find that the major axis of genetic variation in M. m. domesticus is a south-to-north gradient within Europe and the Mediterranean. The dominant ancestry component in North America, Australia, New Zealand and various small offshore islands is of northern European origin. Next we show that inbreeding is surprisingly pervasive and highly variable, even between nearby populations. By inspecting the length distribution of homozygous segments in individual genomes, we find that inbreeding in commensal populations is mostly due to consanguinity. Our results offer new insight into the natural history of an important model organism for medicine and evolutionary biology.

genetics↗

Consequences of coupled barriers to gene flow for the build-up of genomic differentiation

Theory predicts that when different barriers to gene flow become coincident, their joint effects enhance reproductive isolation and genomic divergence beyond their individual effects, but empirical tests of this coupling hypothesis are rare. Here, we analyze patterns of gene exchange among populations of European corn borer moths that vary in the number of acting barriers, allowing for comparisons of genomic variation when barrier traits or loci are in coincident or independent states. We find that divergence is mainly restricted to barrier loci when populations differ by a single barrier, whereas the coincidence of temporal and behavioral barriers is associated with divergence of two chromosomes harboring barrier loci. Furthermore, differentiation at temporal barrier loci increases in the presence of behavioral divergence and differentiation at behavioral barrier loci increases in the presence of temporal divergence. Our results demonstrate how the joint action of coincident barrier effects leads to levels of genomic differentiation that far exceed those of single barriers acting alone, consistent with theory arguing that coupling allows indirect selection to combine with direct selection and thereby lead to a stronger overall barrier to gene flow. Thus, the state of barriers - independent or coupled - strongly influences the accumulation of genomic differentiation.

evolutionary biology↗

Phylogeographic structure of the pygmy shrew: revisiting the roles of southern and northern refugia in Europe.

Southern and northern glacial refugia are considered paradigms that explain the complex phylogeographic patterns and processes of European biota. Although the Eurasian pygmy shrew Sorex minutus Linnaeus, 1766 (Eulipotyphla, Soricidae) has been used a model species to study geographic isolation and genetic diversification in Mediterranean peninsulas in the Last Glacial Maximum (LGM), and post-glacial population expansion from cryptic northern glacial refugia in Western and Central Europe, there has been incomplete knowledge about the phylogeographic structure, genetic differentiation and demographic history within these regions. Here, we provide a revisited statistical phylogeographic study of S. minutus with greater sampling coverage in terms of numbers of individuals and geographic range, making it the most comprehensive investigation of this species to date. The results showed support for genetically distinct and diverse phylogeographic groups consistent with southern and northern glacial refugia, as expected from previous studies, but also identified geographical barriers concordant with glaciated mountain ranges during the LGM, early diversification events dated between the Upper Pleistocene and Lower Holocene for the main phylogeographic groups, and recent (post-LGM) patterns of demographic expansions. The results have implications for the conservation of intraspecific diversity and the preservation of the evolutionary potential of S. minutus.

evolutionary biology↗

Long-term reciprocal gene flow in wild and domestic geese reveals complex domestication history

Hybridization has frequently been observed between wild and domestic species and can substantially impact genetic diversity of both counterparts. Geese show some of the highest levels of interspecific hybridization across all bird orders, and two of the goose species in genus Anser have been domesticated providing excellent opportunity for joint study of domestication and hybridization. Until now, knowledge on the details of the goose domestication process has come from archaeological findings and historical writings supplemented with few studies based on mitochondrial DNA. Here, we used genome-wide markers to make the first genome-based inference of the timing of European goose domestication. We also analyzed the impact of hybridization on the genome-wide genetic variation in current populations of the European domestic goose and its wild progenitor: the greylag goose (Anser anser). Our dataset consisted of 58 wild greylags sampled around Eurasia and 75 domestic geese representing 14 breeds genotyped for 33,527 single nucleotide polymorphisms. Demographic reconstruction and clustering analysis suggested that divergence between wild and domestic geese around 5,300 generations ago was followed by long-term genetic exchange, and that greylag populations have 3.2-58.0% admixture proportions with domestic geese, with distinct geographic patterns. Surprisingly, many modern European breeds share considerable (> 10%) ancestry with Chinese domestic geese that is derived from the swan goose Anser cygnoid. We show that domestication process can progress despite continued and pervasive gene flow from the wild form.\n\nSignificance StatementReproductive isolation between conspecific wild and domestic populations is a cornerstone of the domestication process, yet gene flow between such wild and domestic populations has been frequently documented. European domestic geese and their wild progenitor (greylags) co-occur and can hybridize and we show that they represent a particularly persuasive case where wild and domestic populations are not isolated gene pools. Our study makes a first genome-based estimate of goose domestication, which up to now has mostly relied on archaeological findings and historical writings. We show ongoing gene flow between greylags and European domestic geese following domestication, but we also observe a surprisingly large contribution of Chinese domestic geese (a separate species) to the genetic make-up of European domestic geese.

evolutionary biology↗

Genetic characterization of invasive house mouse populations on small islands

House mice (Mus musculus) have dispersed to nearly every major landmass around the globe as a result of human activity. They are a highly successful invasive species, but their presence can be devastating for native ecosystems. This is particularly true on small offshore islands where mouse populations may grow unchecked by predators. Here we use genome-wide SNP genotypes to examine ancestry and population structure on two islands of ecological interest - Southeast Farallon Island, near San Francisco, CA; and Floreana Island in the Galapagos - in the context of a total cohort of 520 mice with diverse geographic origins, as a first step towards genetically-based eradication campaigns. We show that Farallon and Floreana mice, like those from previously-studied islands in both the Atlantic and Pacific Oceans, are of admixed European ancestry. We find that these populations are on average more inbred than mainland ones and passed through a strong colonization bottleneck with little subsequent genetic exchange. Finally we show that rodenticide resistance alleles present in parts of Europe are absent from all island populations studied. Our results add nuance to previous studies of island populations based on mitochondrial sequences or small numbers of microsatellites and will be useful for future eradication and monitoring efforts.

genetics↗