Genetic admixture drives climate adaptation in the bank vole.

Genetic admixture introduces new variants at relatively high frequencies, potentially aiding rapid responses to environmental changes. Here, we evaluate its role in adaptive variation related to climatic conditions in bank voles (Clethrionomys glareolus) in Britain, using whole-genome data. Our results reveal loci showing excess ancestry from one of the two postglacial colonist populations inconsistent with overall admixture patterns. Notably, loci associated with climate adaptation exhibit disproportionate amounts of excess ancestry, highlighting the impact of admixture between colonist populations on local adaptation. The results suggest strong and localized selection on climate-adaptive loci, as indicated by steep clines and/or shifted cline centres, during population replacement. A subset, including a haemoglobin gene, is associated with oxidative stress responses, underscoring a role of oxidative stress in local adaptation. Our study highlights the important contribution of admixture during secondary contact between populations from distinct climatic refugia enriching adaptive diversity. Understanding these dynamics is crucial for predicting future adaptive capacity to anthropogenic climate change.

Structural Variants and Speciation: Multiple Processes at Play.

Research on the genomic architecture of speciation has increasingly revealed the importance of structural variants (SVs) that affect the presence, abundance, position, and/or direction of a nucleotide sequence. SVs include large chromosomal rearrangements such as fusion/fissions and inversions and translocations, as well as smaller variants such as duplications, insertions, and deletions (CNVs). Although we have ample evidence that SVs play a key role in speciation, the underlying mechanisms differ depending on the type and length of the SV, as well as the ecological, demographic, and historical context. We review predictions and empirical evidence for classic processes such as underdominance due to meiotic aberrations and the coupling effect of recombination suppression before exploring how recent sequencing methodologies illuminate the prevalence and diversity of SVs. We discuss specific properties of SVs and their impact throughout the genome, highlighting that multiple processes are at play, and possibly interacting, in the relationship between SVs and speciation.

Local adaptation and future climate vulnerability in a wild rodent.

As climate change continues, species pushed outside their physiological tolerance limits must adapt or face extinction. When change is rapid, adaptation will largely harness ancestral variation, making the availability and characteristics of that variation of critical importance. Here, we used whole-genome sequencing and genetic-environment association analyses to identify adaptive variation and its significance in the context of future climates in a small Palearctic mammal, the bank vole (Clethrionomys glareolus). We found that peripheral populations of bank vole in Britain are already at the extreme bounds of potential genetic adaptation and may require an influx of adaptive variation in order to respond. Analyses of adaptive loci suggest regional differences in climate variables select for variants that influence patterns of population adaptive resilience, including genes associated with antioxidant defense, and support a pattern of thermal/hypoxic cross-adaptation. Our findings indicate that understanding potential shifts in genomic composition in response to climate change may be key to predicting species' fate under future climates.

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 Origins and Patterns of Diversification in Animal Brood Parasitism.

AbstractBrood parasitism involves the exploitation of host parental care rather than the extraction of resources directly from hosts. We identify defining characteristics of this strategy and consider its position along continua with adjacent behaviors but focus on canonical brood parasites, where parasitism is obligate and hosts are noneusocial (thereby distinguishing from social parasitism). A systematic literature survey revealed 59 independently derived brood parasitic lineages with most origins (49) in insects, particularly among bees and wasps, and other origins in birds (seven) and fish (three). Insects account for more than 98% of brood parasitic species, with much of that diversity reflecting ancient (≥100-million-year-old) brood parasitic lineages. Brood parasites usually, but not always, evolve from forms that show parental care. In insects, brood parasitism often first evolves through exploitation of a closely related species, following Emery's rule, but this is less typical in birds, which we discuss. We conducted lineage-level comparisons between brood parasitic clades and their sister groups, finding mixed results but an overall neutral to negative effect of brood parasitism on species richness and diversification. Our review of brood parasites reveals many unanswered questions requiring new research, including further modeling of the coevolutionary dynamics of brood parasites and their hosts.

The Impact of Chromosomal Rearrangements in Speciation: From Micro- to Macroevolution.

Chromosomal rearrangements (CRs) have been known since almost the beginning of genetics. While an important role for CRs in speciation has been suggested, evidence primarily stems from theoretical and empirical studies focusing on the microevolutionary level (i.e., on taxon pairs where speciation is often incomplete). Although the role of CRs in eukaryotic speciation at a macroevolutionary level has been supported by associations between species diversity and rates of evolution of CRs across phylogenies, these findings are limited to a restricted range of CRs and taxa. Now that more broadly applicable and precise CR detection approaches have become available, we address the challenges in filling some of the conceptual and empirical gaps between micro- and macroevolutionary studies on the role of CRs in speciation. We synthesize what is known about the macroevolutionary impact of CRs and suggest new research avenues to overcome the pitfalls of previous studies to gain a more comprehensive understanding of the evolutionary significance of CRs in speciation across the tree of life.

Seasonal Adaptation: Geographic Photoperiod-Temperature Patterns Explain Genetic Variation in the Common Vole Tsh Receptor.

The vertebrate photoperiodic neuroendocrine system uses the photoperiod as a proxy to time the annual rhythms in reproduction. The thyrotropin receptor (TSHR) is a key protein in the mammalian seasonal reproduction pathway. Its abundance and function can tune sensitivity to the photoperiod. To investigate seasonal adaptation in mammals, the hinge region and the first part of the transmembrane domain of the Tshr gene were sequenced for 278 common vole (Microtus arvalis) specimens from 15 localities in Western Europe and 28 localities in Eastern Europe. Forty-nine single nucleotide polymorphisms (SNPs; twenty-two intronic and twenty-seven exonic) were found, with a weak or lack of correlation with pairwise geographical distance, latitude, longitude, and altitude. By applying a temperature threshold to the local photoperiod-temperature ellipsoid, we obtained a predicted critical photoperiod (pCPP) as a proxy for the spring onset of local primary food production (grass). The obtained pCPP explains the distribution of the genetic variation in Tshr in Western Europe through highly significant correlations with five intronic and seven exonic SNPs. The relationship between pCPP and SNPs was lacking in Eastern Europe. Thus, Tshr, which plays a pivotal role in the sensitivity of the mammalian photoperiodic neuroendocrine system, was targeted by natural selection in Western European vole populations, resulting in the optimized timing of seasonal reproduction.

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

Invasive 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. We 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. We used DNA metabarcoding of gut contents from >300 individuals of both species to determine each species' diet and measured the body size (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 body size were compared in these different stages. The body size of the invasive C. russula and composition of its diet changes between when it first invades an area and after it becomes established. During the initial stages of the invasion, individual shrews are larger and consume larger sized invertebrate prey species. During later stages of the invasion, C. russula switches to consuming smaller prey taxa that are more essential for the native species. As a result, the level of interspecific dietary overlap increases from between 11% and 14% when they first come into contact with each other to between 39% and 46% after the invasion. Here we show that an invasive species can quickly alter its dietary niche in a new environment, ultimately causing the replacement of a native species. In addition, the invasive shrew could also be potentially 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.

Tracking Chromosomal Origins in the Northern Italy System of Metacentric Races of the House Mouse.

The Western European house mouse is chromosomally diverse, with diploid karyotypes ranging from the standard 40 telocentric chromosomes down to 22 chromosomes. Karyotypes are modified through Robertsonian (Rb) fusion of 2 telocentrics into a single metacentric, occurring repeatedly with fixation, and whole-arm reciprocal translocations (WARTs) generating additional novel karyotypes. Over 100 metacentric populations (chromosomal races) have been identified, geographically clustered into "systems." Chromosomal races within systems often hybridise, and new races may emerge through this hybridisation ("zonal raciation"). We wished to determine the degree to which chromosomal races in a system have evolved independently or share common ancestry. Recombination between chromosomes from hybridising chromosomal races can erase the signals associated with a particular metacentric of interest, making inferences challenging. However, reduced recombination near the centromeres of chromosomal race-specific metacentrics makes centromere-adjacent markers ideal for solving this problem. For the Northern Italy System (NIS), we used microsatellite markers near the centromere to test previous hypotheses about evolutionary relationships of 5 chromosomal races. We chose markers from chromosomes 1, 3, 4, and 6, all of which comprise one arm of a metacentric in at least 2 of these NIS metacentric populations. We used estimates of FST and RST, as well as principal components analyses and neighbour-joining phylogenetic analyses, to infer evolutionary relationships between these 5 chromosomal races and neighbouring mice with the standard karyotype. We showed that the metacentric populations form a single grouping distinct from the standard populations, consistent with their common origin and consistent with a parsimonious sequence of chromosomal rearrangements to explain the relationship of the chromosomal races. That origin and evolution of the chromosomal races in the system would have involved Rb fusions, explaining the occurrence of chromosomal races with diploid numbers as low as 22. However, WARTs and zonal raciation have also been inferred, and the rare occurrence of chromosome 1 in different metacentrics in closely related chromosomal races is almost certainly explained by a WART. Our results with centromeric microsatellites are consistent with the above scenarios, illustrating, once again, the value of markers in the centromeric region to test evolutionary hypotheses in house mouse chromosomal systems.

Characterising Mitochondrial Capture in an Iberian Shrew.

Mitochondrial introgression raises questions of biogeography and of the extent of reproductive isolation and natural selection. Previous phylogenetic work on the Sorex araneus complex revealed apparent mitonuclear discordance in Iberian shrews, indicating past hybridisation of Sorex granarius and the Carlit chromosomal race of S. araneus, enabling introgression of the S. araneus mitochondrial genome into S. granarius. To further study this, we genetically typed 61 Sorex araneus/coronatus/granarius from localities in Portugal, Spain, France, and Andorra at mitochondrial, autosomal, and sex-linked loci and combined our data with the previously published sequences. Our data are consistent with earlier data indicating that S. coronatus and S. granarius are the most closely related of the three species, confirming that S. granarius from the Central System mountain range in Spain captured the mitochondrial genome from a population of S. araneus. This mitochondrial capture event can be explained by invoking a biogeographical scenario whereby S. araneus was in contact with S. granarius during the Younger Dryas in central Iberia, despite the two species currently having disjunct distributions. We discuss whether selection favoured S. granarius with an introgressed mitochondrial genome. Our data also suggest recent hybridisation and introgression between S. coronatus and S. granarius, as well as between S. araneus and S. coronatus.

Genic distribution modelling predicts adaptation of the bank vole to climate change.

The most likely pathway for many species to survive future climate change is by pre-existing trait variation providing a fitness advantage under the new climate. Here we evaluate the potential role of haemoglobin (Hb) variation in bank voles under future climate change. We model gene-climate relationships for two functionally distinct Hb types, HbS and HbF, which have a north-south distribution in Britain presenting an unusually tractable system linking genetic variation in physiology to geographical and temporal variation in climate. Projections to future climatic conditions suggest a change in relative climatic suitability that would result in HbS being displaced by HbF in northern Britain. This would facilitate local adaptation to future climate-without Hb displacement, populations in northern Britain would likely be suboptimally adapted because their Hb would not match local climatic conditions. Our study shows how pre-existing physiological differences can influence the adaptive capacity of species to climate change.

The complete mitochondrial genome of Talpa martinorum (Mammalia: Talpidae), a mole species endemic to Thrace: genome content and phylogenetic considerations.

The complete mitogenome sequence of Talpa martinorum, a recently described Balkan endemic mole, was assembled from next generation sequence data. The mitogenome is similar to that of the three other Talpa species sequenced to date, being 16,835 bp in length, and containing 13 protein-coding genes, two ribosomal RNA genes, 22 transfer RNA genes, an origin of L-strand replication, and a control region or D-loop. Compared to other Talpa mitogenomes sequenced to date, that of T. martinorum differs in the length of D-loop and stop codon usage. TAG and T-- are the stop codons for the ND1 and ATP8 genes, respectively, in T. martinorum, whilst TAA acts as a stop codon for both ND1 and ATP8 in the other three Talpa species sequenced. Phylogeny reconstructions based on Maximum Likelihood and Bayesian inference analyses yielded phylogenies with similar topologies, demonstrating that T. martinorum nests within the western lineage of the genus, being closely related to T. aquitania and T. occidentalis.

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 are 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.

Genome of the bee Holcopasites calliopsidis-a species showing the common apid trait of brood parasitism.

Brood parasites represent a substantial but often poorly studied fraction of the wider diversity of bees. Brood parasitic bees complete their life cycles by infiltrating the nests of solitary host bees thereby enabling their offspring to exploit the food provisions intended for the host's offspring. Here, we present the draft assembly of the bee Holcopasites calliopsidis, the first brood parasitic species to be the subject of detailed genomic analysis. Consistent with previous findings on the genomic signatures of parasitism more broadly, we find that H. calliopsidis has the smallest genome currently known among bees (179 Mb). This small genome does not appear to be the result of purging of repetitive DNA, with some indications of novel repetitive elements which may show signs of recent expansion. Nor does H. calliopsidis demonstrate any apparent net loss of genic content in comparison with nonparasitic species, though many individual gene families do show significant contractions. Although the basis of the small genome size of this species remains unclear, the identification of over 12,000 putative genes-with functional annotation for nearly 10,000 of these-is an important step in investigating the genomic basis of brood parasitism and provides a valuable dataset to be compared against new genomes that remain to be sequenced.

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.

Genomic Analysis Reveals Subdivision of Black Rats (Rattus rattus) in India, Origin of the Worldwide Species Spread.

In contrast to the detailed and globally extensive studies on the spread of the commensal black rat, Rattus rattus, there has been relatively little work on the phylogeography of the species within India, from where this spread originated. Taking a genomic approach, we typed 27 R. rattus samples from Peninsular India using the genotyping-by-sequencing (GBS) method. Filtering and alignment of the FASTQ files yielded 1499 genome-wide SNPs. Phylogenomic tree reconstruction revealed a distinct subdivision in the R. rattus population, manifested as two clusters corresponding to the east and west coasts of India. We also identified signals of admixture between these two subpopulations, separated by an Fst of 0.20. This striking genomic difference between the east and west coast populations mirrors what has previously been described with mitochondrial DNA sequencing. It is notable that the west coast population of R. rattus has been spread globally, reflecting the origins of commensalism of the species in Western India and the subsequent transport by humans worldwide.

Genetic assessment reveals inbreeding, possible hybridization, and low levels of genetic structure in a declining goose population.

The population numbers of taiga bean goose (Anser fabalis fabalis) have halved during recent decades. Since this subspecies is hunted throughout most of its range, the decline is of management concern. Knowledge of the genetic population structure and diversity is important for guiding management and conservation efforts. Genetically unique subpopulations might be hunted to extinction if not managed separately, and any inbreeding depression or lack of genetic diversity may affect the ability to adapt to changing environments and increase extinction risk. We used microsatellite and mitochondrial DNA markers to study the genetic population structure and diversity among taiga bean geese breeding within the Central flyway management unit using non-invasively collected feathers. We found some genetic structuring with the maternally inherited mitochondrial DNA between four geographic regions (ɸ ST = 0.11-0.20) but none with the nuclear microsatellite markers (all pairwise F ST-values = 0.002-0.005). These results could be explained by female natal philopatry and male-biased dispersal, which completely homogenizes the nuclear genome. Therefore, the population could be managed as a single unit. Genetic diversity was still at a moderate level (average H E = 0.69) and there were no signs of past population size reductions, although significantly positive inbreeding coefficients in all sampling sites (F IS = 0.05-0.10) and high relatedness values (r = 0.60-0.86) between some individuals could indicate inbreeding. In addition, there was evidence of either incomplete lineage sorting or introgression from the pink-footed goose (Anser brachyrhynchus). The current population is not under threat by genetic impoverishment but monitoring in the future is desirable.

Phylogenetic relationships and the evolution of host preferences in the largest clade of brood parasitic bees (Apidae: Nomadinae).

Brood parasites (also known as cleptoparasites) represent a substantial fraction of global bee diversity. Rather than constructing their own nests, these species instead invade those of host bees to lay their eggs. Larvae then hatch and consume the food provisions intended for the host's offspring. While this life history strategy has evolved numerous times across the phylogeny of bees, the oldest and most speciose parasitic clade is the subfamily Nomadinae (Apidae). However, the phylogenetic relationships among brood parasitic apids both within and outside the Nomadinae have not been fully resolved. Here, we present new findings on the phylogeny of this diverse group of brood parasites based on ultraconserved element (UCE) sequence data and extensive taxon sampling with 114 nomadine species representing all tribes. We suggest a broader definition of the subfamily Nomadinae to describe a clade that includes almost all parasitic members of the family Apidae. The tribe Melectini forms the sister group to all other Nomadinae, while the remainder of the subfamily is composed of two sister clades: a "nomadine line" representing the former Nomadinae sensu stricto, and an "ericrocidine line" that unites several mostly Neotropical lineages. We find the tribe Osirini Handlirsch to be polyphyletic, and divide it into three lineages, including the newly described Parepeolini trib. nov. In addition to our taxonomic findings, we use our phylogeny to explore the evolution of different modes of parasitism, detecting two independent transitions from closed-cell to open-cell parasitism. Finally, we examine how nomadine host-parasite associations have evolved over time. In support of Emery's rule, which suggests close relationships between hosts and parasites, we confirm that the earliest nomadines were parasites of their close free-living relatives within the family Apidae, but that over time their host range broadened to include more distantly related hosts spanning the diversity of bees. This expanded breadth of host taxa may also be associated with the transition to open-cell parasitism.

A dynamic history of admixture from Mediterranean and Carpathian glacial refugia drives genomic diversity in the bank vole.

Understanding the historical contributions of differing glacial refugia is key to evaluating the roles of microevolutionary forces, such as isolation, introgression, and selection in shaping genomic diversity in present-day populations. In Europe, where both Mediterranean and extra-Mediterranean (e.g., Carpathian) refugia of the bank vole (Clethrionomys glareolus) have been identified, mtDNA indicates that extra-Mediterranean refugia were the main source of colonization across the species range, while Mediterranean peninsulas harbor isolated, endemic lineages. Here, we critically evaluate this hypothesis using previously generated genomic data (>6,000 SNPs) for over 800 voles, focusing on genomic contributions to bank voles in central Europe, a key geographic area in considering range-wide colonization. The results provide clear evidence that both extra-Mediterranean (Carpathian) and Mediterranean (Spanish, Calabrian, and Balkan) refugia contributed to the ancestry and genomic diversity of bank vole populations across Europe. Few strong barriers to dispersal and frequent admixture events in central Europe have led to a prominent mid-latitude peak in genomic diversity. Although the genomic contribution of the centrally located Carpathian refugium predominates, populations in different parts of Europe have admixed origins from Mediterranean (28%-47%) and the Carpathian (53%-72%) sources. We suggest that the admixture from Mediterranean refugia may have provisioned adaptive southern alleles to more northern populations, facilitating the end-glacial spread of the admixed populations and contributing to increased bank vole diversity in central Europe. This study adds critical details to the complex end-glacial colonization history of this well-studied organism and underscores the importance of genomic data in phylogeographic interpretation.