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Ritchie, M. G.

Publications and source records attributed to Ritchie, M. G..

At least 19 recordsLinked to original sources

Adaptive introgression improves heat-tolerance despite barriers to gene flow: a case study in Drosophila flavomontana and Drosophila montana

As global temperatures rise and heat waves become more frequent, populations must adapt rapidly to avoid local extinctions. Adaptive introgression allows species to quickly acquire adaptive genetic material from close relatives. However, certain genomic regions, containing barrier loci, may resist introgression. We experimentally tested whether strong heat stress selection can overcome such barriers and facilitate the transfer of adaptive alleles to improve heat tolerance. We also examined whether chromosomal inversions, which can tightly link adaptive and barrier loci through reduced recombination, promote or prevent introgression. We conducted a hybridize, evolve, and re-sequence experiment by crossing the heat-sensitive D. flavomontana with the more heat-tolerant D. montana, exposing heat-selection lines to transient heat for three generations while maintaining control lines. We also mapped long-term barriers to gene flow between natural populations using a demographically explicit genome scan. The heat-selection lines exhibited approximately twice the introgression and higher male fertility under heat stress compared to control lines and the heat-sensitive parental D. flavomontana. This introgression was primarily located in colinear autosomal regions and correlated with improved heat tolerance. Some introgression occurred also in inverted autosomal regions in the heat-selection lines but not in the control lines. The X chromosome, with three overlapping inversions, resisted introgression in both heat-selection and control lines, thereby maintaining a strong species barrier. Finally, genetic barriers in the control lines significantly overlapped with long-term barriers, but this overlap was less pronounced in the heat-selection lines. Our study demonstrates that strong selection can lead to adaptive introgression despite long-standing genetic barriers. These findings highlight that introgression can serve as a rapid source of adaptive genetic material under stressful thermal conditions, potentially mitigating climate-induced population extinctions.

evolutionary biology↗

A chromosomal inversion accumulates adaptive and barrier loci in a cold-adapted insect species

Chromosomal inversions can play a crucial role in population adaptation and divergence by reducing gene flow and preserving adaptive allelic combinations between populations with different arrangements. However, demonstrating this empirically is challenging due to numerous interacting processes with similar genomic signatures affecting inversion evolution. In this study, we characterized a large (9.5Mb) polymorphic inversion in the cold-adapted and widely distributed species, Drosophila montana, using long- and short-read sequencing across several populations. The origin of this inversion predates the divergence of North American (NA) and Fennoscandian (North European) populations, suggesting it emerged in the ancestral D. montana population in the Rocky Mountains of NA. Despite the species expansion across the northern hemisphere, this inversion has remained exclusive to the Rocky Mountains populations, where it is fixed in the southernmost high-elevation population and appears at lower frequencies in the more northern and lower-elevation populations. By independently mapping SNPs linked to climate adaptation and barriers to gene flow (barrier loci; identified through reduced migration rates), we found enrichment of both within the inversion, with barrier and adaptive regions partially overlapping. However, the inversion was not enriched for SNPs related to cold tolerance. These findings suggest that inversions may maintain associations between multiple adaptive and barrier loci, effectively coupling them, and that locally adaptive regions may act as barriers to gene flow. Our study provides empirical evidence that inversions can contribute to population adaptation and divergence by reducing gene flow, maintaining adaptive allelic combinations, and facilitating the coupling of different barriers to gene flow. SignificanceChromosomal inversions, genomic rearrangements with reversed gene order, are important drivers of population adaptation and divergence, but demonstrating this empirically is challenging due to complex interacting processes that produce similar genomic signatures. We characterized and analysed a large polymorphic inversion in Drosophila montana, a cold-adapted and widely distributed insect, using whole-genome sequencing data, phenotypic experiments, and recent methodological developments. This inversion is found only in mountain populations and is enriched with SNPs potentially associated with climate adaptation, as well as regions that act as barriers to gene flow, with these regions partially overlapping. These results suggest that adaptive loci can act as barriers to gene flow and that inversions help maintain adaptive allelic combinations and associations between multiple barrier loci, thereby contributing to population adaptation and divergence.

evolutionary biology↗

DNA Methylation in Sex Chromosomes and Genes under Selection Underpins the Emergence of Sexual Size Dimorphism

Sexual size dimorphism (SSD) refers to the differences in body size between males and females. Epigenetics such as methylation contribute to shaping phenotypes, nevertheless, their role in SSD is still unclear. Here, we used Cynoglossus semilaevis, a species with larger females known as female-biased SSD, as a model to investigate the role of methylation in the emergence and regulation of SSD. Methylomes and transcriptomes were constructed in four tissues (brain, liver, muscle, and gonad) from three key life stages: juveniles (3-months post fertilization), male mature stage (1-year post fertilization; ypf), and female mature stage (3 ypf). In 1 ypf and 3 ypf females showed lower methylation, while the number of differentially methylated regions between sexes increased during the lifetime. Genes at the top of the growth hormone/insulin-like growth factor (GH/IGF) axis and hypothalamus-pituitary-gonadal axis (gh1, igf1, gnrhr2r-like, err{gamma}, etc.) showed differential methylation between sexes, consistent with sex-related differences in growth. The female-specific W chromosome showed higher methylation than the autosomes or the Z chromosome. Genes of the IGF signaling network that negatively regulate growth and located on W chromosome were hyper-methylated than their Z homologs. Furthermore, genes with a faster evolutionary rate in C. semilaevis exhibited lower methylation levels than the background genes, suggesting an important evolutionary role for DNA methylation in shaping SSD. Our results provide a comprehensive depiction of methylation regulation of SSD in vertebrates, and improve our understanding of how methylation regulation can help organisms to respond to natural selection, and allocate resources between the sexes.

developmental biology↗

Speciation on a complex landscape; phylogeny and demography of Mexican Goodeid fish.

Understanding the phylogeographic history of a group and identifying the factors contributing to speciation is an important challenge in evolutionary biology. Vicariance has clearly played a major role in diversification across diverse groups of organisms, but how this interacts with intrinsic biological features such as changes in reproductive system or sexual selection is less well understood. The Goodeinae are a Mexican endemic group of live-bearing fish. Here, we develop genomic resources for species within the Goodeinae and use phylogenomic approaches to characterise their evolutionary history. We sequenced, assembled and annotated the genomes of four new Goodeinae genomes, including A. toweri, the only matrotrophic live-bearing fish without a trophotaenia in the group. We produced a phylogeny of the Goodeinae and estimate timings of species divergence. We determined the extent and timing of introgression between the species to assess if this may have occurred during an early radiation, or in more recent episodes of secondary contact. We also analyse patterns in the changes of effective population size for the species and examine the time course of expansion and decline. We used branch-site models to detect genome-wide positive selection across Goodeinae, and we specifically ask if this differs in A. toweri, where reversal of placental viviparity has recently occurred. We find that Goodeinae diverged rapidly, with reductions in effective population size after each split. Contrary to expectations, we find evidence of gene flow between geographically isolated species, suggesting vicariant speciation was supplemented by limited post-speciation gene flow, potentially as a result of river piracy. Genes under positive selection in the group are likely to be associated with the switch to live-bearing. Overall, our studies suggest that both volcanism driven vicariance and changes in reproductive mode influenced radiation in the Goodeinae.

evolutionary biology↗

Genomic signatures associated with transitions to viviparity in Cyprinodontiformes

The transition from oviparity to viviparity has occurred independently over a hundred times across vertebrates, presenting a compelling case of phenotypic convergence. However, whether repeated, independent evolution of viviparity is driven by redeployment of similar genetic mechanisms and whether these leave a common genetic signature in genomic divergence remains unknown. Whilst investigations into the evolution of viviparity have demonstrated striking similarity among the genes and pathways involved across vertebrate groups, quantitative tests for genome-wide convergence provide ambivalent answers. Here, we investigate molecular convergence during independent transitions to viviparity across an order of ray-finned freshwater fish (Cyprinodontiformes). We assembled de novo and publicly-available genomes of viviparous and oviparous species to quantify molecular convergence across coding and non-coding regions. We found no evidence for an excess of molecular convergence in amino acid substitutions and rates of sequence divergence, implying independent genetic changes are associated with these transitions. However, statistical power and biological confounds (hemiplasy and introgression) could constrain our ability to detect correlated evolution. We therefore also identified candidate genes with potential signatures of molecular convergence in viviparous Cyprinodontiformes lineages. While we detected no evidence of positive or relaxed selection for these genes in branches associated with the evolution of viviparity in Cyprinodontiformes, motif-enrichment and gene ontology analyses suggest transcriptional changes associated with early morphogenesis, brain development and immunity occurred alongside the evolution of viviparity. Overall, our findings indicate that an excess of molecular convergence, at any level, is not strongly associated with independent transitions to viviparity in these fish.

evolutionary biology↗

Selection on the fly: short term adaptation to an altered sexual selection regime in Drosophila pseudoobscura

Experimental evolution studies are powerful approaches to unveil the evolutionary history of lab populations. Such studies have shed light on how selection changes phenotypes and genotypes. Most of these studies have not examined the time course of adaptation under sexual selection manipulation, by resequencing the populations genomes at multiple time points. Here, we analyse allele frequency trajectories in Drosophila pseudoobscura where we altered their sexual selection regime for 200 generations and sequenced pooled populations at 5 time points. The intensity of sexual selection was either relaxed in monogamous populations (M) or elevated in polyandrous lines (E). We present a comprehensive study of how selection alters population genetics parameters at the chromosome and gene level. We investigate differences in the effective population size - Ne - between the treatments, and perform a genome-wide scan to identify signatures of selection from the time-series data. We found genomic signatures of adaptation to both regimes in D. pseudoobscura. There are more significant variants on E lines as expected from stronger sexual selection. However, we found that the response on the X chromosome was substantial in both treatments, only more marked in E and restricted to chromosome arm XR in M. Ne is lower on the X at the start of the experiment, which might indicate a swift adaptive response at the onset of selection. Additionally, we show that the third chromosome was also affected by elevated polyandry. Its distal end harbours a region showing a strong signal of adaptive divergence in E lines.

evolutionary biology↗

Divergence and introgression among the virilis group of Drosophila

Speciation with gene flow is now widely regarded as common. However, the frequency of introgression between recently diverged species and the evolutionary consequences of gene flow are still poorly understood. The virilis group of Drosophila contains around a dozen species that are geographically widespread and show varying levels of pre-zygotic and post-zygotic isolation. Here, we utilize de novo genome assemblies and whole-genome sequencing data to resolve phylogenetic relationships and describe patterns of introgression and divergence across the group. We suggest that the virilis group consists of three, rather than the traditional two, subgroups. We found evidence of pervasive phylogenetic discordance caused by ancient introgression events between distant lineages within the group, and much more recent gene flow between closely-related species. When assessing patterns of genome-wide divergence in species pairs across the group, we found no consistent genomic evidence of a disproportionate role for the X chromosome. Some genes undergoing rapid sequence divergence across the group were involved in chemical communication and may be related to the evolution of sexual isolation. We suggest that gene flow between closely-related species has potentially had an impact on lineage-specific adaptation and the evolution of reproductive barriers. Our results show how ancient and recent introgression confuse phylogenetic reconstruction, and suggest that shared variation can facilitate adaptation and speciation.

evolutionary biology↗

DrosoPhyla: genomic resources for drosophilid phylogeny and systematics

The vinegar fly Drosophila melanogaster is a pivotal model for invertebrate development, genetics, physiology, neuroscience, and disease. The whole family Drosophilidae, which contains over 4000 species, offers a plethora of cases for comparative and evolutionary studies. Despite a long history of phylogenetic inference, many relationships remain unresolved among the groups and genera in the Drosophilidae. To clarify these relationships, we first developed a set of new genomic markers and assembled a multilocus data set of 17 genes from 704 species of Drosophilidae. We then inferred well-supported group and species trees for this family. Additionally, we were able to determine the phylogenetic position of some previously unplaced species. These results establish a new framework for investigating the evolution of traits in fruit flies, as well as valuable resources for systematics.

evolutionary biology↗

Experimental sexual selection reveals rapid divergence in male and female reproductive transcriptomes and their interactions

Postcopulatory interactions between the sexes in internally fertilizing species elicits both sexual conflict and sexual selection. Macroevolutionary and comparative studies have linked these processes to rapid transcriptomic evolution in sex-specific tissues and substantial transcriptomic postmating responses in females, patterns of which are altered when mating between reproductively isolated species. Here we test multiple predictions arising from sexual selection and conflict theory about the evolution of sex-specific and tissue-specific gene expression and the postmating response at the microevolutionary level. Following over 150 generations of experimental evolution under either reduced (enforced monogamy) or elevated (polyandry) sexual selection in Drosophila pseudoobscura, we found a substantial effect of sexual selection treatment on transcriptomic divergence in virgin male and female reproductive tissues (testes, male accessory glands, the female reproductive tract and ovaries). Sexual selection treatment also had a dominant effect on the postmating response, particularly in the female reproductive tract - the main arena for sexual conflict - compared to ovaries. This affect was asymmetric with monandry females typically showing more postmating responses than polyandry females, with enriched gene functions varying across treatments. The evolutionary history of the male partner had a larger effect on the postmating response of monandry females, but females from both sexual selection treatments showed unique patterns of gene expression and gene function when mating with males from the alternate treatment. Our microevolutionary results mostly confirm comparative macroevolutionary predictions on the role of sexual selection on transcriptomic divergence and altered gene regulation arising from divergent coevolutionary trajectories between sexual selection treatments.

evolutionary biology↗

The discovery, distribution and diversity of DNA viruses associated with Drosophila melanogaster in Europe

Drosophila melanogaster is an important model for antiviral immunity in arthropods, but very few DNA viruses have been described from the family Drosophilidae. This deficiency limits our opportunity to use natural host-pathogen combinations in experimental studies, and may bias our understanding of the Drosophila virome. Here we report fourteen DNA viruses detected in a metagenomic analysis of approximately 6500 pool-sequenced Drosophila, sampled from 47 European locations between 2014 and 2016. These include three new Nudiviruses, a new and divergent Entomopox virus, a virus related to Leptopilina boulardi filamentous virus, and a virus related to Musca domestica salivary gland hypertrophy virus. We also find an endogenous genomic copy of Galbut virus, a dsRNA Partitivirus, segregating at very low frequency. Remarkably, we find that Drosophila Vesanto virus, a small DNA virus previously described as a Bidnavirus, may be composed of up to 12 segments and represent a new lineage of segmented DNA viruses. Two of the DNA viruses, Drosophila Kallithea nudivirus and Drosophila Vesanto virus are relatively common, found in 2% or more of wild flies. The others are rare, with many likely to be represented by a single infected fly. We find that virus prevalence in Europe reflects the prevalence seen in publicly-available datasets, with Drosophila Kallithea nudivirus and Drosophila Vesanto virus the only ones commonly detectable in public data from wild-caught flies and large population cages, and the other viruses being rare or absent. These analyses suggest that DNA viruses are at lower prevalence than RNA viruses in D. melanogaster, and may be less likely to persist in laboratory cultures. Our findings go some way to redressing an earlier bias toward RNA virus studies in Drosophila, and lay the foundation needed to harness the power of Drosophila as a model system for the study of DNA viruses.

microbiology↗

Experimental evolution confirms signatures of sexual selection in genomic divergence.

Comparative genomics has contributed to the growing evidence that sexual selection is an important component of evolutionary divergence and speciation. Divergence by sexual selection is implicated in faster rates of divergence of the X chromosome and of genes thought to underlie sexually selected traits, including genes that are sex-biased in expression. However, accurately inferring the relative importance of complex and interacting forms of natural selection, demography and neutral processes which occurred in the evolutionary past is challenging. Experimental evolution provides an opportunity to apply controlled treatments for multiple generations and examine the consequent genomic divergence. Here we altered sexual selection intensity, elevating sexual selection in polyandrous lines and eliminating it in monogamous lines, and examined patterns of divergence in the genome of Drosophila pseudoobscura after more than 160 generations of experimental evolution. Divergence is not uniform across the genome but concentrated in "islands", many of which contain candidate genes implicated in mating behaviours and other sexually selected phenotypes. These are more often seen on the X chromosome, which shows divergence greater than neutral expectations. There are characteristic signatures of selection seen in these regions, with lower diversity and greater FST on the X chromosome than the autosomes, and differences in diversity on the autosomes between selection regimes. Reduced Tajimas D implies that selective sweeps have occurred within some of the divergent regions, despite considerable recombination. These changes are associated with both differential gene expression between the lines and sex-biased gene expression within the lines. Our results are very similar to those thought to implicate sexual selection in divergence in natural populations, and hence provide experimental support for the likely role of sexual selection in driving such types of genetic divergence, but also illustrate how variable outcomes can be for different genomic regions. Impact SummaryHow does sexual selection contribute to the divergence of genomes? It is often thought that sexual selection is a potent force in evolutionary divergence, but finding signatures of sexual selection in the genome is not straight-forward, and has been quite controversial recently. Here we used experimental evolution to allow replicate populations of fruit fly to evolve under relaxed or strengthened sexual selection for over 160 generations, then sequenced their genomes to see how they had diverged. The features we find are very similar to those reported in populations of natural species thought to be under strong sexual selection. We found that genomic divergence was concentrated in small patches of the genome rather than widespread. These are more often seen on the X chromosome, which overall shows especially elevated divergence. There are also characteristic signatures of selection seen in these regions, with lower genetic diversity suggesting that selection was strong in these regions. The changes are associated with both differential gene expression between the lines and sex-biased gene expression within the lines. Many of the patches of divergence also contain candidate genes implicated in mating behaviours and other sexually selected phenotypes. Our results provide experimental support for the likely role of sexual selection in driving such types of genetic divergence.

evolutionary biology↗

The Pleistocene species pump past its prime: evidence from European butterfly sister species

The Pleistocene glacial cycles had a profound impact on the ranges and genetic make-up of organisms. Whilst it is clear that the contact zones that have been described for many sister taxa are secondary and have formed during the last interglacial, it is unclear when the taxa involved began to diverge. Previous estimates based on small numbers of loci are unreliable given the stochasticity of genetic drift and the contrasting effects of incomplete lineage sorting and gene flow on gene divergence. Here we use genome-wide transcriptome data to estimate divergence for 18 sister species pairs of European butterflies showing either sympatric or contact zone distributions. We find that in most cases species divergence predates the mid-Pleistocene transition or even the entire Pleistocene period. We also show that although post divergence gene flow is restricted to contact zone pairs, they are not systematically younger than sympatric pairs. This suggests that contact zones are not limited to the embryonic stages of the speciation process, but can involve notably old taxa. Finally, we show that mitochondrial and nuclear divergence are only weakly correlated and mitochondrial divergence is higher for contact-zone pairs. This suggests a possible role of selective sweeps affecting mitochondrial variation in maintaining contact zones. Impact SummaryThe influence of the Pleistocene glacial cycles on structuring species and genetic diversity in temperate taxa has permeated biogeographic and phylogeographic thinking for decades. Although phylogeographic studies have repeatedly claimed that the Pleistocene acted as a species pump, systematic tests of this idea based on robust estimates of species divergence are lacking. Here we estimate divergence times for all sister species pairs of European butterfly using genome-wide transcriptome data. We find that most species pairs are substantially older than the onset of Pleistocene glacial cycling. We also show that post divergence gene flow is restricted to pairs that form contact-zones. However, in contrast to expectations under a null model of allopatric speciation contract zone pairs are not necessarily younger than sympatric pairs.

evolutionary biology↗

Sex-specific responses to cold in a very cold-tolerant, northern Drosophila species

Organisms can plastically alter resource allocation in response to changing environmental factors. For example, in harsh conditions organisms are expected to shift investment from reproduction towards survival, however, the factors and mechanisms that govern the magnitude of such shifts are relatively poorly studied. Here we compared the impact of cold on males and females of the highly cold-tolerant species Drosophila montana at the phenotypic and transcriptomic levels. Although both sexes showed similar changes in cold tolerance and gene expression in response to cold treatment, indicating that the majority of changes are concordant between the sexes, we identified a clear reduction in sexually dimorphic gene expression, suggesting that preparing for colder season also involves reducing investment in sex-specific traits. This reduction was larger in males than females, as expected if male sexual traits are more condition-dependent than female traits, as predicted by theory. Gene expression changes were primarily associated with shifts in metabolic profile which likely play a role in increasing cold tolerance. Finally, we found that the expression of immune genes was reduced following cold treatment, suggesting that reduced investment in immunity may be important in helping flies survive colder periods.

evolutionary biology↗

Within-population sperm competition intensity does not predict asymmetry in conpopulation sperm precedence

Postcopulatory sexual selection can generate coevolutionary arms races between the sexes resulting in the rapid coevolution of reproductive phenotypes. As traits affecting fertilisation success diverge between populations postmating prezygotic barriers to gene flow may evolve. Conspecific sperm precedence is a form of such isolation thought to evolve early during speciation yet has mostly been studied between species. Here we show conpopulation sperm precedence between Drosophila montana populations. Using genomic data to estimate divergence times and patterns of gene flow between populations, we show gene flow has played a considerable role during divergence. We find conpopulation sperm precedence is asymmetric and is concordant with asymmetry in non-competitive postmating prezygotic reproductive isolation. These results suggest these phenomena have a shared mechanism, but we show that this asymmetry is unrelated to the strength of postcopulatory sexual selection acting within populations. We tested whether overlapping foreign and coevolved ejaculates within the female reproductive tract altered fertilisation success but found no effect. Our results show that neither time since divergence nor sperm competitiveness predicts the strength of postmating prezygotic reproductive isolation. We suggest that divergence of postcopulatory phenotypes resulting in postmating prezygotic isolation is potentially driven by cryptic female choice, or mutation order divergence.

evolutionary biology↗

Cold adaptation drives population genomic divergence in the ecological specialist, Drosophila montana

Detecting signatures of ecological adaptation in comparative genomics is challenging, but analysing population samples with characterised geographic distributions, such as clinal variation, can help identify genes showing covariation with important ecological variation. Here we analysed patterns of geographic variation in the cold-adapted species Drosophila montana across phenotypes, genotypes and environmental conditions and tested for signatures of cold adaptation in population genomic divergence. We first derived the climatic variables associated with the geographic distribution of 24 populations across two continents to trace the scale of environmental variation experienced by the species, and measured variation in the cold tolerance of the flies of six populations from different geographic contexts. We then performed pooled whole genome sequencing of these six populations, and used Bayesian methods to identify SNPs where genetic differentiation is associated with both climatic variables and the population phenotypic measurements, while controlling for effects of demography and population structure. The top candidate SNPs were enriched on the X and 4th chromosomes, and they also lay near genes implicated in other studies of cold tolerance and population divergence in this species and its close relatives. We conclude that ecological adaptation has contributed to the divergence of D. montana populations throughout the genome and in particular on the X and 4th chromosomes, which also showed highest interpopulation FST. This study demonstrates that ecological selection can drive genomic divergence at different scales, from candidate genes to chromosome-wide effects.

evolutionary biology↗

Identifying genomic markers associated with female re-mating rate in Drosophila pseudoobscura by replicated bulk segregant analysis.

Identifying loci associated with a phenotype is a critical step in many evolutionary studies. Most methods require large sample sizes or breeding designs that can be prohibitively difficult. Here we apply a rarely used approach to identify SNP loci associated with a complex phenotype. We mate siblings from isofemale lines isolate genotypes from three wild populations. After phenotyping we perform whole genome sequencing of isofemale lines from the extremes of the phenotypic distribution of each population and identify SNPs that are consistently fixed for alternative alleles across line pairs. The focal phenotype is female remating rate in the fly Drosophila pseudoobscura, defined as the willingness of a female to mate with a second male after her first mating. This is an integral part of mating system evolution, sexual selection and sexual conflict, and is a quantitative polygenic trait. About 200 SNPs are consistently fixed for alternate alleles in the three pairs of isofemale lines. We use different simulation approaches to explore how many SNPs would be expected to be fixed. We find the surprising result that we uncover fewer observed fixed SNPs than are expected by either simulation approach. We also complete functional analyses of these SNPs. Many lie near genes or regulatory regions known to be involved in Drosophila courtship and mating behaviours, and some have previously been associated with re-mating rates in Genome-Wide Association Studies. Given the small sample size, these results should be treated with caution. Nevertheless, this study suggests that even from a relatively small number of isofemale lines established from wild populations, it is possible to identify candidate loci potentially associated with a complex quantitative trait. However, further work is required to understand modelling the expected distribution of differences.

genomics↗

Silent crickets reveal the genomic footprint of recent adaptive trait loss

Secondary trait loss is widespread and has profound consequences, from generating diversity to driving adaptation. Sexual trait loss is particularly common1. Its genomic impact is challenging to reconstruct because most reversals occurred in the distant evolutionary past and must be inferred indirectly2, and questions remain about the extent of disruption caused by pleiotropy, altered gene expression and loss of homeostasis3. We tested the genomic signature of recent sexual signal loss in Hawaiian field crickets, Teleogryllus oceanicus. Song loss is controlled by a sex-linked Mendelian locus, flatwing, which feminises male wings by erasing sound-producing veins. This variant spread rapidly under pressure from an eavesdropping parasitoid fly. We sequenced, assembled and annotated the T. oceanicus genome, produced a high-density linkage map, and localised flatwing on the X chromosome. We characterised pleiotropic effects of flatwing, including changes in embryonic gene expression and alteration of another sexual signal, chemical pheromones. Song loss is associated with pleiotropy, hitchhiking and genome-wide regulatory disruption which feminises flatwing male pheromones. The footprint of recent adaptive trait loss illustrates R. A. Fishers influential prediction that variants with large mutational effect sizes can invade genomes during the earliest stages of adaptation to extreme pressures, despite having severely disruptive genomic consequences.

evolutionary biology↗

Genomic analysis of European Drosophila melanogaster populations on a dense spatial scale reveals longitudinal population structure and continent-wide selection

Genetic variation is the fuel of evolution, with standing genetic variation especially important for short-term evolution and local adaptation. To date, studies of spatio-temporal patterns of genetic variation in natural populations have been challenging, as comprehensive sampling is logistically difficult, and sequencing of entire populations costly. Here, we address these issues using a collaborative approach, sequencing 48 pooled population samples from 32 locations, and perform the first continent-wide genomic analysis of genetic variation in European Drosophila melanogaster. Our analyses uncover longitudinal population structure, provide evidence for continent-wide selective sweeps, identify candidate genes for local climate adaptation, and document clines in chromosomal inversion and transposable element frequencies. We also characterise variation among populations in the composition of the fly microbiome, and identify five new DNA viruses in our samples.

evolutionary biology↗