0000000001301565
AUTHOR
Michael G. Ritchie
Two distinct genomic regions, harbouring the period and fruitless genes, affect male courtship song in Drosophila montana
Acoustic signals often have a significant role in pair formation and in species recognition. Determining the genetic basis of signal divergence will help to understand signal evolution by sexual selection and its role in the speciation process. An earlier study investigated quantitative trait locus for male courtship song carrier frequency (FRE) in Drosophila montana using microsatellite markers. We refined this study by adding to the linkage map markers for 10 candidate genes known to affect song production in Drosophila melanogaster. We also extended the analyses to additional song characters (pulse train length (PTL), pulse number (PN), interpulse interval, pulse length (PL) and cycle nu…
Cold adaptation drives population genomic divergence in the ecological specialist, Drosophila montana
Funding: UK Natural Environment Research Council (Grant Number(s): NE/L501852/1, NE/P000592/1); Academy of Finland (GrantNumber(s): 267244, 268214, 322980), Ella ja Georg Ehrnroothin Säätiö. 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…
Copulation duration, but not paternity share, potentially mediates inbreeding avoidance in Drosophila montana
Studying the incidence of inbreeding avoidance is important for understanding the evolution of mating systems, especially in the context of mate choice for genetic compatibility. We investigated whether inbreeding avoidance mechanisms have evolved in the malt fly, Drosophila montana, by measuring mating latency (a measure of male attractiveness), copulation duration, days to remating, offspring production, and the proportion of offspring sired by the first (P1) and second (P2) male to mate in full-sibling and unrelated pairs. SNP markers were used for paternity analysis and for calculating pairwise relatedness values (genotype sharing) between mating pairs. We found 18 % inbreeding depressi…
Sex-specific responses to cold in a very cold-tolerant, northern Drosophila species
Funding: This work was supported by Academy of Finland projects 268214 and 322980 to MK and a NERC (UK) grant NE/P000592/1 to MGR. 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 toward 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…
Sex-specific responses to cold in a very cold-tolerant, northern Drosophila species
AbstractOrganisms 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 reducti…
MALE COURTSHIP SONG AND FEMALE PREFERENCE VARIATION BETWEEN PHYLOGEOGRAPHICALLY DISTINCT POPULATIONS OF DROSOPHILA MONTANA
Understanding the variation within and between populations in important male mating traits and female preferences is crucial to theories concerning the origin of sexual isolation by coevolution or other processes. There have been surprisingly few studies on the extent of variation and covariation within and between populations, especially where the evolutionary relationships between populations are understood. Here we examine variation in female preferences and a sexually selected male song trait, the carrier frequency of the song, within and between populations from different phylogeographic clusters of Drosophila montana. Song is obligatory for successful mating in this species, and both …
Incipient speciation in Drosophila melanogaster involves chemical signals.
WOS: 000300572900001; International audience; The sensory and genetic bases of incipient speciation between strains of Drosophila melanogaster from Zimbabwe and those from elsewhere are unknown. We studied mating behaviour between eight strains - six from Zimbabwe, together with two cosmopolitan strains. The Zimbabwe strains showed significant sexual isolation when paired with cosmopolitan males, due to Zimbabwe females discriminating against these males. Our results show that flies' cuticular hydrocarbons (CHs) were involved in this sexual isolation, but that visual and acoustic signals were not. The mating frequency of Zimbabwe females was highly significantly negatively correlated with t…
The genetic architecture of sexually selected traits in two natural populations of Drosophila montana
The work was supported by the National Environment Research Council (grant NE/E015255/1 to MGR and RKB) and the Academy of Finland (project 132619 to AH). We investigated the genetic architecture of courtship song and cuticular hydrocarbon traits in two phygenetically distinct populations of Drosophila montana. To study natural variation in these two important traits, we analysed within-population crosses among individuals sampled from the wild. Hence, the genetic variation analysed should represent that available for natural and sexual selection to act upon. In contrast to previous between-population crosses in this species, no major quantitative trait loci (QTLs) were detected, perhaps be…
Postmating–prezygotic isolation between two allopatric populations of Drosophila montana: fertilisation success differs under sperm competition
This study was funded by the Academy of Finland (grant 250999 to O. A.-H.). Postmating but prezygotic (PMPZ) interactions are increasingly recognized as a potentially important early-stage barrier in the evolution of reproductive isolation. A recent study described a potential example between populations of the same species: single matings between Drosophila montana populations resulted in differential fertilisation success because of the inability of sperm from one population (Vancouver) to penetrate the eggs of the other population (Colorado). As the natural mating system of D. montana is polyandrous (females remate rapidly), we set up double matings of all possible crosses between the sa…
A microsatellite linkage map forDrosophila montanashows large variation in recombination rates, and a courtship song trait maps to an area of low recombination
Current advances in genetic analysis are opening up our knowledge of the genetics of species differences, but challenges remain, particularly for out-bred natural populations. We constructed a microsatellite-based linkage map for two out-bred lines of Drosophila montana derived from divergent populations by taking advantage of the Drosophila virilis genome and available cytological maps of both species. Although the placement of markers was quite consistent with cytological predictions, the map indicated large heterogeneity in recombination rates along chromosomes. We also performed a quantitative trait locus (QTL) analysis on a courtship song character (carrier frequency), which differs be…
The discovery, distribution and diversity of DNA viruses associated withDrosophila melanogasterin Europe
AbstractDrosophila melanogasteris 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 theDrosophilavirome. Here we report fourteen DNA viruses detected in a metagenomic analysis of approximately 6500 pool-sequencedDrosophila, sampled from 47 European locations between 2014 and 2016. These include three new Nudiviruses, a new and divergent Entomopox virus, a virus related toLeptopilina boulardifilamentous virus, and a virus related toMusca domesticasalivary gland hypertrophy…
Sexual and postmating reproductive isolation between allopatric Drosophila montana populations suggest speciation potential
This work was funded by a European Commission Research Training Grant RTN2-2001-00049, the Centre of Excellence for Evolutionary Research at the University of Jyväskylä and a Marie Curie Initial Training Network, ‘Understanding the evolutionary origin of biological diversity’ (ITN-2008-213780 SPECIATION) Background: Widely distributed species with populations adapted to different environmental conditions can provide valuable opportunities for tracing the onset of reproductive incompatibilities and their role in the speciation process. Drosophila montana, a D. virilis group species found in high latitude boreal forests in Nearctic and Palearctic regions around the globe, could be an excellen…
Divergence and introgression among the virilis group of Drosophila
AbstractSpeciation 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 p…
Selection for reproduction under short photoperiods changes diapause-associated traits and induces widespread genomic divergence.
The work has been supported by the Academyof Finland to A.H. (project 267244) and Natural Environment Research Council (NERC) funding (NE/J020818/1 to M.G.R.; NE/L501852/1 to R.A.W.W.). The incidence of reproductive diapause is a critical aspect of life history in overwintering insects from temperate regions. Much has been learned about the timing, physiology and genetics of diapause in a range of insects, but how the multiple changes involved in this and other photoperiodically regulated traits are inter-related is not well understood. We performed quasinatural selection on reproduction under short photoperiods in a northern fly species, Drosophila montana, to trace the effects of photoper…
Inter- and intra-specific genomic divergence in Drosophila montana shows evidence for cold adaptation
This work was supported by the Academy of Finland to AH (projects 132619 and 267244) and to MK (projects 268214 and 272927) and NERC (UK) funding to MGR (grants NE/E015255/1 and NE/J020818/1) and PhD studentship to DJP (NE/I528634/1). The genomes of species that are ecological specialists will likely contain signatures of genomic adaptation to their niche. However, distinguishing genes related to ecological specialism from other sources of selection and more random changes is a challenge. Here we describe the genome of Drosophila montana, which is the most extremely cold-adapted Drosophila species. We use branch tests to identify genes showing accelerated divergence in contrasts between col…
How consistent are the transcriptome changes associated with cold acclimation in two species of the Drosophila virilis group?
This work was financially support by a Marie Curie Initial Training Network grant, “Understanding the evolutionary origin of biological diversity” (ITN-2008–213780 SPECIATION), grants from the Academy of Finland to A.H. (project 132619) and M.K. (projects 268214 and 272927), a grant from NERC, UK to M.G.R. (grant NE/J020818/1), and NERC, UK PhD studentship to D.J.P. (NE/I528634/1). For many organisms the ability to cold acclimate with the onset of seasonal cold has major implications for their fitness. In insects, where this ability is widespread, the physiological changes associated with increased cold tolerance have been well studied. Despite this, little work has been done to trace chang…
When are vomiting males attractive? Sexual selection on condition-dependent nuptial feeding in Drosophila subobscura
Nuptial gifts are any nutritious items or inedible tokens transferred from the male to the female as a part of courtship or copulation. Although nuptial gift donation has been studied in a variety of taxa, this behavior has been largely overlooked in Drosophila. We studied nuptial feeding in Drosophila subobscura, where the gift is a regurgitated drop of liquid, in order to examine the importance of this behavior for male mating success and female fecundity. We varied male and female condition by dietary restriction to assess any condition dependence of male nuptial feeding ability and female feeding behavior and mate discrimination. Our results show that there was directional selection for…
Preparing for Winter: The Transcriptomic Response Associated with Different Day Lengths in Drosophila montana
The work has been supported by a Natural Environment Research Council studentship to D.J.P. and an Academy of Finland grant to M.K. (project 268214). At northern latitudes, the most robust cue for assessing the onset of winter is the shortening of day lengths. Many species use day length as a cue to increase their cold tolerance and/or enter into diapause, but little is known about changes in gene expression that occur under different day lengths. We investigate the gene expression changes associated with differences in light/dark cycles in Drosophila montana, a northerly distributed species with a strong adult photoperiodic reproductive diapause. To examine gene expression changes induced …
Localization of quantitative trait loci for diapause and other photoperiodically regulated life history traits important in adaptation to seasonally varying environments.
Seasonally changing environments at high latitudes present great challenges for the reproduction and survival of insects, and photoperiodic cues play an important role in helping them to synchronize their life cycle with prevalent and forthcoming conditions. We have mapped quantitative trait loci (QTL) responsible for the photoperiodic regulation of four life history traits, female reproductive diapause, cold tolerance, egg-to-eclosion development time and juvenile body weight in Drosophila montana strains from different latitudes in Canada and Finland. The F2 progeny of the cross was reared under a single photoperiod (LD cycle 16:8), which the flies from the Canadian population interpret a…
Transcriptomes of parents identify parenting strategies and sexual conflict in a subsocial beetle
This work was funded by UK NERC grants to M.G.R. and A.J.M. an NERC studentship to D.J.P. the University of Georgia and a US NSF grant to A.J.M. and M.G.R. Parenting in the burying beetle Nicrophorus vespilloides is complex and, unusually, the sex and number of parents that can be present is flexible. Such flexibility is expected to involve specialized behaviour by the two sexes under biparental conditions. Here, we show that offspring fare equally well regardless of the sex or number of parents present. Comparing transcriptomes, we find a largely overlapping set of differentially expressed genes in both uniparental and biparental females and in uniparental males including vitellogenin, ass…
Genomic Analysis of European Drosophila melanogaster Populations Reveals Longitudinal Structure, Continent-Wide Selection, and Previously Unknown DNA Viruses
Genetic variation is the fuel of evolution, with standing genetic variation especially important for short-term evolution and local adaptation. To date, studies of spatiotemporal 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, ide…
Debating Sexual Selection and Mating Strategies
Published at full length with the title 'Reproductive behaviour: sexual selection remains the best explanation' in Science E-letters, 6 April 2006
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 6668 pool-sequenced Drosophila, sampled from forty-seven European locations between 2014 and 2016. These include three new nudiviruses, a new and divergent entomopoxvirus, a virus related to Leptopilina boulardi filamentous virus, and a virus related to Musca domestica salivary gland hypertrophy viru…
Multiple quantitative trait loci influence intra-specific variation in genital morphology between phylogenetically distinct lines of Drosophila montana
The evolution of animal genitalia has gained renewed interest because of their potential roles during sexual selection and early stages of species formation. Although central to understanding the evolutionary process, knowledge of the genetic basis of natural variation in genital morphology is limited to a very few species. Using an outbred cross between phylogenetically distinct lines of Drosophila montana, we characterized quantitative trait loci (QTLs) affecting the size and shape of the distiphallus, a prominent part of the male intromittent organ. Our microsatellite-based linkage analysis shows that intra-specific variation in the distiphallus involves several QTLs of largely additive …
What do we need to know about speciation?
Speciation has been a major focus of evolutionary biology research in recent years, with many important advances. However, some of the traditional organising principles of the subject area no longer provide a satisfactory framework, such as the classification of speciation mechanisms by geographical context into allopatric, parapatric and sympatry classes. Therefore, we have asked where speciation research should be directed in the coming years. Here, we present a distillation of questions about the mechanisms of speciation, the genetic basis of speciation and the relationship between speciation and diversity. Our list of topics is not exhaustive; rather we aim to promote discussion on rese…
Sexual selection on song and cuticular hydrocarbons in two distinct populations ofDrosophila montana
Sexual selection has the potential to contribute to population divergence and speciation. Most studies of sexual selection in Drosophila have concentrated on a single signaling modality, usually either courtship song or cuticular hydrocarbons (CHCs), which can act as contact pheromones. We have examined the relationship between both signal types and reproductive success using F1–3 offspring of wild-collected flies, raised in the lab. We used two populations of the Holarctic species Drosophila montana that represent different phylogeographic clades that have been separate for ca. 0.5 million years (MY), and differ to some extent in both traits. Here, we characterize the nature and identify t…
Erratum: Transcriptomes of parents identify parenting strategies and sexual conflict in a subsocial beetle
Parenting in the burying beetle Nicrophorus vespilloides is complex and, unusually, the sex and number of parents that can be present is flexible. Such flexibility is expected to involve specialized behaviour by the two sexes under biparental conditions. Here, we show that offspring fare equally well regardless of the sex or number of parents present. Comparing transcriptomes, we find a largely overlapping set of differentially expressed genes in both uniparental and biparental females and in uniparental males including vitellogenin, associated with reproduction, and takeout, influencing sex-specific mating and feeding behaviour. Gene expression in biparental males is similar to that in non…
Data from: Localization of QTL for diapause and other photoperiodically regulated life-history traits important in adaptation to seasonally varying environments
Seasonally changing environments at high latitudes present great challenges for the reproduction and survival of insects, and photoperiodic cues play an important role in helping them to synchronize their life cycle with prevalent and forthcoming conditions. We have mapped quantitative trait loci (QTL) responsible for the photoperiodic regulation of four life history traits, female reproductive diapause, cold tolerance, egg-to-eclosion development time and juvenile body weight in Drosophila montana strains from different latitudes in Canada and Finland. The F2 progeny of the cross was reared under a single photoperiod (LD cycle 16:8), which the flies from the Canadian population interpret a…
Data from: Postmating-prezygotic isolation between two allopatric populations of Drosophila montana: fertilisation success differs under sperm competition
Postmating but prezygotic (PMPZ) interactions are increasingly recognized as a potentially important early-stage barrier in the evolution of reproductive isolation. A recent study described a potential example between populations of the same species: single matings between Drosophila montana populations resulted in differential fertilisation success because of the inability of sperm from one population (Vancouver) to penetrate the eggs of the other population (Colorado). As the natural mating system of D. montana is polyandrous (females remate rapidly), we set up double matings of all possible crosses between the same populations to test whether competitive effects between ejaculates influe…
Data from: Inter- and intra-specific genomic divergence in Drosophila montana shows evidence for cold adaptation
D. montana gff fileGenome annotation file for D. montana genome (Accession number: LUVX00000000)D.mont_freeze_v1.4.gff.txt
Data from: Two distinct genomic regions, harbouring the period and fruitless genes, affect male courtship song in Drosophila montana
Acoustic signals often play a significant role in pair formation and in species recognition. Determining the genetic basis of signal divergence will help to understand signal evolution by sexual selection and its role in the speciation process. An earlier study investigated QTL for male courtship song carrier frequency in Drosophila montana using microsatellite markers. We refined this study by adding to the linkage map markers for ten candidate genes known to affect song production in D. melanogaster. We also extended the analyses to additional song characters (pulse train length, pulse number, interpulse interval, pulse length and cycle number). Our results indicate that loci in two diffe…
Data from: The genetic architecture of sexually selected traits in two natural populations of Drosophila montana
We investigated the genetic architecture of courtship song and cuticular hydrocarbon traits in two phygenetically distinct populations of Drosophila montana. In order to study natural variation in these two important traits, we analysed within-population crosses among individuals sampled from the wild. Hence, the genetic variation analysed should represent that available for natural and sexual selection to act upon. In contrast to previous between-population crosses in this species, no major QTLs were detected, perhaps because the between-population QTL were due to fixed differences between the populations. Partitioning the trait variation to chromosomes suggested a broadly polygenic geneti…
Data from: Sexual selection on song and cuticular hydrocarbons in two distinct populations of Drosophila montana
Sexual selection has the potential to contribute to population divergence and speciation. Most studies of sexual selection in Drosophila have concentrated on a single signaling modality, usually either courtship song or cuticular hydrocarbons (CHCs), which can act as contact pheromones. We have examined the relationship between both signal types and reproductive success using F1-3 offspring of wild-collected flies, raised in the lab. We used two populations of the Holarctic species Drosophila montana, that represent different phylogeographic clades which have been separate for ca. 0.5 MY, and which differ to some extent in both traits. Here we characterise the nature and identify the target…
Data from: Transcriptomes of parents identify parenting strategies and sexual conflict in a subsocial beetle
Parenting in the burying beetle Nicrophorus vespilloides is complex and, unusually, the sex and number of parents that can be present is flexible. Such flexibility is expected to involve specialized behaviour by the two sexes under biparental conditions. Here, we show that offspring fare equally well regardless of the sex or number of parents present. Comparing transcriptomes, we find a largely overlapping set of differentially expressed genes in both uniparental and biparental females and in uniparental males including vitellogenin, associated with reproduction, and takeout, influencing sex-specific mating and feeding behaviour. Gene expression in biparental males is similar to that in non…