0000000000947794
AUTHOR
Maaria Kankare
Strength of sexual and postmating prezygotic barriers varies between sympatric populations with different histories and species abundances.
The impact of different reproductive barriers on species or population isolation may vary in different stages of speciation depending on evolutionary forces acting within species and through species' interactions. Genetic incompatibilities between interacting species are expected to reinforce prezygotic barriers in sympatric populations and lead to cascade reinforcement between conspecific populations living within and outside the areas of sympatry. We tested these predictions and studied whether and how the strength and target of reinforcement between Drosophila montana and Drosophila flavomontana vary between sympatric populations with different histories and species abundances. All barri…
Experimental introgression in Drosophila : Asymmetric postzygotic isolation associated with chromosomal inversions and an incompatibility locus on the X chromosome
Interspecific gene flow (introgression) is an important source of new genetic variation, but selection against it can reinforce reproductive barriers between interbreeding species. We used an experimental approach to trace the role of chromosomal inversions and incompatibility genes in preventing introgression between two partly sympatric Drosophila virilis group species, D. flavomontana and D. montana. We backcrossed F1 hybrid females from a cross between D. flavomontana female and D. montana male with the males of the parental species for two generations and sequenced pools of parental strains and their reciprocal 2nd generation backcross (BC2mon and BC2fla) females. Contrasting the obser…
Transcriptional Differences between Diapausing and Non-Diapausing D. montana Females Reared under the Same Photoperiod and Temperature
Background A wide range of insects living at higher latitudes enter diapause at the end of the warm season, which increases their chances of survival through harsh winter conditions. In this study we used RNA sequencing to identify genes involved in adult reproductive diapause in a northern fly species, Drosophila montana. Both diapausing and non-diapausing flies were reared under a critical day length and temperature, where about half of the emerging females enter diapause enabling us to eliminate the effects of varying environmental conditions on gene expression patterns of the two types of female flies. Results RNA sequencing revealed large differences between gene expression patterns of…
Changes in gene expression linked with adult reproductive diapause in a northern malt fly species: a candidate gene microarray study
Abstract Background Insect diapause is an important biological process which involves many life-history parameters important for survival and reproductive fitness at both individual and population level. Drosophila montana, a species of D. virilis group, has a profound photoperiodic reproductive diapause that enables the adult flies to survive through the harsh winter conditions of high latitudes and altitudes. We created a custom-made microarray for D. montana with 101 genes known to affect traits important in diapause, photoperiodism, reproductive behaviour, circadian clock and stress tolerance in model Drosophila species. This array gave us a chance to filter out genes showing expression…
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…
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…
Adaptation to a seasonally varying environment: a strong latitudinal cline in reproductive diapause combined with high gene flow inDrosophila montana
Adaptation to seasonal changes in the northern hemisphere includes an ability to predict the forthcoming cold season from gradual changes in environmental cues early enough to prepare for the harsh winter conditions. The magnitude and speed of changes in these cues vary between the latitudes, which induces strong selection pressures for local adaptation. We studied adaptation to seasonal changes in Drosophila montana, a northern maltfly, by defining the photoperiodic conditions leading to adult reproductive diapause along a latitudinal cline in Finland and by measuring genetic differentiation and the amount of gene flow between the sampling sites with microsatellites. Our data revealed a cl…
Sequence variation in couch potato and its effects on life-history traits in a northern malt fly, Drosophila montana
Abstract Couch potato ( cpo ) has previously been connected to reproductive diapause in several insect species including Drosophila melanogaster , where it has been suggested to provide a link between the insulin signalling pathway and the hormonal control of diapause. In the first part of the study we sequenced nearly 3.6 kb of this gene in a northern Drosophila species ( Drosophila montana ) with a robust photoperiodically determined diapause and found several types of polymorphisms along the sequenced area. We also found variation among five Drosophila virilis group species in the length of the 5th exon of cpo and in the site of the stop codon at the end of this exon. The second part of …
Photoperiodic effects on diapause-associated gene expression trajectories in EuropeanLeptinotarsa decemlineatapopulations
Behavioural and physiological changes during diapause, an important strategy of insects for surviving harsh seasonal conditions, have been intensively studied. The genetic and molecular mechanisms underpinning diapause development are less well known. We took a candidate gene approach to study prediapause gene expression patterns in the Colorado potato beetle (Leptinotarsa decemlineata), an invasive insect that has rapidly spread northwards to high seasonality environments. Newly eclosed beetles originating from southern (Italy) and northern (Russia) Europe were reared under short- [12 h light (L):12 h dark (D)] and long-day (18L:6D) photoperiods for 10 days. This time period includes the s…
Strength of sexual and postmating prezygotic barriers varies between sympatric populations with different histories and species abundances
The impact of different reproductive barriers on species or population isolation may vary in different stages of speciation depending on evolutionary forces acting within species and through species’ interactions. Genetic incompatibilities between interacting species are expected to reinforce prezygotic barriers in sympatric populations and lead to cascade reinforcement between conspecific populations living within and outside the areas of sympatry. We tested these predictions and studied whether and how the strength and target of reinforcement between Drosophila montana and Drosophila flavomontana vary between sympatric populations with different histories and species abundances. All barri…
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…
Reinforcement targets sexual or postmating prezygotic reproductive barriers depending on species abundance and population history
AbstractThe impact of different reproductive barriers on species or population isolation may vary in different stages of speciation depending on evolutionary forces acting within species and through species’ interactions. Genetic incompatibilities between interacting species are expected to reinforce prezygotic barriers in sympatric populations and create character displacement between conspecific populations living within and outside the area of sympatry. The outcome of reinforcement has been suggested to be affected by the strength of postzygotic barriers, the history of species coexistence, and the impact of species abundancies on females’ discrimination against heterospecific males. We …
Drosophila Evolution over Space and Time (DEST) - A New Population Genomics Resource
Abstract Drosophila melanogaster is a leading model in population genetics and genomics, and a growing number of whole-genome datasets from natural populations of this species have been published over the last 20 years. A major challenge is the integration of these disparate datasets, often generated using different sequencing technologies and bioinformatic pipelines, which hampers our ability to address questions about the evolution and population structure of this species. Here we address these issues by developing a bioinformatics pipeline that maps pooled sequencing (Pool-Seq) reads from D. melanogaster to a hologenome consisting of fly and symbiont genomes and estimates allele frequenc…
Repeated exposure of fluazinam fungicides affects gene expression profiles yet carries no costs on a nontarget pest
Fungicides are used to control pathogenic fungi of crop species, but they have also been shown to alter behavioral, life history and fitness related traits of non-target insects. Here, we tested the fungicide effects on feeding behavior, survival and physiology of the non-target pest insect, the Colorado potato beetle (Leptinotarsa decemlineata). Feeding behavior was studied by a choice test of adult beetles, which were allowed to choose between a control and a fungicide (fluazinam) treated potato leaf. Larval survival was recorded after 24-hour and 72-hour exposure to control and fungicide-treated leaves with two different concentrations. The adults did not show fungicide avoidance behavio…
Microsatellite-based species identification method for Drosophila virilis group species
Species of the D. virilis group are widely used in evolutionary research, but the individuals of different species are difficult to distinguish from each other morphologically. We constructed a fast and easy microsatellite-based identification method for the species of the group occurring sympatrically in northern Europe. The neighbor joining tree based on 14 microsatellite loci also gave a good resolution of the species divergence pattern in the whole group.
Additional file 1 of Multiple paths to cold tolerance: the role of environmental cues, morphological traits and the circadian clock gene vrille
Additional file 1: Table S1. Information on fly collecting sites and years, and the exact coordinates (latitude, longitude) and altitudes for each collecting site. Table S2. A List of 19 bioclimatic variables used in the PCA (WorldClim database v2.1, 2.5 min spatial resolutions; current data 1970–2000; Fick and Hijmans 2017; www.worldclim.org ). Table S3. 19 bioclimatic variables for each site were extracted from WorldClim database v2.1. Table S4. Principal components with their variance, cumulative variance and Eigenvalues. Table S5. Contributions (loadings) of the altitude and 19 bioclimatic variables on the Principal Component (PC). Table S6. The best-fit model for CCRT, CTmin, body colo…
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…
Mitochondrial DNA variation of Drosophila obscura (Diptera: Drosophilidae) across Europe
Drosophila obscura is a common fruit fly that inhabits the temperate forests of Europe. While it is abundant in the north compared to other Drosophila, its density decreases southwards, where it is gradually replaced by other Drosophila species. This study describes variation in the mitochondrial Cyt b gene of D. obscura from several European populations. We observed a large number of haplotypes, together with the structuring of genetic variation. Genetic variation is higher in the west where O1 and related divergent haplotypes dominate. In the east, the O2 haplotype is most frequent, together with haplotypes that recently arose from it. In the central part of the species range, both O1 and…
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…
Drosophila Evolution over Space and Time (DEST) : A New Population Genomics Resource
Drosophila melanogaster is a leading model in population genetics and genomics, and a growing number of whole-genome datasets from natural populations of this species have been published over the last years. A major challenge is the integration of disparate datasets, often generated using different sequencing technologies and bioinformatic pipelines, which hampers our ability to address questions about the evolution of this species. Here we address these issues by developing a bioinformatics pipeline that maps pooled sequencing (Pool-Seq) reads from D. melanogaster to a hologenome consisting of fly and symbiont genomes and estimates allele frequencies using either a heuristic (PoolSNP) or a…
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 …
Seasonal gene expression kinetics between diapause phases in Drosophila virilis group species and overwintering differences between diapausing and non-diapausing females.
AbstractMost northern insect species experience a period of developmental arrest, diapause, which enables them to survive over the winter and postpone reproduction until favorable conditions. We studied the timing of reproductive diapause and its long-term effects on the cold tolerance of Drosophila montana, D. littoralis and D. ezoana females in seasonally varying environmental conditions. At the same time we traced expression levels of 219 genes in D. montana using a custom-made microarray. We show that the seasonal switch to reproductive diapause occurs over a short time period and that overwintering in reproductive diapause has long-lasting effects on cold tolerance. Some genes, such as…
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…
Multiple paths to cold tolerance: the role of environmental cues, morphological traits and the circadian clock gene vrille
AbstractBackgroundTracing the association between insect cold tolerance and latitudinally and locally varying environmental conditions, as well as key morphological traits and molecular mechanisms, is essential for understanding the processes involved in adaptation. We explored these issues in two closely-related species, Drosophila montana and Drosophila flavomontana, originating from diverse climatic locations across several latitudes on the coastal and mountainous regions of North America. We also investigated the association between sequence variation in one of the key circadian clock genes, vrille, and cold tolerance in both species. Finally, we studied the impact of vrille on fly cold…
Photosensitive Alternative Splicing of the Circadian Clock Gene timeless Is Population Specific in a Cold-Adapted Fly, Drosophila montana.
To function properly, organisms must adjust their physiology, behavior and metabolism in response to a suite of varying environmental conditions. One of the central regulators of these changes is organisms' internal circadian clock, and recent evidence has suggested that the clock genes are also important in the regulation of seasonal adjustments. In particular, thermosensitive splicing of the core clock gene <i>timeless</i> in a cosmopolitan fly, <i>Drosophila melanogaster</i> , has implicated this gene to be involved in thermal adaptation. To further investigate this link we examined the splicing of <i>timeless</i> in a northern malt fly species, <i&…
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…
Cold tolerance and cold-induced modulation of gene expression in two Drosophila virilis group species with different distributions
Abstract The importance of high and low temperature tolerance in adaptation to changing environmental conditions has evoked new interest in modulations in gene expression and metabolism linked with stress tolerance. We investigated the effects of rapid cold hardening and cold acclimatization on the chill coma recovery times of two Drosophila virilis group species, Drosophila montana and D. virilis, with different distributions and utilized a candidate gene approach to trace changes in their gene expression during and after the cold treatments. The study showed that cold acclimatization clearly decreases chill coma recovery times in both species, whereas rapid cold hardening did not have a s…
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…
Photoperiodic regulation of cold tolerance and expression levels of regucalcin gene in Drosophila montana
Temperature-induced plasticity of cold tolerance has been reported in many insect species, but cold tolerance can also be affected by changes in day (or night) length. In the present study we elucidate the direct and indirect effects of photoperiod on the cold tolerance of females of two Drosophila montana strains--one which possesses a robust photoperiodic diapause and another which does not. In the diapause-strain the time needed for recovery from chill coma showed a positive correlation with day length, but diapause itself played only a minor role in photoperiodic acclimation. The strain that was not able to enter to diapause as a response to day length also lacked photoperiodic cold acc…
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…
Circadian clock of Drosophila montana is adapted to high variation in summer day lengths and temperatures prevailing at high latitudes
Photoperiodic regulation of the circadian rhythms in insect locomotor activity has been studied in several species, but seasonal entrainment of these rhythms is still poorly understood. We have traced the entrainment of activity rhythm of northern Drosophila montana flies in a climate chamber mimicking the photoperiods and day and night temperatures that the flies encounter in northern Finland during the summer. The experiment was started by transferring freshly emerged females into the chamber in early and late summer conditions to obtain both non-diapausing and diapausing females for the studies. The locomotor activity of the females and daily changes in the expression levels of two core …
Additional file 1 of Multiple paths to cold tolerance: the role of environmental cues, morphological traits and the circadian clock gene vrille
Additional file 1: Table S1. Information on fly collecting sites and years, and the exact coordinates (latitude, longitude) and altitudes for each collecting site. Table S2. A List of 19 bioclimatic variables used in the PCA (WorldClim database v2.1, 2.5 min spatial resolutions; current data 1970–2000; Fick and Hijmans 2017; www.worldclim.org ). Table S3. 19 bioclimatic variables for each site were extracted from WorldClim database v2.1. Table S4. Principal components with their variance, cumulative variance and Eigenvalues. Table S5. Contributions (loadings) of the altitude and 19 bioclimatic variables on the Principal Component (PC). Table S6. The best-fit model for CCRT, CTmin, body colo…
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: 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: Strength of sexual and postmating prezygotic barriers varies between sympatric populations with different histories and species abundances
The impact of different reproductive barriers on species or population isolation may vary in different stages of speciation depending on evolutionary forces acting within species and through species’ interactions. Genetic incompatibilities between interacting species are expected to reinforce prezygotic barriers in sympatric populations and lead to cascade reinforcement between conspecific populations living within and outside the areas of sympatry. We tested these predictions and studied whether and how the strength and target of reinforcement between Drosophila montana and Drosophila flavomontana vary between sympatric populations with different histories and species abundances. All barri…
Changes in gene expression linked with adult reproductive diapause in a northern malt fly species: a candidate gene microarray study
Background: Insect diapause is an important biological process which involves many life-history parameters important for survival and reproductive fitness at both individual and population level. Drosophila montana, a species of D. virilis group, has a profound photoperiodic reproductive diapause that enables the adult flies to survive through the harsh winter conditions of high latitudes and altitudes. We created a custom-made microarray for D. montana with 101 genes known to affect traits important in diapause, photoperiodism, reproductive behaviour, circadian clock and stress tolerance in model Drosophila species. This array gave us a chance to filter out genes showing expression changes…