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 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 fourth 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 fourth 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.Publisher PDFPeer reviewe

DrosoPhyla: resources for drosophilid phylogeny and systematics

This is the author accepted manuscript. The final version is available on open access from Oxford University Press via the DOI in this recordData availability: The data underlying this article are available on Zenodo (10.5281/zenodo.5091961)The vinegar fly Drosophila melanogaster is a pivotal model for invertebrate development, genetics, physiology, neuroscience, and disease. The whole family Drosophilidae, which contains over 4,400 species, offers a plethora of cases for comparative and evolutionary studies. Despite a long history of phylogenetic inference, many relationships remain unresolved among the genera, subgenera and species groups in the Drosophilidae. To clarify these relationships, we first developed a set of new genomic markers and assembled a multilocus dataset of 17 genes from 704 species of Drosophilidae. We then inferred a species tree with highly supported groups 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.Wellcome Trus

Latitudinal clines in the timing and temperature‐sensitivity of photoperiodic reproductive diapause in Drosophila montana

Abstract Reproductive diapause is a primary mechanism used by arthropods to synchronize their life cycle with seasonal changes in temperate regions. Our study species, Drosophila montana, represents the northern insect species where flies enter reproductive diapause under short day conditions and where the precise timing of diapause is crucial for both survival and offspring production. We have studied clinal variation in the critical day length for female diapause induction (CDL) and their overall susceptibility to enter diapause (diapause incidence), as well as the temperature sensitivity of these traits. The study was performed using multiple strains from four latitudinal clines of the species — short clines in Finland and Alaska and long clines in the Rocky Mountains and the western coast of North America — and from one population in Kamchatka, Russia. CDL showed strong latitudinal clines on both continents, decreasing by one hour per five degrees decline in latitude, on average. CDL also decreased in all populations along with an increase in fly rearing temperature postponing the diapause to later calendar time, the effects of temperature being stronger in southern than in northern population. Female diapause incidence was close to 100% under short day/low temperature conditions in all populations, but decreased below 50% even under short days in 19°C in the southern North American western coast populations and in 22°C in most populations. Comparing a diversity of climatic data for the studied populations showed that while CDL is under a tight photoperiodic regulation linked with latitude, its length depends also on climatic factors determining the growing season length. Overall, the study deepens our understanding of how spatial and environmental parameters affect the seasonal timing of an important biological event, reproductive diapause and helps to estimate the evolutionary potential of insect populations to survive in changing climatic conditions

Factors driving Wolbachia prevalence in native and invasive populations of Drosophila suzukii

Understanding the factors that drive the prevalence of endosymbionts in natural populations is a central goal of evolutionary ecology. The success of maternally transmitted symbionts can be explained by three parameters: reproductive manipulations of the host, vertical transmission rates and effects on host fitness. Those parameters can be modulated by both environmental and genetic factors. The Wolbachia strain wSuz, which infects the invasive pest species Drosophila suzukii, is a canonical example of maternally transmitted symbiont with low to intermediate prevalence in host populations and weak reproductive manipulation. For Wolbachia strains with such properties, the mechanisms inherent to the infection dynamics remain poorly understood. We investigated infection frequencies and wSuz intra-strain polymorphism in 24 natural populations of D. suzukii from both native (China and Japan) and invasive areas (Europe and America). Infection frequencies in populations from China were on average significantly higher than those in populations from invasive areas. Based on the study of an insertion sequence site and a genomic rearrangement polymorphism in wSuz genome, we could identify three wSuz variants (i.e. European, American and Asian) corresponding to the initial sample location. More in-depth investigations indicated that the European variant was also present in some Asian populations and that one population from Europe included the European and American variants. Additional analyses based on whole-genome sequencing of 70 D. suzukii population samples showed lower Wolbachia genomic diversity in invasive populations (America and Europe) than in native (Japan, Korea and China) populations, consistent with a bottleneck in invasive populations. Finally, we analyzed two types of factors that could affect Wolbachia infection frequencies in natural populations: climatic variation and Wolbachia-induced cytoplasmic incompatibility. We found that variations in the strength of cytoplasmic incompatibilities or in monthly temperatures were not sufficient to fully explain observed prevalence pattern. Overall, our results show that, despite reduced intra-strain genomic diversity, both population prevalence and phenotypic effects on host reproduction can vary greatly among Wolbachia variants, suggesting complex interactions with host genetic background and environmental factors