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Kapun, M.

Publications and source records attributed to Kapun, M..

28 records · Page 2Linked to original sources

Genomic signals of admixture and reinforcement between two closely related species of European sepsid flies

Interspecific gene flow by hybridization may weaken species barriers and adaptive divergence, but can also initiate reinforcement of reproductive isolation trough natural and sexual selection. The extent of interspecific gene flow and its consequences for the initiation and maintenance of species barriers in natural systems remain poorly understood, however. To assess genome-wide patterns of gene flow between the two closely related European dung fly species Sepsis cynipsea and Sepsis neocynipsea (Diptera: Sepsidae), we tested for historical gene flow with the aid of ABBA-BABA test using whole-genome resequencing data from pooled DNA of male specimens originating from natural and laboratory populations. We contrasted genome-wide variation in DNA sequence differences between samples from sympatric populations of the two species in France and Switzerland with that of interspecific differences between pairs of samples involving allopatric populations from Estonia and Italy. In the French Cevennes, we detected a relative excess of DNA sequence identity, suggesting interspecific gene flow in sympatry. In contrast, at two sites in Switzerland, we observed a relative depletion of DNA sequence identity compatible with reinforcement of species boundaries in sympatry. Our results suggest that the species boundaries between S. cynipsea and S. neocynipsea in Europe depend on the eco-geographic context.

evolutionary biology↗

Continent-wide structure of bacterial microbiomes of European Drosophila melanogaster suggests host-control

The relative importance of host-control, environmental effects, and stochasticity in the assemblage of host-associated microbiomes has been much debated. With recent sampling efforts, the underpinnings of D. melanogasters microbiome structure have become tractable on larger spatial scales. We analyzed the microbiome among fly populations that were sampled across Europe by the European Drosophila Population Genomics Consortium (DrosEU). We combined environmental data on climate and food-substrate, dense genomic data on host population structure, and microbiome profiling. Food-substrate, temperature, and host population-structure correlated with microbiome-structure. The microbes, whose abundance was co-structured with host populations, also differed in abundance between flies and their substrate in an independent survey, suggesting host-control. Patterns of enrichment and depletion of microbes between host and substrate were consistent with a model of host-control, where the host manipulates its microbiome for its benefit. Putative host-control was bacterial strain specific, supporting recent evidence for high specificity of D. melanogaster-microbe interaction.

evolutionary biology↗

A clinal polymorphism in the insulin signaling transcription factor foxo contributes to life-history adaptation in Drosophila

A fundamental aim of adaptation genomics is to identify polymorphisms that underpin variation in fitness traits. In D. melanogaster latitudinal life-history clines exist on multiple continents and make an excellent system for dissecting the genetics of adaptation. We have previously identified numerous clinal SNPs in insulin/insulin-like growth factor signaling (IIS), a pathway known from mutant studies to affect life history. However, the effects of natural variants in this pathway remain poorly understood. Here we investigate how two clinal alternative alleles at foxo, a transcriptional effector of IIS, affect fitness components (viability, size, starvation resistance, fat content). We assessed this polymorphism from the North American cline by reconstituting outbred populations, fixed for either the low- or high-latitude allele, from inbred DGRP lines. Since diet and temperature modulate IIS, we phenotyped alleles across two temperatures (18{degrees}C, 25{degrees}C) and two diets differing in sugar source and content. Consistent with clinal expectations, the high-latitude allele conferred larger body size and reduced wing loading. Alleles also differed in starvation resistance and expression of InR, a transcriptional target of FOXO. Allelic reaction norms were mostly parallel, with few GxE interactions. Together, our results suggest that variation in IIS makes a major contribution to clinal life-history adaptation.

evolutionary biology↗

Allelic polymorphism at foxo contributes to local adaptation in Drosophila melanogaster

The insulin insulin-like growth factor signaling pathway has been hypothesized as a major determinant of life history profiles that vary adaptively in natural populations. In Drosophila melanogaster, multiple components of this pathway vary predictably with latitude; this includes foxo, a conserved gene that regulates insulin signaling and has pleiotropic effects on a variety of fitness-associated traits. We hypothesized that allelic variation at foxo underlies genetic variance for traits that vary with latitude and reflect local adaptation. To evaluate this, we generated recombinant outbred populations in which the focal foxo allele was homozygous and fixed for either the allele common at high latitude or low latitude and the genomic background was randomized across 20 inbred lines. After eight generations of recombination, experimental populations were phenotyped for a series of traits related to gene function. Our results demonstrate that natural allelic variation at foxo has major and predictable effects on body size and starvation tolerance, but not on development time. These patterns mirror those observed in natural populations collected across the latitudinal gradient in the eastern U.S.: clines were observed for starvation tolerance and body size, but development time exhibited no association with latitude. Furthermore, differences in size between foxo genotypes were equivalent to those observed between populations sampled from the latitudinal extremes, although contribution to the genetic variance for starvation tolerance was less pronounced. These results suggest that allelic variation at foxo is a major contributor to adaptive patterns of life history variation in natural populations of this genetic model.

evolutionary biology↗

Wolbachia modifies thermal preference in Drosophila melanogaster

Environmental variation can have profound and direct effects on fitness, fecundity, and host symbiont interactions. Replication rates of microbes within arthropod hosts, for example, are correlated with incubation temperature but less is known about the influence of host-symbiont dynamics on environmental preference. Hence, we conducted thermal preference (Tp) assays and tested if infection status and genetic variation in endosymbiont bacterium Wolbachia affected temperature choice of Drosophila melanogaster. We demonstrate that isogenic flies infected with Wolbachia preferred lower temperatures compared to uninfected Drosophila. Moreover, Tp varied with respect to three investigated Wolbachia variants (wMel, wMelCS and wMelPop). While uninfected individuals preferred 24.4{degrees}C, we found significant shifts of - 1.2{degrees}C in wMel- and -4{degrees}C in flies infected either with wMelCS or wMelPop. We, therefore, postulate that Wolbachia-associated Tp variation within a host species might represent a behavioral accommodation to host-symbiont interactions and trigger behavioral self-medication and bacterial titer regulation by the host.

microbiology↗

Altering the temporal regulation of one transcription factor drives sensory trade-offs

Size trade-offs of visual versus olfactory organs is a pervasive feature of animal evolution. Comparing Drosophila species, we find that larger eyes correlate with smaller antennae, where olfactory organs reside, and narrower faces. We demonstrate that this tradeoff arises through differential subdivision of the head primordium into visual versus non-visual fields. Specification of the visual field requires a highly-conserved eye development gene called eyeless in flies and Pax6 in humans. We discover that changes in the temporal regulation of eyeless expression during development is a conserved mechanism for sensory trade-offs within and between Drosophila species. We identify a natural single nucleotide polymorphism in the cis-regulatory region of eyeless that is sufficient to alter its temporal regulation and eye size. Because Pax6 is a conserved regulator of sensory placode subdivision, we propose that alterations in the mutual repression between sensory territories is a conserved mechanism for sensory trade-offs in animals.

developmental biology↗

Early split between African and European populations of Drosophila melanogaster

Natural populations of the fruit fly Drosophila melanogaster have been used extensively as a model system to investigate the effect of neutral and selective processes on genetic variation. The species expanded outside its Afrotropical ancestral range during the last glacial period and numerous studies have focused on identifying molecular adaptations associated with the colonization of northern habitats. The sequencing of many genomes from African and non-African natural populations has facilitated the analysis of the interplay between adaptive and demographic processes. However, most of the non-African sequenced material has been sampled from American and Australian populations that have been introduced within the last hundred years following recent human dispersal and are also affected by recent genetic admixture with African populations. Northern European populations, at the contrary, are expected to be older and less affected by complex admixture patterns and are therefore more appropriate to investigate neutral and adaptive processes. Here we present a new dataset consisting of 14 fully sequenced haploid genomes sampled from a natural population in Ume[a], Sweden. We co-analyzed this new data with an African population to compare the likelihood of several competing demographic scenarios for European and African populations. We show that allowing for gene flow between populations in neutral demographic models leads to a significantly better fit to the data and strongly affects estimates of the divergence time and of the size of the bottleneck in the European population. Our results indicate that the time of divergence between cosmopolitan and ancestral populations is 30,000 years older than reported by previous studies.

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↗

Rapid seasonal evolution in innate immunity of wild Drosophila melanogaster

Understanding the rate of evolutionary change and the genetic architecture that facilitates rapid adaptation is a current challenge in evolutionary biology. Comparative studies show that genes with immune function are among the most rapidly evolving genes in a range of taxa. Here, we use immune defense in natural populations of D. melanogaster to understand the rate of evolution in natural populations and the genetics underlying the rapid change. We probed the immune system using the natural pathogens Enterococcus faecalis and Providencia rettgeri to measure post-infection survival and bacterial load of wild D. melanogaster populations collected across seasonal time along a latitudinal transect on the eastern North America (Massachusetts, Pennsylvania, and Virginia). There are pronounced and repeatable changes in the immune response over approximately 10 generations between the spring and fall populations with a significant but less distinct difference among geographic locations. Genes with known immune function are not enriched among alleles that cycle with seasonal time, but the immune function of a subset of seasonally cycling alleles in immune genes was tested using reconstructed outbred populations. We find that flies containing seasonal alleles in Thioester-containing protein 3 (Tep3) have different functional responses to infection and that epistatic interactions among seasonal Tep3 and Drosomycin-like 6 (Dro6) alleles produce the immune phenotypes observed in natural populations. This rapid, cyclic response to seasonal environmental pressure broadens our understanding of the complex ecological and genetic interactions determining the evolution of immune defense in natural populations.

evolutionary biology↗

A simple genetic basis of adaptation to a novel thermal environment results in complex metabolic rewiring in Drosophila

Population genetic theory predicts that rapid adaptation is largely driven by complex traits encoded by many loci of small effect. Because large effect loci are quickly fixed in natural populations, they should not contribute much to rapid adaptation. To investigate the genetic architecture of thermal adaptation - a highly complex trait - we performed experimental evolution on a natural Drosophila simulans population. Transcriptome and respiration measurements revealed extensive metabolic rewiring after only [~]60 generations in a hot environment. Analysis of genome-wide polymorphisms identified two interacting selection targets, Sestrin and SNF4A{gamma}, pointing to AMPK, a central metabolic switch, as a key factor for thermal adaptation. Our results demonstrate that large-effect loci segregating at intermediate allele frequencies can allow natural populations to rapidly respond to selection. Because SNF4A{gamma} also exhibits clinal variation in various Drosophila species, we suggest that this large effect polymorphism is maintained by temporal and spatial temperature variation in natural environments.

evolutionary biology↗