Genome-wide patterns of local adaptation in Western European Drosophila melanogaster natural populations

AbstractPopulation genomic data has revealed patterns of genetic variation associated with adaptation in many taxa. Yet understanding the adaptive process that drives such patterns is challenging - it requires disentangling the ecological agents of selection, determining the relevant timescales over which evolution occurs, and elucidating the genetic architecture of adaptation. Doing so for the adaptation of hosts to their microbiome is of particular interest with growing recognition of the importance and complexity of host-microbe interactions. Here, we track the pace and genomic architecture of adaptation to an experimental microbiome manipulation in replicate populations of Drosophila melanogaster in field mesocosms. Manipulation of the microbiome altered population dynamics and increased divergence between treatments in allele frequencies genome-wide, with regions showing strong divergence found on all chromosomes. Moreover, at divergent loci previously associated with adaptation across natural populations, we found that the more common allele in fly populations experimentally enriched for a certain microbial group was also more common in natural populations with high relative abundance of that microbial group. These results suggest that microbiomes may be an agent of selection that shapes the pattern and process of adaptation and, more broadly, that variation in a single ecological factor within a complex environment can drive rapid, polygenic adaptation over short timescales.Significance statementNatural selection can drive evolution over short timescales. However, there is little understanding of which ecological factors are capable of driving rapid evolution and how this rapid evolution alters allele frequencies across the genome. Here we combine a field experiment with population genomic data from natural populations across a latitudinal gradient to assess whether and how microbiome composition drives rapid genomic evolution of host populations. We find that differences in microbiome composition cause divergence in allele frequencies genome-wide, including in genes previously associated with local adaptation. Moreover, we observed concordance between experimental and natural populations in terms of the direction of allele frequency change, suggesting that microbiome composition may be an agent of selection that drives adaptation in the wild.

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Spatiotemporal patterns of desiccation tolerance in natural populations of Drosophila melanogaster

10.1101/079616 ◽

2016 ◽

Cited By ~ 1

Author(s):

Subhash Rajpurohit ◽

Eran Gefen ◽

Alan Bergland ◽

Dmitri Petrov ◽

Allen G Gibbs ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Drought Tolerance ◽

North American ◽

Desiccation Tolerance ◽

Experimental Evolution ◽

Association Studies ◽

Natural Populations ◽

Genome Wide Association Studies ◽

Physiological Basis ◽

Genome Wide

AbstractWater availability is a major environmental challenge to a variety of terrestrial organisms. In insects, desiccation tolerance varies predictably over various spatial and temporal scales and is an important physiological basis of fitness variation among natural populations. Here, we examine the dynamics of desiccation tolerance in North American populations of Drosophila melanogaster using: 1) natural populations sampled across latitudes and seasons in the eastern USA; 2) experimental evolution in the field in response to changing seasonal environments; 3) a sequenced panel of inbred lines (DGRP) to perform genome wide associations and examine whether SNPs/genes associated with variation in desiccation tolerance exhibit patterns of clinal and/or seasonal enrichment in pooled sequencing of populations. In natural populations we observed a shallow cline in desiccation tolerance, for which tolerance exhibited a positive association with latitude; the steepness of this cline increased with decreasing culture temperature, demonstrating a significant degree of thermal plasticity. No differences in desiccation tolerance were observed between spring and autumn collections from three mid-to-northern latitude populations, or as a function of experimental evolution to seasonality. Similarly, water loss rates did not vary significantly among latitudinal, seasonal or experimental evolution populations. However, changes in metabolic rates during prolonged exposure to dry conditions indicate increased tolerance in higher latitude populations. Genome wide association studies identified thirty-six SNPs in twenty-eight genes associated with sex-averaged drought tolerance. Among North American populations, genes associated with drought tolerance do not show increased signatures of spatially varying selection relative to the rest of the genome, whereas among Australian populations they do.

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Allelic polymorphism at foxo contributes to local adaptation in Drosophila melanogaster

10.1101/471565 ◽

2018 ◽

Cited By ~ 1

Author(s):

Nicolas J. Betancourt ◽

Subhash Rajpurohit ◽

Esra Durmaz ◽

Daniel K. Fabian ◽

Martin Kapun ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Life History ◽

Body Size ◽

Local Adaptation ◽

Development Time ◽

Genetic Variance ◽

Allelic Variation ◽

Natural Populations ◽

Life History Variation ◽

Starvation Tolerance

AbstractThe 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.

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Cis and trans-acting variants contribute to survivorship in a naïve Drosophila melanogaster population exposed to ryanoid insecticides

10.1101/502161 ◽

2018 ◽

Author(s):

Llewellyn Green ◽

Paul Battlay ◽

Alexandre Fournier-Level ◽

Robert T. Good ◽

Charles Robin

Keyword(s):

Drosophila Melanogaster ◽

Insecticide Resistance ◽

Allelic Variation ◽

Association Studies ◽

Natural Populations ◽

Intermediate Frequency ◽

Genome Wide Association ◽

Systems Genetics ◽

Genome Wide Association Studies ◽

Genome Wide

AbstractInsecticide resistance is a paradigm of microevolution and insecticides are responsible for the strongest cases of recent selection in the genome of Drosophila melanogaster. Here we use a naïve population and a novel insecticide class to examine the ab initio genetic architecture of a potential selective response. Genome wide association studies of chlorantraniliprole susceptibility reveal variation in a gene of major effect, Stretchin Myosin light chain kinase (Strn-Mlck), which we validate with linkage mapping and transgenic manipulation of gene expression. We propose that allelic variation in Strn-Mlck alters sensitivity to the calcium depletion attributable to chlorantraniliprole’s mode of action. Genome-wide association studies also reveal a network of genes involved in neuromuscular biology. In contrast, phenotype to transcriptome associations identify differences in constitutive levels of multiple transcripts regulated by cnc, the homologue of mammalian Nrf2. This suggests that genetic variation acts in trans to regulate multiple metabolic enzymes in this pathway. The most outstanding association is with the transcription level of Cyp12d1 which is also affected in cis by copy number variation. Transgenic overexpression of Cyp12d1 reduces susceptibility to both chlorantraniliprole and the closely related insecticide cyantraniliprole. This systems genetics study reveals multiple allelic variants segregating at intermediate frequency in a population that is completely naïve to this new insecticide chemistry and it adumbrates a selective response among natural populations to these chemicals.SignificanceAround the world insecticides are being deregistered and banned, as their environmental costs are deemed too great or their efficacy against pest insects is reduced through the evolution of insecticide resistance. With the introduction of replacement insecticides comes the responsibility to assess the way new insecticides perturb various levels of biological systems; from insect physiology to ecosystems. We used a systems genetics approach to identify genetic variants affecting survivorship of Drosophila melanogaster exposed to chlorantraniliprole. The study population was completely naïve to this insecticide chemistry and yet we find associations with variants in neuromuscular genes and co-regulated detoxification genes. We predict that these variants will increase in populations of this ‘sentinel species’ as these insecticides are applied in the environment.

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Global adaptation confounds the search for local adaptation

10.1101/742247 ◽

2019 ◽

Cited By ~ 1

Author(s):

Tom R. Booker ◽

Sam Yeaman ◽

Michael C. Whitlock

Keyword(s):

Genetic Differentiation ◽

Local Adaptation ◽

Natural Populations ◽

Wide Distribution ◽

Structured Populations ◽

Substantial Contribution ◽

Beneficial Mutations ◽

Genome Wide ◽

Spatially Varying ◽

Spatially Varying Selection

AbstractSpatially varying selection promotes variance in allele frequencies, increasing genetic differentiation between the demes of a metapopulation. For that reason, outliers in the genome wide distribution of summary statistics measuring genetic differentiation, such as FST, are often interpreted as evidence for alleles which contribute to local adaptation. However, in spatially structured populations, the spread of beneficial mutations with spatially uniform effects can also induce transient genetic differentiation and numerous theoretical studies have suggested that species-wide, or global, adaptation makes a substantial contribution to molecular evolution. In this study, we ask whether such global adaptation affects the genome-wide distribution of FST and generates statistical outliers which could be mistaken for local adaptation. Using forward-in-time population genetic simulations assuming parameters for the rate and strength of beneficial mutations similar to those that have been estimated for natural populations, we show the spread of globally beneficial in parapatric populations can readily generate FST outliers, which may be misinterpreted as evidence for local adaptation. The spread of beneficial mutations causes selective sweeps at flanking sites, so the effects of global versus local adaptation may be distinguished by examining patterns of nucleotide diversity along with FST. Our study suggests that global adaptation should be considered in the interpretation of genome-scan results and the design of future studies aimed at understanding the genetic basis of local adaptation.

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Secondary contact and local adaptation contribute to genome-wide patterns of clinal variation in Drosophila melanogaster

10.1101/009084 ◽

2014 ◽

Cited By ~ 2

Author(s):

Alan O. Bergland ◽

Ray Tobler ◽

Josefa Gonzalez ◽

Paul Schmidt ◽

Dmitri Petrov

Keyword(s):

Drosophila Melanogaster ◽

North America ◽

Local Adaptation ◽

Latitudinal Gradients ◽

Secondary Contact ◽

Clinal Variation ◽

Evolutionary Forces ◽

Genome Wide ◽

Spatially Varying ◽

Spatially Varying Selection

Populations arrayed along broad latitudinal gradients often show patterns of clinal variation in phenotype and genotype. Such population differentiation can be generated and maintained by historical demographic events and local adaptation. These evolutionary forces are not mutually exclusive and, moreover, can in some cases produce nearly identical patterns of genetic differentiation among populations. Here, we investigate the evolutionary forces that generated and maintain clinal variation genome-wide among populations ofDrosophila melanogastersampled in North America and Australia. We contrast patterns of clinal variation in these continents with patterns of differentiation among ancestral European and African populations. Using established and novel methods we derive here, we show that recently derived North America and Australia populations were likely founded by both European and African lineages and that this admixture event contributed to genome-wide patterns of parallel clinal variation. The pervasive effects of admixture meant that only a handful of loci could be attributed to the operation of spatially varying selection using an FST outlier approach. Our results provide novel insight into the well-studied system of clinal differentiation inD. melanogasterand provide a context for future studies seeking to identify loci contributing to local adaptation in a wide variety of organisms, including other invasive species as well as some temperate endemics.

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