Genome‐wide patterns of latitudinal differentiation among populations of Drosophila melanogaster from North America

Abstract

Understanding the genetic underpinnings of adaptive change is a fundamental but largely unresolved problem in evolutionary biology. Drosophila melanogaster, an ancestrally tropical insect that has spread to temperate regions and become cosmopolitan, offers a powerful opportunity for identifying the molecular polymorphisms underlying clinal adaptation. Here, we use genome-wide next-generation sequencing of DNA pools ('pool-seq') from three populations collected along the North American east coast to examine patterns of latitudinal differentiation. Comparing the genomes of these populations is particularly interesting since they exhibit clinal variation in a number of important life history traits. We find extensive latitudinal differentiation, with many of the most strongly differentiated genes involved in major functional pathways such as the insulin/TOR, ecdysone, torso, EGFR, TGFβ/BMP, JAK/STAT, immunity and circadian rhythm pathways. We observe particularly strong differentiation on chromosome 3R, especially within the cosmopolitan inversion In(3R)Payne, which contains a large number of clinally varying genes. While much of the differentiation might be driven by clinal differences in the frequency of In(3R)P, we also identify genes that are likely independent of this inversion. Our results provide genome-wide evidence consistent with pervasive spatially variable selection acting on numerous loci and pathways along the well-known North American cline, with many candidates implicated in life history regulation and exhibiting parallel differentiation along the previously investigated Australian cline.

Genomic Patterns of Geographic Differentiation in Drosophila simulans

“…Genome wide, higher-latitude populations have higher mean heterozygosity than lower-latitude populations based both on genome-wide b p s and mean b p in 100-kb windows (Table S1, Figure S1), and this pattern is consistent across the genome (Wilcoxon signed rank on mean b p in 100-kb windows: P , 10 215 for both continents). This contrasts with observations in D. melanogaster of higher heterozygosity at lower latitudes (Kolaczkowski et al 2011;Fabian et al 2012;Reinhardt et al 2014). We note that of the four populations, FL has the lowest heterozygosity genome wide, reflecting perhaps more severe drift than the other three populations.…”

“…Second, focusing on SNPs that are strongly differentiated on two continents will, to some degree, mitigate potential false discoveries that may arise as a consequence of sampling error, fine-scale local environmental adaptation, or demography. Such comparative population genomic approaches may inform our understanding of parallelism at various levels from the nucleotide level to gene annotations or pathways and also may provide useful information regarding constraints, repeatability, and diversity of mechanisms of adaptation in these two species.Similar genome-wide studies of differentiation in comparable populations of D. melanogaster (Turner et al 2008;Kolaczkowski et al 2011;Fabian et al 2012;Reinhardt et al 2014) have detected signals of parallel differentiation and, in particular, a strong association of large inversions with allele-frequency differentiation. The prevalence of inversion frequency clines in D. melanogaster is thought to reflect some response to spatially varying selection, but their adaptive significance remains unclear.…”

“…Similar genome-wide studies of differentiation in comparable populations of D. melanogaster (Turner et al 2008;Kolaczkowski et al 2011;Fabian et al 2012;Reinhardt et al 2014) have detected signals of parallel differentiation and, in particular, a strong association of large inversions with allele-frequency differentiation. The prevalence of inversion frequency clines in D. melanogaster is thought to reflect some response to spatially varying selection, but their adaptive significance remains unclear.…”

Evolutionary toxicology in an omics world

“…While that is a benefit of full‐genome population resequencing, it is not always necessary when examining large genetic sweeps in populations. Pool‐seq has been successfully applied in selection studies and the description of transposable element migration in several Drosophila species (Boitard, Schlotterer, Nolte, Pandey, & Futschik, 2012; Fabian et al., 2012; Kofler, Betancourt, & Schlotterer, 2012; Orozco‐TerWengel et al., 2012). This method may allow evolutionary toxicology genomic comparisons to be performed more economically.…”

A hidden Markov model approach for simultaneously estimating local ancestry and admixture time using next generation sequence data in samples of arbitrary ploidy

“…Evidence suggests spatially varying selection affects the distribution of genetic variants [40][41][42][43][44][45]. Furthermore, strong epistatic reproductive isolation barriers partially isolate individuals from northern and southern populations along this ancestry cline [46,47].…”