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

Daniel K Fabian,Martin Kapun,Paul S Schmidt,Christian Schlötterer,Viola Nolte,Thomas Flatt,Robert Kofler

doi:10.1111/j.1365-294x.2012.05731.x

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.

Highlights

Unravelling the genetic basis of adaptive change in natural populations is one of the most fundamental aims ofD
While this method has been criticized, for instance because large genetic differentiation can be due to demographic factors independent of selection, it has generally proved to be quite robust against effects of demography and relatively successful at identifying putatively adaptive loci (Schlotterer 2002; Beaumont & Balding 2004; Beaumont 2005; Stinchcombe & Hoekstra 2007; Nosil et al 2009; Kolaczkowski et al 2011)
Since the major cosmopolitan inversions are thought to explain a substantial proportion of clinal variation (Krimbas & Powell 1992; De Jong & Bochdanovits 2003; Rako et al 2006; Hoffmann & Weeks 2007), we examined their contribution to differentiation

Summary

Introduction

Unravelling the genetic basis of adaptive change in natural populations is one of the most fundamental aims ofD. One common approach for identifying polymorphisms that might be targets of spatially variable selection is to search for alleles that show exceptionally strong differentiation among geographically distinct populations: strong outlier ‘signals’ are taken to be indicative of selection and local adaptation relative to background ‘noise’ caused by gene flow and drift (Lewontin & Krakauer 1973, 1975; Black et al 2001; Luikart et al 2003; Beaumont 2005; Akey 2009; Akey et al 2010). Because clines are often highly repeatable across different geographical regions, populations and species, both at the level of phenotypic and genetic change, they are widely thought to reflect spatially varying selection (Mayr 1963; Dobzhansky 1970; Endler 1977; Barton 1983, 1999)

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