Quantifying the relative contributions of the X chromosome, autosomes, and mitochondrial genome to local adaptation*

Abstract

During local adaptation with gene flow, some regions of the genome are inherently more responsive to selection than others. Recent theory predicts that X‐linked genes should disproportionately contribute to local adaptation relative to other genomic regions, yet this prediction remains to be tested. We carried out a multigeneration crossing scheme, using two cline‐end populations of Drosophila melanogaster, to estimate the relative contributions of the X chromosome, autosomes, and mitochondrial genome to divergence in four traits involved in local adaptation (wing size, resistance to heat, desiccation, and starvation stresses). We found that the mitochondrial genome and autosomes contributed significantly to clinal divergence in three of the four traits. In contrast, the X made no significant contribution to divergence in these traits. Given the small size of the mitochondrial genome, our results indicate that it plays a surprisingly large role in clinal adaptation. In contrast, the X, which represents roughly 20% of the Drosophila genome, contributes negligibly—a pattern that conflicts with theoretical predictions. These patterns reinforce recent work implying a central role of mitochondria in climatic adaptation, and suggest that different genomic regions may play fundamentally different roles in processes of divergence with gene flow.

Genetic covariances promote climatic adaptation in AustralianDrosophila*

“…; Lasne et al. ), studies conducted since The Millenial Drought (1996–2010) have reported elevated desiccation resistance in temperate populations from southeastern Australia, where desiccation stresses have been particularly intense (Lasne et al., , ; the current study). In light of these observations, our four focal traits are among the best candidates for adaptive divergence by latitude across eastern Australia.…”

“…Australian Drosophila populations have played a key role in studies of climatic adaptation, repeatedly exhibiting genetically based clinal divergence in body size and thermal stress traits, despite strong gene flow across the cline (Kennington et al 2003;Hoffmann and Weeks 2007;Sgrò et al 2010;Hangartner et al 2015;Lasne et al 2018). Although desiccation resistance has shown less consistent clinal divergence than our other focal traits (Hoffmann et al 2001;Lasne et al 2018), studies conducted since The Millenial Drought (1996)(1997)(1998)(1999)(2000)(2001)(2002)(2003)(2004)(2005)(2006)(2007)(2008)(2009)(2010) have reported elevated desiccation resistance in temperate populations from southeastern Australia, where desiccation stresses have been particularly intense (Lasne et al, 2018(Lasne et al, , 2019; the current study). In light of these observations, our four focal traits are among the best candidates for adaptive divergence by latitude across eastern Australia.…”

Robbery in progress: Historical museum collections bring to light a mitochondrial capture within a bird species widespread across southern Australia, the Copperback Quail‐thrush Cinclosoma clarum

“…Recently, sometimes unexpected complexity of sex chromosome markers has been highlighted ( cf . Lasne, van Heerwaarden, Sgrò, & Connallon, 2018; Battey, 2020; Hayes, Barton, & Zeng, 2020). This system offers much to the study of the genomics of differentiation and speciation.…”

Digest: All genomes are not equal: How variation in autosomal, sex chromosome, and mitochondrial genomes contributes to the process of local adaptation*

“…Lasne et al. () explore this problem by investigating trait variation in two divergent populations of Drosophila melanogaster from each end of the eastern Australian latitudinal cline. First, they construct a series of theoretical models to create predictions about the contribution of mitochondrial, autosomal, and sex chromosomes to adaptive trait divergence given different patterns of dispersal and variation in population size and selection strength.…”

“…Although recent work has made predictions about the importance of different genomes for adaptation, namely, the mitochondrial genome (e.g., Camus et al 2017), there is little experimental evidence available for the relative contributions of autosomal chromosomes, sex chromosomes, and mitochondrial genomes to adaptive trait divergence and local adaptation. Lasne et al (2019) explore this problem by investigating trait variation in two divergent populations of Drosophila melanogaster from each end of the eastern Australian latitudinal cline. First, they construct a series of theoretical models to create predictions about the contribution of mitochondrial, autosomal, and sex chromosomes to adaptive trait divergence given * This article corresponds to Lasne, C., B.…”