Abstract
Unraveling the genetic architecture of adaptive phenotypic divergence is a fundamental quest in evolutionary biology. In Drosophila melanogaster, high-altitude melanism has evolved in separate mountain ranges in sub-Saharan Africa, potentially as an adaptation to UV intensity. We investigated the genetic basis of this melanism in three populations using a new bulk segregant analysis mapping method. We identified 19 distinct QTL regions from nine mapping crosses, with several QTL peaks overlapping between two or all populations, and yet different crosses involving the same melanic population commonly yielded distinct QTL. The strongest QTL often overlapped well-known pigmentation genes, but we typically did not find wide signals of genetic differentiation (FST) between lightly and darkly pigmented populations at these genes. Instead, we found small numbers of highly differentiated SNPs at the probable causative genes. A simulation analysis showed that these patterns of polymorphism were consistent with selection on standing genetic variation. Overall, our results suggest that, even for potentially simpler traits like pigmentation, the complexity of adaptive trait evolution poses important challenges for QTL mapping and population genetic analysis.
Highlights
Unraveling the genetic architecture of adaptive phenotypic divergence is a fundamental quest in evolutionary biology
In tropical Africa, which harbors the ancestral range of the species (David and Capy 1988; Pool et al 2012), unusually dark populations have been discovered in different mountain ranges (Pool and Aquadro 2007; Bastide et al 2014)
The pigmentation of African D. melanogaster is best predicted by UV intensity, offering a plausible selective agent to drive the recurrent evolution of melanism (Bastide et al 2014)
Summary
Unraveling the genetic architecture of adaptive phenotypic divergence is a fundamental quest in evolutionary biology. Genome-wide association studies (GWAS) of female abdominal pigmentation variation ( measuring the black portion of the seventh, posterior-most abdominal segment) within four temperate populations all revealed major effects of the two melanin synthesis genes tan and ebony and the transcription factor bric-a-brac 1 (bab1), other minor effect genes were detected (Bastide et al 2013; Dembeck et al 2015; Endler et al 2016). In one population (Uganda), a haplotype carrying a series of causative cis-regulatory mutations at ebony was a major contributor to melanism ( the background color of the fourth abdominal segment) and showed evidence of a strong partial selective sweep (Pool and Aquadro 2007; Rebeiz et al 2009). Genetic differentiation at one locus (ebony in Ethiopia) was found to be consistent with natural selection acting on standing genetic variation
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