Genetic dissection of a major polymorphism underlying population divergence in sexually selected pheromones in Drosophila serrata

Abstract

With the advent of QTL mapping in the late 1980s, evolutionary geneticists have actively dissected the genetic basis of adaptive phenotypes. In recent times, advances in whole genome sequencing have allowed for finer scale mapping of traits that have diverged due to natural selection. These relatively inexpensive sequencing technologies have also greatly facilitated adaptive trait dissection in non-model species that exhibit especially interesting patterns of adaptation. One class of trait that has largely escaped the attention of the next generation ecological and evolutionary genomics research programme, are sexually-selected traits. Sexual selection is a strong form of directional selection in nature and is thought to be responsible for the evolution of elaborate sexual ornaments and armaments. However we still know comparatively little of the genetic basis of such traits.The cuticular hydrocarbons (CHCs) of Drosophila serrata provide an opportunity for dissecting the divergence of sexually selected traits. Populations along the eastern Australian coast exhibit latitudinal variation in these traits in association with climatic factors and consistent with the action of divergent natural selection. Under experimental settings, divergent sexual as well as natural selection has been implicated in the evolution of CHCs. Natural populations of D. serrata along the northern part of the Eastern Australian coast have recently been observed to exhibit a polymorphism in three of their CHC compounds representing the shortest carbon chains; 5,9-tetracosadiene (5,9-C 24 ), 5,9-pentacosadiene (5,9-C 25 ) and 9-pentacosene (9-C 25 ). One class of phenotype only expresses these three compounds in trace amounts ('low' phenotype) whereas the other has normal levels ('high' phenotype). These short-chained CHCs also exhibit strong genetically-based latitudinal clines up to, but not beyond, 20 degrees south of the equator. Based on both traditional QTL and modern sequence-based genomic mapping approaches, the aim of this study was to dissect the genetic basis of the polymorphism in D. serrata CHCs and to examine its adaptive significance within the context of sexual and natural selection.Through F2 QTL mapping based on a cross between two inbred lines, from the opposite ends of the D. serrata CHC cline, one a 'low' phenotype and the other a 'high' phenotype, the genetic basis of all CHCs in this species was mapped to twenty two overlapping QTLs on chromosomes 2 and 3.The short-chain CHC polymorphism was traced to two major effect recessive QTLs on the right arm of chromosome 3, which including their interaction, accounted for more than 70% of the variance in the polymorphism (Chapter 2). Fine mapping of this major polymorphism was then conducted using next generation DNA sequencing and bulk segregant analysis of an advanced F60 cross of the same founding lines. Bulk segregant analysis revealed a single peak of genetic differentiation on chromosome 3R (~20kb), harbouring three adjacent fatty acyl-CoA reductase ii genes (Cha...