Genome-Wide Association Study on Male Genital Shape and Size in Drosophila melanogaster.

Baku Takahara,Kazuo H Takahashi,Alistair P Mcgregor

doi:10.1371/journal.pone.0132846

Abstract

Male genital morphology of animals with internal fertilization and promiscuous mating systems have been one of the most diverse and rapidly evolving morphological traits. The male genital morphology in general is known to have low phenotypic and genetic variations, but the genetic basis of the male genital variation remains unclear. Drosophila melanogaster and its closely related species are morphologically very similar, but the shapes of the posterior lobe, a cuticular projection on the male genital arch are distinct from each other, representing a model system for studying the genetic basis of male genital morphology. In this study, we used highly inbred whole genome sequenced strains of D. melanogaster to perform genome wide association analysis on posterior lobe morphology. We quantified the outline shape of posterior lobes with Fourier coefficients obtained from elliptic Fourier analysis and performed principal component analysis, and posterior lobe size. The first and second principal components (PC1 and PC2) explained approximately 88% of the total variation of the posterior lobe shape. We then examined the association between the principal component scores and posterior lobe size and 1902142 single nucleotide polymorphisms (SNPs). As a result, we obtained 15, 14 and 15 SNPs for PC1, PC2 and posterior lobe size with P-values smaller than 10-5. Based on the location of the SNPs, 13, 13 and six protein coding genes were identified as potential candidates for PC1, PC2 and posterior lobe size, respectively. In addition to the previous findings showing that the intraspecific posterior shape variation are regulated by multiple QTL with strong effects, the present study suggests that the intraspecific variation may be under polygenic regulation with a number of loci with small effects. Further studies are required for investigating whether these candidate genes are responsible for the intraspecific posterior lobe shape variation.

Highlights

Male genital structures of animals with internal fertilization and promiscuous mating systems have been one of the most diverse and rapidly evolving morphological traits, whereas female genital structures have been relatively invariant during evolution [1]
Because the DGRP strains were established from a single local population (Raleigh, USA), the genetic variation in the posterior lobe shape among the DGRP strains indicates sufficient genetic variation in the intraspecific posterior lobe shape even in a single wild population of D. melanogaster
Those single nucleotide polymorphisms (SNPs) were distributed to all the major chromosomes of D. melanogaster, whereas in the study by McNeil et al [14], the three quantitative trait loci (QTL) for posterior lobe shape were found only on the left arms of the 2nd and 3rd chromosomes and the centromere doi:10.1371/journal.pone.0132846.g007

Summary

Introduction

Male genital structures of animals with internal fertilization and promiscuous mating systems have been one of the most diverse and rapidly evolving morphological traits, whereas female genital structures have been relatively invariant during evolution [1]. Drosophila melanogaster, one of the best studied model insects, and its closely related species are morphologically very similar; the shapes of the posterior lobe, a cuticular projection on the male genital arch are distinct from each other [9]. & Kamimura [12] have revealed that posterior lobes with allospecific features caused more severe damage to females than those with conspecific features, implying a potential coevolution of male and female genital structures through sexual selection. The association between the male posterior lobe morphology and mating success is still under investigation, posterior lobes of the D. melanogaster species group represent a model system for studying reproductive isolation via the lock-and-key mechanism of secondary sexual structures

Methods

Results

Conclusion