Non-Coding Changes Cause Sex-Specific Wing Size Differences between Closely Related Species of Nasonia

David W Loehlin,M Victoria Cattani,Deodoro C S G Oliveira,John H Werren,Michael E Clark,Rachel Edwards,Leo W Beukeboom,Eveline C Verhulst,Jonathan D Giebel,Monica Muñoz-Torres,Louis Van De Zande,David L Stern

doi:10.1371/journal.pgen.1000821

David W Loehlin, M Victoria Cattani + Show 10 more

Open Access

https://doi.org/10.1371/journal.pgen.1000821

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Abstract

The genetic basis of morphological differences among species is still poorly understood. We investigated the genetic basis of sex-specific differences in wing size between two closely related species of Nasonia by positional cloning a major male-specific locus, wing-size1 (ws1). Male wing size increases by 45% through cell size and cell number changes when the ws1 allele from N. giraulti is backcrossed into a N. vitripennis genetic background. A positional cloning approach was used to fine-scale map the ws1 locus to a 13.5 kilobase region. This region falls between prospero (a transcription factor involved in neurogenesis) and the master sex-determining gene doublesex. It contains the 5′-UTR and cis-regulatory domain of doublesex, and no coding sequence. Wing size reduction correlates with an increase in doublesex expression level that is specific to developing male wings. Our results indicate that non-coding changes are responsible for recent divergence in sex-specific morphology between two closely related species. We have not yet resolved whether wing size evolution at the ws1 locus is caused by regulatory alterations of dsx or prospero, or by another mechanism. This study demonstrates the feasibility of efficient positional cloning of quantitative trait loci (QTL) involved in a broad array of phenotypic differences among Nasonia species.

Highlights

Somatic sexual differentiation is an ancient feature of animals, yet sex differences in morphological traits can evolve rapidly
While protein-coding changes have been the focus of most historical studies of phenotypic evolution, it has been argued that changes to non-coding cis-regulatory elements may be more important, as they are crucial to the spatiotemporal control of gene expression in development and can change with potentially fewer pleiotropic effects on other processes [4,5]
The giraulti allele at this locus was shown to increase wing size by approximately 60% when introgressed from N. giraulti into a N. vitripennis background, accounting for 44% of the species difference

Summary

Introduction

Somatic sexual differentiation is an ancient feature of animals, yet sex differences in morphological traits can evolve rapidly. There have been few studies investigating the genetic and molecular basis of the recent evolution of morphological differences between species, due in part to the difficulty of conducting genetic analyses in diverged species that are often reproductively incompatible. An active debate concerns whether the evolution of differences between species are due primarily to cis-regulatory or protein coding changes (e.g., [4,5,6,7,8]). Additional genetic studies of phenotypic evolution in recently diverged species are needed to help reveal the processes by which new morphologies evolve and the relative roles of cis-regulatory versus protein-coding changes in morphological evolution. We investigate the genetic basis of male-specific differences between two species of Nasonia, N. vitripennis and N. giraulti.

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Findings

Materials and Methods