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

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.

Diversification of doublesex function underlies morph-, sex-, and species-specific development of beetle horns

“…These observations parallel in part earlier findings in Nasonia wasps, in which differential dsx expression in males has been proposed to underlie species-specific differences in male wing size (13). However, dsx expression in male Nasonia differs constitutively between species, whereas in male O. taurus it appears to be altered facultatively in response to nutrition.…”

“…Third, recent studies have also revealed that dsx is a nexus for the evolution of sexually dimorphic traits; all cases understood at the molecular level involve either changes in cis-regulatory sequences of dsx target genes (11,12) or changes in the expression of dsx itself (13,14). In addition, the recent finding that developing Drosophila are mosaic for dsx expression-and thus are mosaic for the potential for sexual differentiation-has led to increased appreciation for the potential of evolution through tissuespecific changes in dsx activity (15).…”

The Genetic Basis of Rapidly Evolving Male Genital Morphology inDrosophila

“…Evolution at loci with sex-biased expression affects speciesspecific morphology in some insect traits (Barmina and Kopp 2007;Loehlin et al 2010;Wasik et al 2010). The posterior lobe is a male-specific morphological trait, thus the genes important for specifying differences in posterior lobe morphology may show male-biased expression.…”

“…The first is the sex determination gene dsx, which directs sex-specific development of the genitalia in Drosophila by regulating the action of patterning genes and Hox genes in the genital imaginal disc (Sánchez and Guerrero 2001;Christiansen et al 2002;Estrada et al 2003). Differences in dsx expression level have been implicated in species-specific wing size differences in male Nasonia wasps (Loehlin et al 2010). The second noteworthy gene is Pox neuro (Poxn), which encodes a transcription factor necessary for proper development of the male genitalia in D. melanogaster.…”

“…Both approaches have been successful in identifying genes, genetic pathways, and regulatory differences underlying species-specific morphologies in a variety of taxa including plants (Luo et al 1996;Doebley et al 1997;Da et al 1999;Galego and Almeida 2002;Hubbard et al 2002;Corley et al 2005;Clark et al 2006;Hay and Tsiantis 2006), cnidarians (Khalturin et al 2008), arthropods (Stern 1998;Sucena and Stern 2000;Beldade et al 2002;Ronshaugen et al 2002;Wittkopp et al 2003Wittkopp et al , 2009Reed and Serfas 2004;Gompel et al 2005;Prud'homme et al 2006;Barmina and Kopp 2007;McGregor et al 2007;Moczek and Rose 2009;Hrycaj et al 2010;Loehlin et al 2010;Shirataki et al 2010;Wasik et al 2010;Werner et al 2010;Wasik and Moczek 2011), echinoderms (Hinman and Davidson 2007), fish (Fraser et al 2009), birds (Abzhanov et al 2004(Abzhanov et al , 2006Mallarino et al 2011), mammals (Cretekos et al 2008), as well as morphological differences between more distantly related groups of organisms such as agnathans and gnathostomes (Meulemans and Bronner-Fraser 2002;McCauley and Bronner-Fraser 2006).…”