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

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

Genetics of size and shape evolution in Nasonia

Thesis (Ph. D.)--University of Rochester. Dept. of Biology, 2012. Chapter 2 was co-written with John H. Werren and Deodoro C. S. G. Oliveira. Chapters 3 and 4 were co-written with Werren.My research addresses a fundamental question in biology: What genes and genetic changes are responsible for size and shape differences between species? In Chapter 1, I review the genetics of growth and what patterns might be found in the genetic changes that underlie the evolution of size and shape differences. While much is known about growth-regulating genes and their roles in human disease, one aspect is not well understood: which parts of the growth gene network specify the sizes and shapes of organs. Naturally occurring differences in size and shape, especially species differences, can be used to answer this question. An analysis of the small number of studies of organ size evolution, including my own work, points to a prominent role for cis-regulatory changes to signaling genes. This suggests that these upstream parts of the growth gene network are where many aspects of size and shape are specified. I next focus on determining the genetic basis of huge differences in wing size between two closely related wasps, Nasonia vitripennis and N. giraulti. In Chapter 2, I (along with collaborators) identify the genetic basis of the wing-size1 (ws1) quantitative trait locus (QTL), which changes Nasonia male wing area by 45% with no effect on females. Ws1 maps to a noncoding cis-regulatory element adjacent to the doublesex (dsx) gene and causes wing-specific changes in dsx expression. The capacity for cis-regulatory elements to give a gene new sex- and tissue-specific expression may explain how a conserved sex-signaling gene became recruited to regulate organ size. Chapters 3 and 4 focus on a Nasonia wing shape QTL, widerwing (wdw). In Chapter 3 I report the identification, morphological effects and evolution of wdw in four Nasonia species. In Chapter 4 I report the genetic basis of wdw. The wdw QTL maps down to one gene: the wasp version of unpaired (upd), a Drosophila cell-proliferation regulator in the JAK/STAT signaling pathway. Multiple changes around this upd-like gene are involved, each of which causes spatiotemporal differences in upd-like expression and corresponding spatial changes in wing size, revealing that wdw is a hotspot of wing size evolution