Genetic architecture of male courtship behavior differences in the parasitoid wasp genus Nasonia (Hymenoptera; Pteromalidae)

Abstract

Very little is known about the genetic basis of behavioral variation in courtship behavior, which can contribute to speciation by prezygotic isolation of closely related species. Here, we analyze the genetic basis and architecture of species differences in the male courtship behavior of two closely related parasitoid wasps Nasonia vitripennis and N. longicornis. Both species occur microsympatrically in parts of their ranges and have been found in the same host pupae. Despite strong postzygotic isolation mechanisms between these two Nasonia species, viable hybrid females can be produced in the laboratory if both species are cured of their Wolbachia endosymbionts. We used haploid F2 hybrid males derived from virgin F1 hybrid females of two independent mapping populations to study the genetic architecture of five quantitative and two qualitative components of their courtship behavior. A total of 14 independent Quantitative Trait Loci (QTL) were found in the first mapping population (320 males), which explained 4-25% of the observed phenotypic variance. Ten of these QTL were confirmed by a second independent mapping population (112 males) and no additional ones were found. A genome-wide scan for two-loci interactions revealed many unique but mostly additive interactions explaining an additional proportion of the observed phenotypic variance. Courtship QTL were found on all five chromosomes and four loci were associated with more than one QTL, indicating either possible pleiotropic effects of individual QTL or individual loci contributing to multiple courtship components. Our results indicate that these two evolutionary young species have rapidly evolved multiple significant phenotypic differences in their courtship behavior that have a polygenic and highly interactive genetic architecture. Based on the location of the QTL and the published Nasonia genome sequence we were able to identify a series of candidate genes for further study.