Genetics of divergence in male wing pigmentation and courtship behavior between Drosophila elegans and D. gunungcola

Abstract

Many sex-specific traits involved in mating consist of functionally coordinated morphologies and behaviors. How the components of these complex traits evolve and become coordinated during evolution is unknown. In order to understand how such trait complexes evolve and diversify, we must decipher the genetic underpinnings of their components. In this study, we begin to elucidate the genetic architecture underlying differences in functionally related male pigmentation and behavior between two Asian Drosophila melanogaster group species, D. elegans and D. gunungcola. D. elegans possesses a male-specific wing melanin spot and a stereotypical wing display element in male courtship, whereas D. gunungcola lacks both of these traits. Using reciprocal F1 male hybrids, we demonstrate that the X-chromosome contains a major locus or loci required for wing spot formation and that autosomal loci largely determine the male courtship display. Using phenotypic and genetic analysis of backcross progeny, we further demonstrate that both the wing spot and courtship differences between the two species are polygenic and both depend at least in small part on genetic factors on both the X and the autosomes. Finally, we find that male wing spot size and courtship wing display are highly correlated in backcross progeny, suggesting that linkage or pleiotropy may have been involved in their coordinated evolution.

Rapid evolutionary change in a sexual signal: genetic control of the mutation ‘flatwing’ that renders male field crickets (Teleogryllus oceanicus) mute

“…Among studies searching for large X-effects on sexually selected traits, results are mixed, particularly in QTL analyses, possibly because these studies also identify the epistatic effects of X-linked loci on autosomal loci (Fairbairn and Roff, 2006). Large X-effects have been noted in studies of the inheritance of mating signals and courtship behavior as well as in postzygotic reproductive isolation (Coyne and Orr, 1989;Hollocher and Wu, 1996;Yeh et al, 2006). It remains to be seen whether the sexlimited wing morphology used to produce the song is controlled by genes found on the X-chromosome as well, or whether the flatwing mutation simply interrupts a pathway leading to the normal development of wing structure.…”

“…For instance, wing spot formation and courtship displays in male Drosophila have been identified as polygenic and attributed to the X-chromosome and autosomal loci, respectively (Yeh et al, 2006); cuticular hydrocarbons are polygenic as well (Coyne et al, 1994;Gleason et al, 2005). In swordtail crickets (Laupala; Shaw, 1996) as well as field crickets (Gray and Cade, 1999), male song is a polygenic trait, and it is often the case that closely related species differ only in their songs.…”

Development and evolution of insect pigmentation: Genetic mechanisms and the potential consequences of pleiotropy

“…An association with pigmentation has been described for diverse behaviors, including swarming [48], feeding [49], social dominance [50], mate preference [32], and courtship display [51]. The molecular basis for these associations, as well as the data supporting them, are also varied.…”

“…In Heliconius butterflies, genetic mapping has shown co-segregation of wing color and mate preference phenotypes in interspecific crosses [32], but the mapping resolution was insufficient to discriminate between pleiotropy and genetic linkage. In Drosophila, genetic analysis of wing pigmentation and courtship display indicates a role for both linkage and pleiotropy in the co-evolution of these traits [51].…”

Sexual dimorphism and courtship behavior in Drosophila prolongata

“…In addition to the standard courtship elements in Drosophila, such as orientation, following, wing vibration, and licking (Spieth 1952;Cobb et al 1986;Yamamoto and Koganezawa 2013), males of species that have wing spots perform ''wing display'' in front of the female (Fuyama 1979;Yeh et al 2006), whereas species lacking wing spots do not. Wing spots are associated with wing display in at least seven species that are phylogenetically independent from each other (Yeh et al 2006). As indicated by these examples, the adaptive roles of sexually dimorphic structures can be better understood in the context of related behavior.…”