Evolution of sexually dimorphic pheromone profiles coincides with increased number of male‐specific chemosensory organs in Drosophila prolongata

Abstract

Binary communication systems that involve sex‐specific signaling and sex‐specific signal perception play a key role in sexual selection and in the evolution of sexually dimorphic traits. The driving forces and genetic changes underlying such traits can be investigated in systems where sex‐specific signaling and perception have emerged recently and show evidence of potential coevolution. A promising model is found in Drosophila prolongata, which exhibits a species‐specific increase in the number of male chemosensory bristles. We show that this transition coincides with recent evolutionary changes in cuticular hydrocarbon (CHC) profiles. Long‐chain CHCs that are sexually monomorphic in the closest relatives of D. prolongata (D. rhopaloa, D. carrolli, D. kurseongensis, and D. fuyamai) are strongly male‐biased in this species. We also identify an intraspecific female‐limited polymorphism, where some females have male‐like CHC profiles. Both the origin of sexually dimorphic CHC profiles and the female‐limited polymorphism in D. prolongata involve changes in the relative amounts of three mono‐alkene homologs, 9‐tricosene, 9‐pentacosene, and 9‐heptacosene, all of which share a common biosynthetic origin and point to a potentially simple genetic change underlying these traits. Our results suggest that pheromone synthesis may have coevolved with chemosensory perception and open the way for reconstructing the origin of sexual dimorphism in this communication system.

The evolution of sexually dimorphic cuticular hydrocarbons in blowflies (Diptera: Calliphoridae)

“…flavifrons ) in the form of multiple qualitatively distinct profile types within the same populations. These distinct types might correspond to differences in individual diet (Fedina et al., 2012) or represent intra‐sexual CHC polymorphisms (Bagnères & Morgan, 1990; Luo et al., 2019; Wurdack, 2015). However, they most likely correspond with age, as it is well known that blowflies show stark age‐specific changes in CHC expression (Trabalon et al., 1992; Roux et al., 2008; Pechal et al., 2014; Braga, Pinto, de Carvalho Queiroz, & Blomquist, 2016; Paula et al, 2016; Bernhardt, Pogoda, Verhoff, Toennes, & Amendt, 2017).…”

Advances in deciphering the genetic basis of insect cuticular hydrocarbon biosynthesis and variation

“…Furthermore, CHCs are principal signals in chemical communication (Carlson et al 1971 ; Blomquist and Bagnères 2010 ). As versatile semiochemicals, they can encode and transmit a wide variety of information including but not limited to reproductive status (e.g., Smith and Liebig 2017 ), species affiliation (e.g., Shahandeh et al 2018 ), sex (e.g., Luo et al 2019 ), age (e.g., Heuskin et al 2014 ), and social rank (e.g., Honorio et al 2019 ). Moreover, in eusocial insects, CHCs are fundamental as the major nestmate and caste recognition cues (Leonhardt et al 2016 ).…”

“…Evolutionary genetic studies on CHC biosynthesis also need to account for sex-specific differences in the regulation of CHC biosynthesis (e.g., Foley et al 2007 ; Dembeck et al 2015 ; Luo et al 2019 ). Despite sharing the same genes in principle, sexes can show pronounced differences in their CHC profiles, qualitatively as well as quantitatively (e.g., Buellesbach et al 2013 ; Berdan et al 2019 ; Berson et al 2019a ).…”

Social Behavior, Ovary Size, and Population of Origin Influence Cuticular Hydrocarbons in the Orchid Bee Euglossa dilemma

“…This scenario is supported by the finding that all behavioral groups, closely related females, and newly emerged females can exhibit both chemotypes (A and B). Furthermore, these chemotypes differ primarily in the relative abundance of two alkenes that are part of a homologous series (C27:1 and C29:1), so it is possible that the phenotypic expression of these chemotypes is the result of a relatively simple genetic polymorphism of a desaturase, elongase, or other fatty acid synthesis gene (Luo et al, 2019;Coyne et al, 1999). Alternatively, it could also be that differences in development primarily affect the expression of chemotype.…”