Replicated evolutionary divergence in the cuticular hydrocarbon profile of male crickets associated with the loss of song in the Hawaiian archipelago

Abstract

Female choice based on male secondary sexual traits is well documented, although the extent to which this selection can drive an evolutionary divergence in male traits among populations is less clear. Male field crickets Teleogryllus oceanicus attract females using a calling song and once contacted switch to courtship song to persuade them to mate. These crickets also secrete onto their cuticle a cocktail of long-chained fatty acids or cuticular hydrocarbons (CHCs). Females choose among potential mates based on the structure of male acoustic signals and on the composition of male CHC profiles. Here, we utilize two naturally occurring mutations that have arisen independently on two Hawaiian islands and render the male silent to ask whether the evolutionary loss of acoustic signalling can drive an evolutionary divergence in the alternative signalling modality, male CHC profiles. Q ST -F ST comparisons revealed strong patterns of CHC divergence among three populations of crickets on the islands of Hawaii, Oahu and Kauai. Contrasts between wild-type and flatwing males on the islands of Oahu and Kauai indicated that variation in male CHC profiles within populations is associated with the loss of acoustic signalling; flatwing males had a relatively low abundance of long-chained CHCs relative to the short-chained CHCs that females find attractive. Given their dual functions in desiccation resistance and sexual signalling, insect CHCs may be particularly important traits for reproductive isolation and ultimately speciation.

Rapid evolution and gene expression: a rapidly evolving Mendelian trait that silences field crickets has widespread effects on mRNA and protein expression

“…In T. oceanicus, flatwing segregates as a single-locus trait (Tinghitella, 2008;Pascoal et al, 2014), suggesting relatively simple genetic control. Accumulating evidence suggests that flatwing's rapid response to selection on several Hawaiian islands may be linked to the expression of other traits, including plasticity in female responsiveness to acoustic signals Tinghitella et al, 2009), male reproductive tactics and morphology , immunity (Bailey et al, 2011), locomotion (Balenger & Zuk, 2015) and CHC profiles (Simmons et al, 2014). The overall complexity of biological processes and molecular functions that we found to change either directly or indirectly as a result of the flatwing mutation provides strong counterevidence against the hypothesis that its molecular effects are restricted to only one or a handful of developmental modules.…”

“…Additionally, a recent study found that flatwing males show increased locomotion in response to a lack of social cues in their environment (Balenger & Zuk, 2015) and locomotion-related annotations were also DE in flatwing males in this experiment. Flatwing males also differ constitutively in the composition of their cuticular hydrocarbon (CHC) profiles, with mutant males showing a shift in abundance of long-vs. short-chained hydrocarbons (Simmons et al, 2014).…”

Social cues affect quantitative genetic variation and covariation in animal personality traits

“…; Simmons et al. ), such that natural populations of these crickets experience either acoustic or silent environments.…”

Macronutrients and micronutrients drive trade‐offs between male pre‐ and postmating sexual traits

“…In T. oceanicus , CHCs have been shown to be sexually dimorphic and play an important role in sex recognition and mate choice (Simmons, Thomas, Simmons, & Zuk, ; Thomas & Simmons, ). Males on the Islands of Oahu and Kauai in the Hawaiian archipelago harbour a mutation that renders them unable to sing (Zuk, Rotenberry, & Tinghitella, ), and these “songless” males produced a greater amount of the CHCs that are attractive to females (Simmons, Thomas, Gray, & Zuk, ). These findings suggest that when acoustic signals are not used, males may be able to direct more resources to the expression of attractive CHCs (Thomas, Gray, & Simmons, ).…”