Sexual signal loss: The link between behaviour and rapid evolutionary dynamics in a field cricket

Abstract

Sexual signals may be acquired or lost over evolutionary time, and are tempered in their exaggeration by natural selection. In the Pacific field cricket, Teleogryllus oceanicus, a mutation ("flatwing") causing loss of the sexual signal, the song, spread in <20 generations in two of three Hawaiian islands where the crickets have been introduced. Flatwing (as well as some normal-wing) males behave as satellites, moving towards and settling near calling males to intercept phonotactic females. From 2005 to 2012, we surveyed crickets and their responses to conspecific song, noting the morph and number of males and females before and after experimental playbacks. The three Hawaiian islands consistently contained different proportions of flatwing crickets, ranging from about 90% of males on Kauai to 50% on Oahu to rare on the Big Island of Hawaii. Flatwing and normal-wing males do not appear to differ in responsiveness to playback, a behaviour that should influence the likelihood of a male encountering a phonotactic female. Instead, male and female crickets from populations in which little to no calling song is perceptible during development tended to seek out callers more readily than crickets that developed in noisier environments. Such increased phonotaxis makes females more likely to find either the caller to which they are responding or to encounter a flatwing (or normal male satellite) that has also been attracted to the song. Our evidence suggests that pre-existing behavioural plasticity (manifest as flexible responses to social-particularly acoustic-information in the environment) is associated with the rapid spread of the flatwing trait. Different social environments select for differential success of flatwing or normal-wing males, which in turn alters the social environment itself.

Sexual signal loss in field crickets maintained despite strong sexual selection favoring singing males

“…This proportion is corroborated by the more exhaustive sampling done by Zuk et al. (). Flatwing males made up an even smaller proportion of the population when we raised the progeny of wild mated females in the lab, where they were protected from the selection pressures imposed by the parasitoid fly.…”

“…) and has been maintained for over 50 cricket generations in three Hawaiian populations without going to fixation (Zuk et al. ). Our estimate of the sexual selection that favors singing thus additionally suggests an approximate strength of balancing natural selection that favors the silent, flatwing phenotype.…”

Direct and indirect effects of sexual signal loss on female reproduction in the Pacific field cricket (Teleogryllus oceanicus)

“…Because these silent males lack sound‐producing structures on their forewings, we refer to their phenotype as “ flatwing .” We refer to wild‐type males capable of singing as “ normal‐wing .” Remarkably, several years later an independent mutation in a different region of the X‐chromosome arose on Oahu that yielded a similar silent (flatwing) male morph, and became established at ~50% of the population (Pascoal et al., ; Zuk et al., ). After extremely rapid initial spreads on each island, the proportions of flatwing males in Kauai and Oahu have remained stable over the past decade (Zuk, Bailey, Gray, & Rotenberry, ). The evolutionary loss of male song has introduced two major changes to affected cricket populations.…”

“…If flatwing females have better mating outcomes than normal‐wing females, it could help explain the rapid success of the silencing mutation. On the other hand, if the flatwing allele is associated with lower reproductive outcomes for females, it could help explain why the mutation has not swept to fixation in Kauai, where ~90% of adult males in the wild exhibit the flatwing phenotype but callers still remain at low frequency (Zuk et al., ). Second, we examined indirect genetic effects of sexual signal loss on female investment in reproductive tissues by exposing female T. oceanicus to either a song‐rich (mimicking an ancestral population with many normal‐wing males) or song‐less environment (which could occur due to either a lack of males, or the presence of many flatwing males) during late juvenile stages and early adulthood.…”

Limited flexibility in female Pacific field cricket (Teleogryllus oceanicus) exploratory behaviors in response to perceived social environment

“…A few years later, an independent mutation that yields a similar phenotype became established on Oahu (Pascoal et al., ). Today, ~90% of males on Kauai and ~50% of males on Oahu are flatwing (Pascoal et al., ; Zuk, Bailey, Gray, & Rotenberry, ). Because flatwing males lack the wing structures necessary to produce song, they are protected from parasitism by the fly, but are unable to call to attract females.…”