Developmental plasticity allows juvenile animals to assess environmental cues and adaptively shape behavioral and morphological traits to maximize fitness in their adult environment. Sexual signals are particularly conspicuous cues, making them likely candidates for mediating such responses. Plasticity in male reproductive traits is a common phenomenon, but empirical evidence for signal-mediated plasticity in males is lacking. We tested whether experience of acoustic sexual signals during juvenile stages influences the development of three adult traits in the continuously breeding field cricket Teleogryllus oceanicus: male mating tactics, reproductive investment, and condition. All three traits were affected by juvenile acoustic experience. Males of this species produce a long-range calling song to attract receptive females, but they can also behave as satellites by parasitizing other males' calls. Males reared in an environment mimicking a population with many calling males were less likely to exhibit satellite behavior, invested more in reproductive tissues, and attained higher condition than males reared in a silent environment. These results contrast with other studies and demonstrate how the effects of juvenile social experience on adult male morphology, reproductive investment, and behavior may subsequently influence sexual selection and phenotypic evolution.

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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.

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.