Preexisting behavior renders a mutation adaptive: flexibility in male phonotaxis behavior and the loss of singing ability in the field cricket Teleogryllus oceanicus

Abstract

Flexibility in behavior and other traits can pave the way for rapid evolutionary change. A wing mutation, “flatwing,” eliminates the ability of >90% of male field crickets (Teleogryllus oceanicus) from one Hawaiian population to produce song to attract females. The morphological change was favored because calling is risky in Hawaii, attracting deadly parasitoid flies. An earlier study suggested that instead of calling, silent flatwing males use satellite behavior, approaching one of the few remaining callers and intercepting females attracted to them. Satellite-like behavior may have existed as a behavioral option prior to the wing mutation, accommodating the loss of singing ability, or behavior may have changed simultaneously with the spread of the mutation. In phonotaxis trials, males from different populations across the crickets’ range varied in the distance at which they settled from the source of broadcast song, behaving more or less like satellites. Anecdotally, we noted satellite behavior in all populations, and importantly, males from the mutated population and its direct ancestor behaved similarly. This suggests that the alternative behavior is not strictly associated with the mutation and instead predated the change in morphology. We hypothesized further that satellite behavior may have been preexisting because it is beneficial under other circumstances, such as poor mating success. Virgin males did not show enhanced phonotaxis relative to multiply mated males, however. We conclude that satellite behavior predated the mutation in wing morphology, providing obligately silent males with an alternative method of locating mates and effectively rendering the wing mutation adaptive. Whereas mating history does not appear to influence phonotaxis behavior in males, other factors such as the acoustic environment and demographic conditions may be important contributors to behavioral decisions during male mate location.