Females often prefer to mate with males that produce extravagant signals. Signals that increase a male's probability of attracting a female, however, can also increase the probability of attracting predators. Relatively little is know about the effect of predation on the evolution of male and female mating behavior. In the variable field cricket, Gryllus lineaticeps, females prefer male songs that contain faster and longer chirps. These song types, however, are also more likely to attract phonotactic parasitoid flies (Ormia ochracea). The flies deposit larvae on singing males, the larvae burrow into the cricket and feed for ten days, then the larvae emerge from the cricket and pupate, killing the cricket. Because the flies prefer the same song types as female crickets, preferred males have a higher risk of fly predation. In addition, females experience a greater risk of fly predation when they are near preferred males, and they likely experience a greater risk of fly predation when they mate with multiple males. This project will examine the effect of fly predation on the evolution of male and female reproductive behavior. Specifically, it will compare seven cricket populations attacked by the flies and seven cricket populations that are not attacked by the flies. Behavioral measures in the two populations will include male singing behavior, female responses to male song, female repeated and multiple mating, male-provided direct benefits, and the reliability of male signals of benefit quality. All crickets tested will be reared in the common environment of the laboratory, which will ensure that any detected differences between parasitized and non-parasitized populations are genetically based. This study will provide unique information on the factors that affect the evolution of male and female reproductive behavior. Broader impacts: Field work will be conducted at several protected reserves and biological field stations. The project will provide research training for at least four undergraduate students per year.
Intellectual Merit Males often produce elaborate signals to attract females because females prefer to mate with males with elaborate signals. These signals, however, can increase male predation risk, and approaching males that attract predators can increase female predation risk. Predation is thus thought to limit the evolution of male signals and female signal preferences, although only a small number of studies have explicitly tested this hypothesis. We tested the effects of predation on the evolution of male signals and female preferences in the variable field cricket, Gryllus lineaticeps. In this animal, females prefer male songs with higher chirp rates and longer chirp durations because males with these song types transfer seminal fluid products that increase female fecundity and lifespan. Male song, however, also attracts the parasitoid fly Ormia ochracea, and male songs with higher chirp rates and longer chirp durations are more likely to attract flies. As a result, males that produce preferred song types are more likely to be killed by the flies. Females that prefer these song types are also more likely to be killed by the flies because they can be parasitized when they approach preferred males. To test the evolutionary effects of fly parasitism, we compared male and female reproductive behavior among 11 populations, six of which are attacked by the flies, five of which are not attacked by the flies. In order to control for environmental and non-genetic maternal effects on male and female behavior, we tested the behavior of lab-reared crickets whose parents were also reared in the lab. We found that males from high risk populations do not sing less than males from low risk populations, and that males from high risk populations produce more attractive and riskier song types. We also found that females from high risk populations are less responsive to male song than females from low risk populations, and that females from high risk populations express stronger, riskier preferences. These results reject the hypothesis that predation limits the evolution of male song and female song preferences in this species. There are at least two, non-mutually exclusive hypotheses that can potentially explain our counterintuitive results. (1) Periodic predation may favor the evolution of riskier male signals and riskier female preferences. Because fly parasitism only occurs during the latter stages of the breeding season, selection may favor the evolution of very attractive song types because there is a premium on mating before the flies start orienting to male song. Similarly, selection may favor strong female chirp rate preferences because there is a premium on producing the maximum number of eggs before the flies start orienting to male song. (2) Predation may drive chase away sexual selection. Predation costs may favor the evolution of reduced female responsiveness to male song because less responsive females mate less frequently and thus have a low risk of parasitism. Reduced female responsiveness to male signals may in turn favor more elaborate male signals because females with a high response threshold will only respond to the most attractive signal types. Broader Impacts This project provided research training for a postdoctoral scholar, multiple graduate students, and multiple undergraduate students. In addition, it supported multiple outreach activities for grade school and high school students (and their parents), including a workshop for the University of Nebraska Women in Science Conference.
