Why Do Breeders Tolerate Non-breeders In Animal Societies?

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Animal societies in which some individuals forgo their own reproduction and help others to reproduce have long puzzled evolutionary biologists. Such societies are found in a wide variety of animals including ants, bees, wasps, birds, and mammals (including traditional human societies). What is particularly poorly understood is why breeding individuals tolerate non-breeders in their social groups when they are not helpers. This project focuses on this question using clown anemonefish as a model. The project involves a combination of laboratory experiments, field experiments, and molecular genetics to test several hypotheses about the potential benefits to the breeding pair of living in a larger group. The clown anemonefish has become a model system for investigations of social systems due to its tractability in the laboratory and in the field thus this study will inform our understanding of similar social groups which are much less experimentally tractable. The research objectives are integrated with multiple broader impact activities. Undergraduates and graduate students will be trained in various transferable skills, such as experimental design, data collection, data management, statistical modeling, and scientific communication while also learning about animal behavior. High school students from groups underrepresented in STEM will be hosted as project interns and will participate in all aspects of the scientific process. In addition, a proposed book, targeted at a teenage audience, will present animal behavior research and profile animal behavior researchers to improve the general public’s understanding of this field. Animal societies are one of the most remarkable products of evolution, and they have been a focus for tests of evolutionary theory ever since Darwin pointed out the difficulties that some features of societies (e.g., non-breeding and helping strategies) posed for the theory of natural selection. To fully understand these societies, it must be understood both why non-breeders tolerate their situation and why breeders tolerate non-breeders. Frequently, breeders tolerate non-breeders because they help provision offspring or the breeders themselves, but in some canonical vertebrate societies the benefits that breeders accrue from non-breeders are not obvious. The overarching objective of this proposal is to resolve this paradox, investigating why breeders tolerate non-breeders in the clown anemonefish (Amphiprion percula), which has emerged as a model system for marine science. The project will evaluate support for three alternative hypotheses for why breeders will tolerate non-breeders, 1) as a bet-hedging strategy against partner loss; 2) that they provide weak kin-selected benefits; and 3) that they provide mutualist (anemone)-mediated benefits. The project will combine long-term field experiments and laboratory experiments to evaluate these alternatives. In sum, the proposed research will investigate why breeders tolerate non-breeders in societies where the benefits that breeders accrue from non-breeders are hidden, providing new insights into social evolution.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.