Collaborative proposal: Evaluating phenotypic plasticity's role in adaptive evolution

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Many organisms can respond to changes in their environment by dramatically altering their morphology, behavior, or physiology, and the widespread occurrence of this ability has provoked a spirited debate. On the one hand, many biologists maintain that the flexibility to change appearance, behavior or physiology are of no relevance to evolution, because evolution requires genetic change. On the other hand, a growing number of researchers have suggested that such flexibility plays a critical role in evolution by jump-starting genetic change. This research will help resolve this controversy by investigating whether changes in appearance, behavior and/or physiology precede (and enable) the evolutionary origins of major, new, genetically-encoded features. The research will specifically evaluate whether pre-existing, diet-induced flexibility has contributed to the evolution of a novel, complex body form in spadefoot frogs. Thus, not only will this research provide important insights into the evolutionary process, it will also shed new light onto one of biology's enduring mysteries: how complex features originate. The research will also promote educational outreach by training school children and undergraduate students and by organizing public talks at museums.This research will test the Plasticity-First hypothesis of adaptive evolution. To do so, the proposed research will focus on spadefoot toads. Like most frogs, tadpoles in the genus Scaphiopus develop only into a typical 'omnivore' morph. By contrast, tadpoles in the genus Spea exhibit striking plasticity: depending on their diet, they develop into either omnivores or a novel 'carnivore' morph. Interestingly, certain components of this distinctive carnivore morph can be diet-induced in Scaphiopus. Moreover, some Spea populations have secondarily lost the omnivore-carnivore plasticity and become monomorphic. Indeed, in some populations, selection has favored the near fixation of the carnivore morph. Thus, as a group, spadefoots appear to represent different stages in the evolution of the novel carnivore morph: from its possible initial induction (in Scaphiopus), to its refinement as part of a novel developmental 'switch' (in many Spea populations), to its ultimate fixation (in some Spea populations). The planned research will evaluate whether this novel carnivore phenotype arose through plasticity-first evolution by contrasting development, genetic variation, and performance in different species/populations that serve as different evolutionary stages in the origins of this distinctive form. In doing so, the research will evaluate the critical predictions of the plasticity-first hypothesis. This research will thereby help to clarify plasticity's role in evolutionary innovation and provide a roadmap for others to test the plasticity-first hypothesis.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.