How Repeatable is Adaptive Evolution? Testing What Promotes Rapid Adaptation in a Replicated Natural System

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Organisms often encounter dramatic pressures in their environment, and over the long term populations under pressure must evolutionarily adapt, migrate or go extinct. Independent adaptations to the same selection pressure provide compelling evidence for the repeatability of adaptive evolution, but how quickly populations can adapt to extreme pressure is a contentious issue. The factors that promote recurrent, rapid evolution in such cases can be difficult to disentangle because it is very unlikely and very rare for researchers to be able to observe the earliest stages of adaptation. Mutations do not occur frequently, and when they do they are not likely to be beneficial. Our project overcomes these obstacles using rapidly evolving crickets (Teleogryllus oceanicus) in a "natural laboratory" on the Hawaiian archipelago. We will evaluate the drivers of rapid adaptation by testing how and why a recent adaptation, male silence, has independently evolved repeatedly under pressure from deadly, eavesdropping parasitoid flies. Evolutionary dynamics can differ during the early stages of adaptation, and the cricket system is unique because we can study populations in which adaptive variants appeared only 15 years ago. In addition, we have recently discovered multiple variants of silent cricket in a geographic mosaic of populations, which allows us to test how mutation, migration, and selection interact to drive repeated rapid adaptation.The project first focuses on selection imposed by the flies, measuring its strength and the geographic pattern of associated phenotypic variation, then characterizes the convergent mutants. It joins all evolutionary processes in a population genomics framework, incorporating migration and selection by modelling selective sweeps at various spatial scales (within populations, across populations within islands, and across the archipelago). Our results will provide a clearer understanding of factors limiting or promoting recent, rapid adaptation, and importantly their relative roles and how they interact. The project will contribute to resolving debate over the strength of selection required to provoke rapid adaptation, and basic information we generate about selection, mutation and migration in this system will inform the general processes of convergent evolution and rapid adaptation in other systems.