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

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.

We will achieve impact by delivering scientific insight to an audience that benefits from this new knowledge. Three components contribute to effective impact: the audience, the message, and the means of delivering it.

AUDIENCE

We have described above the academic beneficiaries of our research outcomes, so here focus on the wider public and the audience who we will engage through impact activities. We expect that the lay public with an interest in general scientific topics will be tuned to our research findings, which we will promote in the lay media as well as in the scientific literature. In addition, we have developed a plan in conjunction with colleagues at St Andrews to engage a younger generation of scientists to critically consider the upper limits on rapid adaptation. The latter audience will consist of high school pupils at the stage of considering higher education who we will engage through our RAPID (Rapid Adaptation Peer Interaction Development) loan boxes and school outreach activities. The audience will also include their teachers. It is vital that this cohort of students is given the best opportunity to study and to be aware of the potential for pursuing a career in cutting-edge adaptation research, and our loan boxes and outreach plans will help make this happen.

MESSAGE

Human beings are facing a critical need to better understand how populations, species and ecosystems do or do not cope with dramatic environmental pressures. At a basic level, evolutionary processes underlying rapid adaptation in such situations can be difficult to observe and characterise during the earliest stages, particularly in the wild, because of the rarity with which adaptive mutations arise in populations under pressure and the even greater rarity with which researchers discover them. Our study of Hawaiian field crickets provides an exceptional opportunity to capture this process and produce insights that are fundamentally important to society at large: How important is extreme selection? What are its effects? How does it interact with population structure? What accounts for high levels of convergent evolution? In addition to the basic scientific findings our study will produce, empirically testing what factors promote or limit adaptation to new pressure in a compelling natural system will be particularly important for specific public sector activities such as agriculture, climate change mitigation, and natural resource management.

MEANS OF DELIVERY

The mechanisms we will use to deliver research impact are more fully described in our Pathways to Impact. These include: direct engagement with teachers from schools in rural areas through the Teachers Together Conference, developing RAPID loan boxes, engaging with teachers and students by visiting schools, and developing an online presence through a website that can link students, teachers and researchers. We will be aided in this effort by the high profile of the cricket system and the compelling evolutionary phenomena of sexual signal loss under pressure from eavesdroppers. Describing the field cricket system invariably stimulates non-scientists' interest and engagement, and Bailey's past research, supported by NERC, has been featured in media outlets such as National Geographic, the BBC, and the New York Times.