Genomic Invasion and the Role of Behaviour in Rapid Evolution

LAY SUMMARY

I want to catch evolution in the act, and my proposal aims to test what happens to genomes when novel mutations "invade". Such an invasion could occur through spontaneous mutation in a section of DNA that codes for or regulates the activity of a gene, or by migration of genes from another population or species due to hybridization. I am particularly interested in how the ability of an organism to adjust its behaviour depending on the prevailing conditions might compensate for negative effects of such a genomic invasion and facilitate more rapid evolutionary change.

The emergence and spread of new mutations with a selective advantage is at the heart of the evolutionary process, but this process is extraordinarily challenging to observe in a natural system for two reasons: the first is that the likelihood of detecting such a genomic invasion is miniscule because they happen so rarely. The second is that evolutionary change has been thought to occur at a very slow pace, much longer than a researcher's lifetime.

My proposal capitalises on a textbook example of rapid evolution that is occurring right now in the Oceanic field cricket, Teleogryllus oceanicus. Male crickets usually sing to attract females for mating, but in the Hawaiian archipelago, they also attract a deadly parasitoid fly (Ormia ochracea). Recently, a mutation that feminises male wings by erasing sound-producing structures on male wings arose and spread. It is called flatwing, and it exists in two populations and appears to have different genetic origins. My research will work out what, exactly, has changed in the genome of these different populations to cause this mutant male type, and it will test how the rest of the genome has responded. In particular, I will make use of a time-series of genomic DNA collections from the wild to visualise and test how the genes that lie in close physical proximity to the mutation get "swept" along with it, or become homogenized with the rest of the genome. In other words, when the flatwing mutation invaded the T. oceanicus genome, two things may have happened. The first is that genes nearby got dragged along and are now over-represented in the population, and the second is that genes in other parts of the genome produced phenotypic effects that worked particularly well with the mutation, and therefore are more likely to be found in the mutant variety of males than in normal males.

I know from previous work that crickets are sensitive to their social environment, in particular, to the presence or absence of acoustic songs that males produce. Both females and males change their mating behaviour to suit the prevailing social conditions, and I will test the hypothesis that the flatwing mutation was able to spread in response to selection from parasitoids more rapidly because social flexibility enabled crickets to cope with the changed social environment, namely, the silent environment that emerged as flatwings became more numerous. I have devised a cricket tracking setup in the lab, which replicates the wild environment and which I can use to test cricket behaviour and mating success. It involves video and audio recording crickets, and enables me to manipulate the composition of interacting individuals during trials. In this manner, I can vary crickets' social experience, what population they are from, and the relative abundance of the different morphs, to test how social flexibility contributes to the reproductive success of mutant males. Results from these trials stand to illuminate how behaviour interacts with the evolutionary process, and how the rate of evolutionary change can be affected by the social environment and individual organisms' responses to that environment.

Who will benefit:

The research I have outlined in my NERC Independent Fellowship application is centered on questions regarding the evolution of biological diversity, which falls squarely with NERC's biodiversity remit. Aside from the academic beneficiaries I have described elsewhere in this proposal, potential beneficiaries include policy-makers and the wider public. My Pathways to Impact document provides further detail about how I will deliver the benefits of my research to these beneficiaries, plus a detailed timeline of activities to ensure that results of my work are disseminated to UK taxpayers who fund the research, as well as to other academics. In a more general sense, impacts of my work will be immediately available once published, and I have a consistent record of timely publication.

How they will benefit:

The rapid and accelerating loss of biodiversity is a global phenomenon that has the potential to cause negative local impacts within the United Kingdom. Dramatic examples include collapse of fisheries, loss of key pollinators, permanent changes in ecosystem functioning and degradation of the quality of our natural environment. My proposal proposes basic scientific research to examine how genomes respond to invasion of new mutations of large effect. The dynamics of such genomic responses are likely to become increasingly relevant as climate change and anthropogenic disturbance increasingly generate novel selection pressures on wild organisms.

Further, I will track genome evolution in real-time, in natural populations and test longstanding but unresolved hypotheses about the nature of genomic change during rapid evolution and the role of behavioural flexibility in modulating that change. Behaviour could influence two relevant types of evolutionary processes: those that generate biological diversity, and those that maintain it. I expect that findings about causal links between social behaviour and these processes will interest those involved in the drafting and implementation of conservation policy. Anthropogenic changes in the physical environment clearly affect the long-term prognosis for species at risk, but the effects of changes in the social environment are less clear, and I expect data on this topic would be useful for informing "on-the-ground" conservation decisions.

The wider public has a stake in understanding biological diversity, both directly for the reasons mentioned above, and indirectly through quality of life considerations and potential future appropriation of biological resources for beneficial medical or agricultural purposes. In addition, basic insight into the natural world is clearly valued by the UK public: Sir David Attenborough's status as a national treasure attests to this. Such knowledge, however, overwhelmingly stems from the UK's commitment to basic research in the biological sciences, and as such, the information that I expect to gain from my fellowship work will add to this knowledge base. Such work increases the competitiveness of the UK by attracting talented scientists, enhancing the profiles of research institutions, and solidifying the UK's leading global reputation for fostering scientific insight and exchange.