Evolutionary ecological genomics of the great tit

Adaptation lies at the heart of Darwin's theory of evolution. For many years, biologists have tried to identify "adaptive genes" that are responsible for phenotypic changes that enable an organism to adapt to its environment. This research is important not only for understanding how Darwinian evolution comes about, but also for practical reasons. For instance, in a time of rapid environmental change, understanding the mechanisms and genetic basis of adaptation is critical to assessing the potential of wild organisms to respond to selective pressures. Studying adaptation is, however, challenging. It requires the use of rigorous mathematical models to analyse genomic DNA sequences, in order to help us understand how the genome of the organism in question evolves over time, and to identify genes showing unusual characteristics compared to the rest of the genome as a result of their involvement in recent adaptations. Thus far, this theory-based approach has mainly been applied to several well-studied organisms such as humans and fruit flies where the necessary resources are available. More recently, the rapid development of high-throughput DNA sequencing technologies has made it economical and efficient to study the genomes of wild organisms, including those studied by ecologists. In this proposal, we will use the theory-based approach to study a wild songbird, the great tit (Parus major). The great tit has been the focus of classical long-term ecological studies throughout Europe, and has been used to study key topics such as when and how the timing of breeding responds to climate change. We will use high-throughput sequencing technologies to obtain the genome sequences of multiple great tit individuals. By making use of, and further developing, state-of-the-art theoretical models, we will obtain a detailed understanding of how genetic variation is distributed across the great tit genome, and what evolutionary forces have influenced this distribution. This knowledge will enable us to search for genes that are responsible for recent adaptations, and will help us answer important questions such as whether genes affecting ecologically important traits such as the timing of breeding are involved in recent adaptations. In addition, we will examine to what extent the great tit genome differs from those of other birds such as the zebra finch, in order to understand the longer-term evolutionary history of genes of interest. These results will help us bridge the gaps in our knowledge of adaptation and genome evolution in wild great tits. More importantly, the methodology we employ is generic, and can be used to study other wild organisms. Thus, our research will be of interest to biologists working on a wide range of topics.

Birds are of enormous ecological, societal and economical importance. Our research concerns the investigation of fundamental questions about genome evolution, as well as the mechanisms and genetic basis of adaptation, in a classic ecological model organism, the great tit (Parus major). As such, this work represents basic science for which the most direct beneficiaries will be biologists working on evolutionary/population genetics, avian genetics, ecological genetics, and genomics. However, a deeper understanding of the nature of adaptation and genome evolution in wild organisms will facilitate progress in management/conservation of biodiversity and improvement of domesticated species. In addition, our project will provide training in statistics and computer programming, which are widely transferrable skills that are essential for both the academic and commercial sectors. We believe our research will be of interest to the following groups of beneficiaries:

1. The general public. Birds are widely-appreciated organisms, with bird watching being one of the most popular hobbies in the UK. The research being carried out by members of the team, both inside and outside this proposal, will allow us to locate genes in the genome that underlie interesting phenotypic variation, demonstrate how natural selection has acted on these genes, and interpret these findings using knowledge about the ecology and natural history of great tits. These outputs can be turned into accessible stories and provide a route for the public to understanding basic genetic and evolutionary principles, which will spark interest in science and increase awareness of the importance of conserving biodiversity.

2. Policymakers and conservation managers. An accurate understanding of the mechanisms and the genetic basis of adaptation is critical to predicting how organisms respond to changing environments. Our project is directly relevant to this issue. In addition, the genetic data will allow us to infer the dynamics of the population size of the great tit population thousands of years into the past. This will put the knowledge about the population dynamics gathered from long-term ecological studies into a much longer evolutionary timescale. This approach can also be applied to other wild species.

3. Scientists working on economically important domesticated birds. The avian karyotype is highly conserved even between distantly-related species. Thus, insights into genome evolution gathered from our research will be useful for studies of other birds such as chickens. For instance, our methods for detecting genes under positive selection can be used to search for genes that respond to artificial selection. In fact, some methods developed by the PI have already been used by other researchers for this purpose in chicken, rice, and sorghum. Identifying these genes will help to understand the genetic basis of economically important traits, which will in turn enable the design of better breeding programmes to improve productivity.