Genomic responses to rapid environmental change: selection, plasticity and adaptation.

The Earth's environments are changing at an unprecedented rate, and its living organisms will have to adapt or go extinct. For many organisms at least part of any adaptation will likely involve changes in the genetic code of life, the DNA. Evolutionary biologists have long been interested in this process of evolutionary adaptation, although the overwhelming majority of what we know is based on adaptations which developed over thousands or millions of years. This evolution occurs through the process of natural selection, in which some variations between individuals in their DNA make some individuals more successful, and the DNA variations responsible increase slowly in frequency over long time periods. To allow adaptation to anthropogenic environmental change, organisms will need to evolve much more rapidly. This was once thought impossible, but in recent years there has been increasing evidence that it can happen. One mechanism that might contribute to such rapid adaptation is 'phenotypic plasticity': alterations in the form or physiology ('phenotype') of organisms brought about by changes in the environment. Phenotypic plasticity results from changes in the expression of DNA: the way in which the code is read by cells. Traditionally, phenotypic plasticity has not been acknowledged as having any special place in the process of adaptation, but there has been a long-lasting debate about this, especially its contribution to rapid adaptation to environmental change. Phenotypic plasticity might allow organisms to persist in rapidly changing environments, allowing time for changes in the DNA to accrue and produce a better evolutionary match to the new environment. Alternatively, phenotypic plasticity might indicate that organisms are struggling to cope, which might actually engender stronger natural selection on the DNA. Hitherto, these different models for adaptation have been difficult to test, but advances in modern technology mean that changes in both the DNA code and its expression can be measured with great accuracy.

In this project we will take advantage of this new technology to examine the process of rapid adaptation to short term environmental change. We will do so by making replicated introductions of marine three-spined stickleback into freshwater ponds, and recording changes in the DNA code and its expression during the earliest stages of adaptation. Stickleback are small fish, common in oceans across the northern hemisphere. They have colonised and adapted to freshwater innumerable times, establishing populations in lakes and rivers after the end of the last ice age. Changes in the DNA of stickleback that have accrued during this 10,000 years of long-term adaptation to freshwater have been exceptionally well documented. It is also well known that stickleback can adapt very quickly to freshwater, with significant changes in phenotype, and even some genes, occurring within one to ten years. However, the patterns of short-term changes in the DNA and its expression are poorly understood. We will document how the expression of genes alters following introduction to freshwater, and what kinds of changes take place in the underlying DNA. By quantifying correlations between the ability of fish to control the salt in their body when put in seawater, and variations in their underlying DNA, we will identify parts of the genome that control this ability. We will compare patterns of change across ponds to determine the extent to which these occur in parallel, or are idiosynchratic, shedding light on the extent to which evolution is predictable, another long-running controversy in biology, palaeontology and philosophy. Our work will provide a model for understanding how organisms in general could adapt to rapid environmental change.

The current proposal is for responsive mode, 'blue skies' research. Its principal benefit is 'simply' a better understanding of how the world around us works. We should never underestimate the value of this knowledge in its own right. We envisage the following impacts:
(1) The project will lead to improved excellence in UK research by supporting the use of cutting edge 'omics technologies in the study of evolution in vertebrate species. In particular, the PDRA on the project will gain advanced bioinformatic skills through the auspices of Richard Emes and the Nottingham Advanced Data Analysis Centre, and as a result of our collaboration with Jun Kitano's major stickleback genomics group.
(2) Funding will give the PDRA the opportunity to codirect a major international collaborative project, while gaining skills in fieldwork, fish husbandry, and genomics. The technician employed on the grant will gain skills in fieldwork and fish husbandry. Biological material and data collected during the project will be used as the basis for Masters and Honours project theses for years to come.
(3) Engagement with the general public local to the different research sites in the Western Isles and at Sherwood Business Park in North Nottinghamshire. ADCM has been engaged in research in the Western Isles, and particularly on North Uist, for the last 12 years. He has developed a network within the local community and has engaged with them by contributing to websites, giving talks to the local natural history society and donating posters about our research to the local museum and arts centre. We will seek to continue to strengthen these links and to develop new opportunities in the Sherwood area by: (a) organising workshops with local conservation bodies in Scotland (e.g. Scottish Natural Heritage and Comann na Mara, the 'Society of the Sea', a North Uist marine conservation group) and landowners to highlight the astonishing local variation in freshwater and brackish environments, which result in waterbodies on the Hebrides supporting populations of sticklebacks that are an excellent model organism for the study of natural selection, plasticity and adaptation. (b) All of the businesses within the Sherwood Business Park have agreed to the work being carried out in the on-site ponds and many have also indicated an interest in finding out more about our work. We will capitalise on this interest and will work with the Nottinghamshire Wildlife Trust and Sherwood Business Park nature group to deliver a workshop/activity to discuss our work and the importance of the Business Park's ponds in helping to deliver it.
In support of these activities we will make contributions to websites in both areas (e.g. Comman na Mara and the Notts Wildlife Trust). We will also create new posters to describe our work; these will supplement existing posters that we have supplied for display in the local community centre in North Uist and will help to inform about our work in Sherwood. The posters will cover how we are using the stickleback as a model organism for the detailed study of genomic adaptation to new environments and hence to answer fundamental questions about evolutionary biology and the response of organisms to environmental change.
(4) Engagement with wider general public, including school children. ADCM has a history of public engagement with interest groups in the Sheffield, Derby and Nottingham areas. He has visited local primary schools to give slide shows and given seminars about his research to night school classes. For this project ADCM and the PDRA will continue to deliver this type of activity as well as talks and activities in the context of the Nottingham Pint of Science festival, held in the city each May, and the University of Nottingham's annual public outreach event Wonder, held annually in June. The PDRA will be encouraged to take part in training offered by the University of Nottingham's Open Air Laboratories (OPAL) network.