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

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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.