The predictability and limits of evolution in response to increased temperature: insights from a natural 'experiment'

The ability to predict evolutionary responses to environmental change is of central importance for future conservation efforts. Increases in temperature from anthropogenic climate change are arguably the most widespread and dramatic alteration of natural ecosystems, with its impact predicted to become more acute with time. These increases in temperature are likely to shift species distributions, or drive developmental and evolutionary changes in local populations. Therefore, knowing how currently extant populations can or have changed in response to warmer conditions would be extremely important. Here we propose to investigate how populations change with respect to their growth, physiology, and anatomy in response to long term exposure to increased temperature. We will also determine what genetic changes may have happened in addition to epigenetic changes (i.e. environmentally-induced structural alterations of the genome that affect its function but don't change the DNA sequence), and relate these to phenotypic variation.

To address this we will use a series of unique study sites in Iceland where populations of threespine stickleback live both in geothermally heated ponds and in unheated (i.e. cool) ponds in close proximity. These pairs of adjacent populations (which occur in several places) have lived at these contrasting temperatures for thousands of generations and preliminary investigation shows evidence of evolutionary divergence between them. This broad-ranging project will use both comparative and experimental approaches to quantify how the phenotype, genome, and epigenome interact when the animal experiences rising temperatures. Lab experiments will use fish from these source populations to investigate 1) population level differences between ambient (cool) and 'warmed' populations at the genomic and epigenomic level, 2) the inheritance of phenotypic traits (including metabolic rate, morphology and locomotor performance) and epigenomic states in sticklebacks reared under reciprocal temperature regimes, 3) alterations of development under warm conditions that could limit evolution, and 4) the genetic and epigenetic basis for variation in phenotypic traits under different temperatures. This project will be holistic through its ability to allow plasticity and heritable epigenetic effects to be assessed together with genetic variation. It will reveal whether there are consistent (and hence predictable) evolutionary and epigenetic changes when populations are exposed to warmer temperatures, and will explore the role of plasticity in shaping adaptive responses. As a result, it will provide novel information on the extent to which populations can adapt to a warming world.

The improved understanding of the role of temperature in determining the performance of fish will also inform our views on the short- and longer-term impacts of environmental change in freshwater ecosystems. Human-influenced environmental change, climate change being of perhaps most notable and immediate concern, is rapidly altering natural habitats and organisms are exposed to more erratic, extreme, unpredictable and unseasonal spells of weather. That these environmental perturbations may have long-term consequences beyond their immediate effects is not widely appreciated or understood. It is therefore justifiably expected by the wider public that biologists should be able to predict, and where the opportunity exists, examine the likely biological consequences of these changes. By focusing on both the short and long-term effects of environmental temperature perturbations in this project we will contribute directly to this body of applied information. This research will therefore be of interest to management agencies - as evidenced by the participation of the Icelandic Institute for Freshwater Fisheries - for making decisions about populations that are of greatest priority for conservation. Our genetic data have the potential to identify what changes are occurring at the molecular level, and this information (given the often common language of genetic variation) could be used to determine the susceptibility and evolutionary potential of other taxa and populations to the effects of climate change. Our outreach activities will promote the understanding of these issues by conservation/policy-forming bodies as well as among the general public. Given that the project is testing whether temperature affects the developmental processes occurring during early growth, it also has a direct relevance to animal scientists rearing captive animals, including those associated with the aquaculture industry.