Evolutionary rescue and the limits to phenotypic plasticity: testing theory in the field

Rapid climate change and habitat loss will cause many species to become extinct this century unless they can cope with changing and more extreme ecological conditions. Understanding what limits species' ecological tolerances is therefore an issue of critical scientific importance because it allows us to predict the consequences of ongoing rates of environmental change to populations and therefore to ecological communities.

A common way that organisms deal with environmental variation is to be 'plastic', i.e. to change their morphological, physiological or behavioural traits (their phenotypes) directly in response to their local environment, without requiring rapid evolutionary change. Such 'phenotypic plasticity' buffers changes in the environment, and can maintain fitness across the range of environments typically experienced by a species. Currently, most of the global responses of biodiversity to climate change have been ascribed to such phenotypic plasticity, rather than to actual evolutionary change, underlining its importance in maintaining ecological outputs.

However, the ability of phenotypic plasticity to cope with environmental change has limits. Not only is maintaining variation in gene expression likely to be energetically expensive, it also evolves to maintain fitness only within the range of environments a species experiences in its recent past. In novel or extreme conditions, there is therefore no reason that a species' plastic responses will still improve their ability to survive and produce offspring. Instead, plastic responses that were adaptive in former environments may actually reduce their fitness in new environments. This idea is especially worrying because it predicts that plasticity will be unable to cope as ecological change continues, leading to sudden population declines as critical environmental limits are exceeded. By contrast, other theoretical models predict that plastic responses will be able to evolve more quickly in novel environments, generating faster evolutionary responses than predicted by laboratory experiments under common garden conditions.

We will test these theoretical predictions by measuring the plastic responses of two ecologically divergent species of ragwort (genus Senecio) to changes in their altitudinal position, both within and outside their prevailing distributions on the slopes of Mount Etna, Sicily. These species, Senecio aethnensis and S. chrysanthemifolius differ in a number of phenotypic traits, as well as in the expression of key genes that are associated with adaptation to different altitudes. We will transplant genotypes of both species into a range of field conditions and monitor their performance and plasticity over a two-year period in order to determine each genotype's response to conditions outside its normal ('home') environment. We will measure growth and development parameters, and reproductive parameters as a measure of each genotype's local fitness, and test the degree to which the declines in fitness expected with changes in altitude are offset by plastic changes in their phenotype and in gene expression.

We predict that although observed plastic responses will keep individuals healthy and productive under their species' usual range of altitudinal conditions, phenotypic responses will no longer be appropriate with altitudinal changes beyond these limits. Such an empirical finding will have important implications for predicting the continued ability of species to respond plastically to climate change. In particular, it will suggest, the rapid evolution will be necessary to prevent population and species' extinction where rates of environmental change exceed prevailing conditions within their geographical range.

Economy and society - understanding ecological resilience in changing environments
Biologists have a crucial role to play in generating global sustainability in the coming decades. Although storms and weather loom large in the public's imagination, many of the effects of climate change on human economies will be felt through its effects on the productivity of ecosystems and crops.

A key issue addressed by this research (and highlighted as a priority by the 2011 UK White Paper on Biodiversity) is the role within-species plasticity and evolution plays in the resilience of ecosystems and the biological services that they provide. Such limits to adaptive plasticity could cause sudden changes in ecological communities as well as population (and crop yield) declines as plastic tolerances are exceeded beyond critical limits. The research funded by this application will test the hypothesis that plasticity can only be expected to be adaptive within narrow ecological limits for a given species.

Predicting the ability of plasticity to continue to buffer changing and more variable environments is crucial to understanding these effects on productivity, and of benefit for international and national governments, to whom defining dangerous levels of environmental change (for food security and economic stability) is a crucial issue. In terms of plasticity this demands: (1) defining where limits to adaptive plasticity typically are relative to current and future environmental regimes and; (2) understanding whether phenotypic responses to marginal conditions will accelerate or prevent the evolution of wider ecological tolerances for species of key economic importance.

Crop breeders and the agricultural industry
The proposed research uses Asteraceae species as a model system to define regions of the genome that are crucial for adaptation (and plastic responses) to changing temperature, and more efficient water use. As well as providing general lessons for the limits of plasticity to environmental change, these genes may be of specific use for agronomically important plants within the Asteraceae, such as sunflowers, lettuce, chicory, and artichoke. "Plastic" genes (and an understanding of the limits to plasticity) are likely to become increasingly important in the coming century for improving the resilience of crop plants in agricultural environments that will not only to be warmer and drier on average in Europe, but also more variable. Our transcriptomic analysis of field-induced variation will be a first step towards identifying such "plastic" genes.

The general public
Beyond predicting the biological effects of climate change, and in addition to the fundamental interest in the rapid ecological divergence of these iconic plant species on Mount Etna, the issues of phenotypic plasticity explored in this proposal are part of what is often called the "Nature vs nurture" debate. Approaching this topic from a biological perspective, particularly using modern genomic and genetic tools, makes this discussion more nuanced than typically depicted by the popular press. However, we think it's important that the complexity of how genomes interact with their internal and external environments to make phenotypes is appreciated more generally. This is especially important because such interactions underlie important social issues, such as punishment and social cohesion, lifestyle choices, and health care funding and planning.