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

快速的气候变化和栖息地的丧失将导致许多物种在本世纪灭绝，除非它们能够应对不断变化和更加极端的生态条件。因此，了解是什么限制了物种的生态耐受性是一个至关重要的科学问题，因为它使我们能够预测持续的环境变化速度对种群的影响，从而对生态群落的影响。生物体应对环境变化的一种常见方式是“可塑性”，即直接改变其形态、生理或行为特征（其表型）以响应其当地环境，而不需要快速的进化变化。这种“表型可塑性”缓冲了环境的变化，并可以在一个物种通常经历的环境范围内保持适应性。目前，大多数全球生物多样性对气候变化的响应都归因于这种表型可塑性，而不是实际的进化变化，强调了其在维持生态产出方面的重要性。然而，表型可塑性应对环境变化的能力是有限的。不仅维持基因表达的变异可能会消耗大量的能量，而且物种进化到只能在其最近经历的环境范围内保持适应性。因此，在新的或极端的条件下，一个物种的可塑性反应没有理由仍然能提高它们生存和繁殖后代的能力。相反，在以前的环境中适应的可塑性反应实际上可能会降低它们在新环境中的适应性。这一观点尤其令人担忧，因为它预测，随着生态变化的持续，生物的可塑性将无法应对，一旦超过临界环境限制，就会导致种群数量突然下降。相比之下，其他理论模型预测，塑料反应将能够在新的环境中更快地进化，产生比在普通花园条件下的实验室实验预测的更快的进化反应。我们将通过测量两种生态上不同的ragwort （Senecio属）物种对其海拔位置变化的可塑性响应来测试这些理论预测，包括在西西里岛埃特纳火山斜坡上的主要分布区域内外。Senecio aethnensis和S. chrysanthemum在许多表型性状以及与适应不同海拔相关的关键基因表达上存在差异。我们将把这两种物种的基因型移植到一系列野外条件下，并在两年的时间内监测它们的表现和可塑性，以确定每种基因型对正常（“家园”）环境以外条件的反应。我们将测量生长和发育参数，以及生殖参数作为衡量每种基因型的局部适合度的指标，并测试随海拔变化而预期的适合度下降在多大程度上被其表型和基因表达的可塑性变化所抵消。我们预测，尽管观察到的可塑性反应将使个体在其物种通常的海拔条件范围内保持健康和生产力，但表型反应将不再适用于超过这些极限的海拔变化。这一实证发现将对预测物种对气候变化的可塑性反应的持续能力具有重要意义。特别是，它将表明，在环境变化速度超过其地理范围内的普遍条件时，为了防止人口和物种的灭绝，快速进化是必要的。

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.