Phenotypic plasticity in evolutionary rescue experiments

Review 2 4 Luis-Miguel Chevin 2 3 4 Romain Gallet 2 3 4 Richard Gomulkiewicz 1 2 4 Robert D. Holt 0 2 4 Simon Fellous 2 4 5 6 0 Department of Biology, University of Florida , Gainesville, FL 32611 , USA 1 School of Biological Sciences, Washington State University , PO Box 644236, Pullman, WA 99164 , USA 2 Subject Areas: evolution , ecology 3 Centre d'Ecologie Fonctionnelle et Evolutive (UMR 5175) , 1919 route de Mende, 34293 Montpellier Cedex 5 , France 4 One contribution of 15 to a Theme Issue 'Evolutionary rescue in changing environments' 5 Institute Institut des Sciences de l'E volution de Montpellier (UMR 5554 ISE-M), CNRS - Universite Montpellier 2 , Place Euge`ne Bataillon, 34095 Montpellier Cedex 05 , France 6 Centre de Biologie et de Gestion des Populations, Institut National de la Recherche Agronomique (INRA), Campus International de Baillarguet , 34988 Montferrier sur Lez cedex , France Population persistence in a new and stressful environment can be influenced by the plastic phenotypic responses of individuals to this environment, and by the genetic evolution of plasticity itself. This process has recently been investigated theoretically, but testing the quantitative predictions in the wild is challenging because (i) there are usually not enough population replicates to deal with the stochasticity of the evolutionary process, (ii) environmental conditions are not controlled, and (iii) measuring selection and the inheritance of traits affecting fitness is difficult in natural populations. As an alternative, predictions from theory can be tested in the laboratory with controlled experiments. To illustrate the feasibility of this approach, we briefly review the literature on the experimental evolution of plasticity, and on evolutionary rescue in the laboratory, paying particular attention to differences and similarities between microbes and multicellular eukaryotes. We then highlight a set of questions that could be addressed using this framework, which would enable testing the robustness of theoretical predictions, and provide new insights into areas that have received little theoretical attention to date. 1. Introduction Abrupt environmental alterations can increase extinction risk and foster rapid phenotypic change, both of which are broadly observed in response to current climate change, species introductions and other anthropogenic modifications of the environment [1,2]. Evolution on the time-scale of population dynamics may affect the demography of a species, that is, the set of vital rates (survivals and fecundities) that determine the size and age/stage composition of a population [3,4]. In particular, evolutionary rescue (hereafter ER) describes the situation where adaptive evolution prevents population extinction in a stressful environment [5,6]. The details of this interaction between evolution and demography, however, depend on the underlying mechanism of phenotypic change, i.e. whether it is caused by a change in the genetic composition of the population in response to natural selection, or by a change in the phenotype of each individual in response to its environment of development or expression. Monitoring of wild populations with known pedigrees increasingly shows that rapid phenotypic change of traits affecting fitness often involves a combination of genetic change and phenotypic plasticity [7 10]. This suggests that phenotypic plasticity may play an important role in the interaction of demography and evolution. Furthermore, plasticity can vary genetically, and may thus itself evolve in response to natural selection [11], so the evolution of plasticity may also be important for ER. On the basis of verbal arguments tracing back to Baldwin [12], recent theory has investigated how the interplay of phenotypic plasticity, genetic evolution and demography, affects population persistence in a new or changing environment [13 15]. Testing predictions from this theory can be challenging in the wild, because of the inherent lack of control on environmental conditions, and of the difficulties in accurately measuring fitness and how it relates to phenotypes and genotypes in natural populations, among other complications [16] (even though some cases of ER are documented in the wild, reviewed in [17]). Alternatively, current theoretical predictions and further questions they raise can be investigated in the laboratory using experimental evolution. While such experiments have rarely been performed so far in the context of plasticity interacting with ER, we argue below that (i) all the conceptual tools are available and (ii) many model organisms are adequate for such studies. To argue our point, we start by briefly defining the concepts of plasticity and generalism in relation to fitness and population growth in variable environments. We then review theoretical predictions for the role of phenotypic plasticity and its evolution in ER following an abrupt environmental shift, and the experimental work that addresses components of this theory. We end by highlighting important questions that could be addressed by this approach, and outline simple prototype experiments. 2. Key concepts In this section, we introduce the conceptual tools that will be discussed in the following sections. A thorough review of the many forms of plasticity and of their mechanistic underpinnings is beyond the scope of this paper, and is already available elsewhere [11,18 20]. Instead, we specifically focus on issues relevant to ER. (a) Phenotypic plasticity and generalism Many morphological, physiological or behavioural traits can change in response to an organisms environment. The curve that captures this relationship between trait and environment for a given genotype is the norm of reaction [19,21], a generic term that applies to fitness or to any other trait. However, in the context of evolutionary demography, it is useful to distinguish fitness and its life-history components (survival and fecundity) from other traits. This is because fitness has the specific attribute of defining adaptiveness for other traits (thus causing their evolution), and because it can determine population growth [4,22,23]. Importantly for ER, the focus is on absolute fitness (broadly defined as the expected number of offspring in the next generation), rather than on relative fitness ( proportional contribution to the next generation, more commonly used in evolutionary genetics), because only the former affects demography. In practice, one can compute absolute fitness from the vital rates (ageor stage-specific survivals and fecundities) using standard life-history theory [3,4,24,25]. Phenotypic plasticity describes any change in the phenotype of a given genotype with its environment of development or expression, leading to non-flat reaction norms. The term plasticity is better suited to characterize effects of the environment on traits that are not direct components of fitness. While some authors (...truncated)