Eco-evolutionary feedbacks, adaptive dynamics and evolutionary rescue theory

Regis Ferriere Stphane Legendre Articles on similar topics can be found in the following collections ecology (543 articles) evolution (715 articles) theoretical biology (71 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top right-hand corner of the article or click here References Subject collections Email alerting service rstb.royalsocietypublishing.org Review Cite this article: Ferriere R, Legendre S. 2013 Eco-evolutionary feedbacks, adaptive dynamics and evolutionary rescue theory. Phil Trans R Soc B 368: 20120081. http://dx.doi.org/10.1098/rstb.2012.0081 Author for correspondence: Regis Ferriere e-mail: Electronic supplementary material is available at http://dx.doi.org/10.1098/rstb.2012.0081 or via http://rstb.royalsocietypublishing.org. Eco-evolutionary feedbacks, adaptive dynamics and evolutionary rescue theory Regis Ferriere1,3 and Stephane Legendre2 1Ecole Normale Superieure, and 2CNRS, Laboratoire Ecologie-Evolution, UMR 7625 UPMC-ENS-CNRS, 46 rue dUlm, 75005 Paris, France 3Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA Adaptive dynamics theory has been devised to account for feedbacks between ecological and evolutionary processes. Doing so opens new dimensions to and raises new challenges about evolutionary rescue. Adaptive dynamics theory predicts that successive trait substitutions driven by eco-evolutionary feedbacks can gradually erode population size or growth rate, thus potentially raising the extinction risk. Even a single trait substitution can suffice to degrade population viability drastically at once and cause evolutionary suicide. In a changing environment, a population may track a viable evolutionary attractor that leads to evolutionary suicide, a phenomenon called evolutionary trapping. Evolutionary trapping and suicide are commonly observed in adaptive dynamics models in which the smooth variation of traits causes catastrophic changes in ecological state. In the face of trapping and suicide, evolutionary rescue requires that the population overcome evolutionary threats generated by the adaptive process itself. Evolutionary repellors play an important role in determining how variation in environmental conditions correlates with the occurrence of evolutionary trapping and suicide, and what evolutionary pathways rescue may follow. In contrast with standard predictions of evolutionary rescue theory, low genetic variation may attenuate the threat of evolutionary suicide and small population sizes may facilitate escape from evolutionary traps. 1. Introduction Population viability is determined by the interplay of environmental influences and individual phenotypic traits shaping life histories and behaviour. A longstanding view in evolutionary ecology has been that adaptive evolution would optimize a populations phenotypic state in the sense of maximizing some suitably chosen measure of fitness (such as its intrinsic growth rate, r, or its basic reproduction ratio R0 [1 3]). On this basis, it was largely expected that adaptive evolution would always improve the demographic balance of a population, resulting in, e.g. higher population size, lower extinction risk or larger geographical spread. This picture is reflected in our current theory of evolutionary rescue. In the most general terms, evolutionary rescue occurs when a population subject to environmental change performs better under the operation of evolutionary processes than without these processes; typically, the currency of population performance is the population size or persistence time [1] (see also [4]). Historically, there have been two main theoretical approaches to evolutionary rescue. One approach capitalizes on a well-established modelling tradition in population genetics to investigate how mutations may reduce the extinction risk of a population reaching low size or negative growth upon some abrupt change in the environment [5 9]. The other approach uses quantitative genetics to study the conditions under which selection enables a population to track a moving evolutionary optimum as the environment changes gradually [10 13]. These two theoretical views of evolutionary rescue show interesting conceptual differences in (i) the type of environmental change (abrupt versus & 2012 The Author(s) Published by the Royal Society. All rights reserved. trait expression ecological interactions life history population dynamics community structure ecosystem function selective pressures on heritable variation Figure 1. Eco-evolutionary feedback loop. Complex selective pressures on individuals phenotypic traits emanate from the interaction of individuals (I) with their local environment (E)consisting of conspecifics, prey and predators, mutualists and parasites, in their ecosystem context. Heritable variation in adaptive traits responds to these pressures, and in turn affects how these individuals impact their environment. This feedback loopfrom the environment to the individuals, and backintimately links ecological and evolutionary processes. gradual), (ii) threat (an actual demographic deficit versus a risk of demographic deficit), and (iii) rescue pathway (returning to demographic balance versus avoiding demographic imbalance). But they both are grounded in the notion that adaptive evolution inherently tends to enhance population viability. Despite the long tradition of describing evolutionary processes through concepts of progress and optimization, as early as in 1932 J. B. S. Haldane pointed out that there was no general principle preventing adaptive evolution from harming population performance [14]. A verbal example comes from considering overtopping growth in plants. Taller trees get more sunlight while casting shade onto their neighbours. As selection causes the average tree height to increase, fecundity declines because more of the trees energy budget is diverted from seed production to wood production. Under these circumstances, it may also take longer for the trees to reach maturity. Thus, arborescent growth as an evolutionary response to selection for competitive ability can cause population abundance and/or the intrinsic rate of population growth to decline. The logical conclusion of this process may even be population extinction, as was first explained by Haldane [14]. The past two decades of research in theoretical evolutionary ecology have done much to flesh out this picture. The concept of the eco-evolutionary feedback loop has been introduced to link the joint operation of ecological and evolutionary processes to the dynamics of populations (figure 1). The selection pressures driving phenotypic evolution should be derived from models that describe the whole eco-evolutionary feedback loop [15 20]. The structure of the loop determines whether an optimization principle can be found in the first place, and, if so, what specific fitness measure it ought to be based o (...truncated)