Inertia: The discrepancy between individual and common good in dispersal and prospecting behaviour

The group selection debate of the 1960s made it clear that evolution does not necessarily increase population performance. Individuals can be selected to have traits that diminish a common good and make population persistence difficult. At the extreme, the discrepancy between levels of selection is predicted to make traits evolve towards values at which a population can no longer persist (evolutionary suicide). Dispersal and prospecting are prime examples of traits that have a strong influence on population persistence under environmental and demographic stochasticity. Theory predicts that an 'optimal' dispersal strategy from a population point of view can differ considerably from that produced by individual-level selection. Because dispersal is frequently risky or otherwise costly, individuals are often predicted to disperse less than would be ideal for population performance (persistence or size). We define this discrepancy as 'inertia' and examine current knowledge of its occurrence and effects on population dynamics in nature. We argue that inertia is potentially widespread but that a framework is currently lacking for predicting precisely the extent to which it has a real influence on population persistence. The opposite of inertia, 'hypermobility' (more dispersal by individuals than would maximize population performance) remains a possibility: it is known that highest dispersal rates do not lead to best expected population performance, and examples of such high dispersal evolving exist at least in the theoretical literature. We also show, by considering prospecting behaviour, that similar issues arise in species with advanced cognitive and learning abilities. Individual prospecting strategies and the information acquired during dispersal are known to influence the decisions and therefore the fate of individuals and, as a corollary, populations. Again, the willingness of individuals to sample environments might evolve to levels that are not optimal for populations. This conflict can take intriguing forms. For example, better cognitive abilities of individuals may not always lead to better population-level performance. Simulation studies have found that 'blind' dispersal can lead to better connected metapopulations than cognitively more advanced habitat choice rules: the latter can lead to too many individuals sticking to nearby safe habitat. The study of the mismatch between individual and population fitness should not be a mere intellectual exercise. Population managers typically need to take a population-level view of performance, which may necessitate human intervention if it differs from what is selected for. We conclude that our knowledge of inertia and hypermobility would advance faster if theoretical studies-without much additional effort-quantified the population consequences of the evolving traits and compared this with hypothetical (not selectively favoured) dispersal rules, and if empirical studies were similarly conducted with the differing levels of selection in mind. © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society.Peer Reviewe

Individual reversible plasticity as a genotype-level bet-hedging strategy

AbstractReversible plasticity in phenotypic traits allows organisms to cope with environmental variation within lifetimes, but costs of plasticity may limit just how well the phenotype matches the environmental optimum. An additional adaptive advantage of plasticity might be to reduce fitness variance, or bet-hedging to maximize geometric (rather than simply arithmetic) mean fitness. Here we model the evolution of reaction norm slopes, with increasing costs as the slope or degree of plasticity increases. We find that greater investment in plasticity (i.e. steeper reaction norm slopes) is favoured in scenarios promoting bet-hedging as a response to multiplicative fitness accumulation (i.e. coarser environmental grains and fewer time steps prior to reproduction), because plasticity lowers fitness variance across environmental conditions. In contrast, in scenarios with finer environmental grain and many time steps prior to reproduction, bet-hedging plays less of a role and individual-level optimization favours evolution of shallower reaction norm slopes. We discuss contrasting predictions from this partitioning of the different adaptive causes of plasticity into short-term individual benefits versus long-term genotypic (bet-hedging) benefits under different costs of plasticity scenarios, thereby enhancing our understanding of the evolution of optimum levels of plasticity in examples from thermal physiology to advances in avian lay dates.Impact summaryPhenotypic plasticity is a key mechanism by which organisms cope with environmental change. Plasticity relies on the existence of some reliable environmental cue that allows organisms to infer current or future conditions, and adjust their traits in response to better match the environment. In contrast, when environmental fluctuations are unpredictable, bet-hedging favours lineages that persist by lowering their fitness variance, either among or within individuals. Plasticity and bet-hedging are therefore often considered to be alternative modes of adaptation to environmental change. However, we here make the point that plasticity also has the capacity to change an organism’s variance in fitness across different environmental conditions, and could thus itself be part of – and not an alternative to – a bet-hedging strategy. We show that bet-hedging at the genotype level affects the optimal degree of plasticity that individuals use to track environmental fluctuations, because despite a reduction in expected fitness at the individual level, costly investment in the ability to be plastic also lowers variance in fitness. We also discuss alternative predictions that arise from scenarios with different types of costs of plasticity. Evolutionary bet-hedging and phenotypic plasticity are both topics experiencing a renewed surge of interest as researchers seek to better integrate different adaptations to ongoing rapid environmental change in a range of areas of literature within ecology and evolution, including behavioural ecology, evolutionary physiology and life-history theory. We believe that demonstrating an important novel link between these two mechanisms is of interest to research in many different fields, and opens new avenues for understanding organismal adaptation to environmental change.</jats:sec