Régis Ferrière

Cheating and the evolutionary stability of mutualisms

Interspecific mutualisms have been playing a central role in the functioning of all ecosystems since the early history of life. Yet the theory of coevolution of mutualists is virtually nonexistent, by contrast with well–developed coevolutionary theories of competition, predator–prey and host–parasite interactions. This has prevented resolution of a basic puzzle posed by mutualisms: their persistence in spite of apparent evolutionary instability. The selective advantage of‘cheatin’, that is, reaping mutualistic benefits while providing fewer commodities to the partner species, is commonly believed to erode a mutualistic interaction, leading to its dissolution or reciprocal extinction. However, recent empirical findings indicate that stable associations of mutualists and cheaters have existed over long evolutionary periods. Here, we show that asymmetrical competition within species for the commodities offered by mutualistic partners provides a simple and testable ecological mechanism that can account for the long–term persistence of mutualisms. Cheating, in effect, establishes a background against which better mutualists can display any competitive superiority. This can lead to the coexistence and divergence of mutualist and cheater phenotypes, as well as to the coexistence of ecologically similar, but unrelated mutualists and cheaters.

Physical performance and darwinian fitness in lizards

Strong evidence for a genetic basis of variation in physical performance has accumulated. Considering one of the basic tenets of evolutionary physiology—that physical performance and darwinian fitness are tightly linked—one may expect phenotypes with exceptional physiological capacities to be promoted by natural selection. Why then does physical performance remain considerably variable in human and other animal populations? Our analysis of locomotor performance in the common lizard (Lacerta vivipara) demonstrates that initial endurance (running time to exhaustion measured at birth) is indeed highly heritable, but natural selection in favour of this trait can be unexpectedly weak. A manipulation of dietary conditions unravels a proximate mechanism explaining this pattern. Fully fed individuals experience a marked reversal of performance within only one month after birth: juveniles with low endurance catch up, whereas individuals with high endurance lose their advantage. In contrast, dietary restriction allows highly endurant neonates to retain their locomotor superiority as they age. Thus, the expression of a genetic predisposition to high physical performance strongly depends on the environment experienced early in life.

Evolutionary rescue: an emerging focus at the intersection between ecology and evolution.

There is concern that the rate of environmental change is now exceeding the capacity of many populations to adapt. Mitigation of biodiversity loss requires science that integrates both ecological and evolutionary responses of populations and communities to rapid environmental change, and can identify the conditions that allow the recovery of declining populations. This special issue focuses on evolutionary rescue (ER), the idea that evolution might occur sufficiently fast to arrest population decline and allow population recovery before extinction ensues. ER emphasizes a shift to a perspective on evolutionary dynamics that focuses on short time-scales, genetic variants of large effects and absolute rather than relative fitness. The contributions in this issue reflect the state of field; the articles address the latest conceptual developments, and report novel theoretical and experimental results. The examples in this issue demonstrate that this burgeoning area of research can inform problems of direct practical concern, such as the conservation of biodiversity, adaptation to climate change and the emergence of infectious disease. The continued development of research on ER will be necessary if we are to understand the extent to which anthropogenic global change will reduce the Earths biodiversity.

THE ADAPTIVE DYNAMICS OF ALTRUISM IN SPATIALLY HETEROGENEOUS POPULATIONS

Abstract.— We study the spatial adaptive dynamics of a continuous trait that measures individual investment in altruism. Our study is based on an ecological model of a spatially heterogeneous population from which we derive an appropriate measure of fitness. The analysis of this fitness measure uncovers three different selective processes controlling the evolution of altruism: the direct physiological cost, the indirect genetic benefits of cooperative interactions, and the indirect genetic costs of competition for space. In our model, habitat structure and a continuous life cycle makes the cost of competing for space with relatives negligible. Our study yields a classification of adaptive patterns of altruism according to the shape of the costs of altruism (with decelerating, linear, or accelerating dependence on the investment in altruism). The invasion of altruism occurs readily in species with accelerating costs, but large mutations are critical for altruism to evolve in selfish species with decelerating costs. Strict selfishness is maintained by natural selection only under very restricted conditions. In species with rapidly accelerating costs, adaptation leads to an evolutionarily stable rate of investment in altruism that decreases smoothly with the level of mobility. A rather different adaptive pattern emerges in species with slowly accelerating costs: high altruism evolves at low mobility, whereas a quasi‐selfish state is promoted in more mobile species. The high adaptive level of altruism can be predicted solely from habitat connectedness and physiological parameters that characterize the pattern of cost. We also show that environmental changes that cause increased mobility in those highly altruistic species can beget selection‐driven self‐extinction, which may contribute to the rarity of social species.

Adaptive Evolution of Social Traits: Origin, Trajectories, and Correlations of Altruism and Mobility

Social behavior involves “staying and helping,” two individual attributes that vary considerably among organisms. Investigating the ultimate causes of such variation, this study integrates previously separate lines of research by analyzing the joint evolution of altruism and mobility. We unfold the network of selective pressures and derive how these depend on physiological costs, eco‐evolutionary feedbacks, and a complex interaction between the evolving traits. Our analysis highlights habitat saturation, both around individuals (local aggregation) and around unoccupied space (local contention), as the key mediator of altruism and mobility evolution. Once altruism and mobility are allowed to evolve jointly, three general insights emerge. First, the cost of mobility affects the origin of altruism, determining whether and how quickly selfishness is overcome. Second, the cost of altruism determines which of two qualitatively different routes to sociality are taken: an evolutionary reduction of mobility, resulting in higher habitat saturation, is either preceded or followed by the adaptive rise of altruism. Third, contrary to conventional expectations, a positive correlation between evolutionarily stable levels of altruism and mobility can arise; this is expected when comparing populations that evolved under different constraints on mobility or that differ in other life‐history traits.

Mother-offspring interactions affect natal dispersal in a lizard

Interactions between relatives operate strong selective pressures on dispersal. Recently, a correlative study in the common lizard (Lacerta vivipara) suggested that natal dispersal might respond plastically to mother–offspring interactions. Here, we describe a factorial experiment supporting this observation. Two crossed treatments were applied to experimental patches of the common lizard: (i) presence versus absence of the mother, inducing a difference of kinship in offspring neighbourhoods; and (ii) high versus low patch density, resulting in two levels of conspecific abundance and modulating the effect of mother presence on the average kinship within a patch. Dispersal of the same cohort of offspring was observed at the juvenile and yearling stages. We found a sex–dependent response of offspring dispersal to the removal of the mother at the two stages. During the juvenile stage, higher dispersal was found in females in the presence of the mother, with males unaffected. During the yearling stage, the responses of both sexes to the presence of the mother opposed each other. In addition, we found a negative relationship between dispersal and patch density at the juvenile stage. No interaction between density and the presence of the mother was detected, which suggests that behavioural responses to kinship and density are disconnected and that kinship is assessed at a small social scale. We discuss the role of competition and inbreeding avoidance to explain the observed pattern.

The evolution of dispersal under demographic stochasticity.

Temporal and spatial variations of the environment are important factors favoring the evolution of dispersal. With few exceptions, these variations have been considered to be exclusively fluctuations of habitat quality. However, since the presence of conspecifics forms part of an individual’s environment, demographic stochasticity may be a component of this variability as well, in particular when local populations are small. To study this effect, we analyzed the evolution of juvenile dispersal in a metapopulation model in which habitat quality is constant in space and time but occupancy fluctuates because of demographic stochasticity. Our analysis extends previous studies in that it includes competition of resources and competition for space. Also, juvenile dispersal is not given by a fixed probability but is made conditional on the presence of free territories in a patch, whereas individuals born in full patches will always disperse. Using a combination of analytical and numerical approaches, we show that demographic stochasticity in itself may provide enough variability to favor dispersal even from patches that are not fully occupied. However, there is no simple relationship between the evolution of dispersal and various indicators of demographic stochasticity. Selected dispersal depends on all aspects of the life‐history profile, including kin selection.

Chaos and evolution

There is growing interest in applying nonlinear methods to evolutionary biology. With good reason: the living world is full of nonlinearities, responsible for steady states, regular oscillations, and chaos in biological systems. Evolutionists may find nonlinear dynamics important in studying short-term dynamics of changes in genotype frequency, and in understanding selection and its constraints. More speculatively, dynamical systems theory may be important because nonlinear fluctuations in some traits may sometimes be favored by selection, and because some long-run patterns of evolutionary change could be described using these methods.

FROM INDIVIDUAL STOCHASTIC PROCESSES TO MACROSCOPIC MODELS IN ADAPTIVE EVOLUTION

We are interested in modelling Darwinian evolution, resulting from the interplay of phenotypic variation and natural selection through ecological interactions. Our models are rooted in the microscopic, stochastic description of a population of discrete individuals characterized by one or several adaptive traits. The population is modelled as a stochastic point process whose generator captures the probabilistic dynamics over continuous time of birth, mutation, and death, as influenced by each individuals trait values, and interactions between individuals. An offspring usually inherits the trait values of her progenitor, except when a mutation causes the offspring to take an instantaneous mutation step at birth to new trait values. We look for tractable large population approximations. By combining various scalings on population size, birth and death rates, mutation rate, mutation step, or time, a single microscopic model is shown to lead to contrasting macroscopic limits of a different nature: deterministic, in the form of ordinary, integro-, or partial differential equations, or probabilistic, like stochastic partial differential equations or superprocesses. In the limit of rare mutations, we show that a possible approximation is a jump process, justifying rigorously the so-called trait substitution sequence. We thus unify different points of view concerning mutation-selection evolutionary models.

Bet Hedging via Seed Banking in Desert Evening Primroses (Oenothera, Onagraceae): Demographic Evidence from Natural Populations

Bet hedging is one solution to the problem of an unpredictably variable environment: fitness in the average environment is sacrificed in favor of lower variation in fitness if this leads to higher long‐run stochastic mean fitness. While bet hedging is an important concept in evolutionary ecology, empirical evidence that it occurs is scant. Here we evaluate whether bet hedging occurs via seed banking in natural populations of two species of desert evening primroses (Oenothera, Onagraceae), one annual and one perennial. Four years of data on plants and 3 years of data on seeds yielded two transitions for the entire life cycle. One year was exceptionally dry, leading to reproductive failure in the sample areas, and the other was above average in precipitation, leading to reproductive success in four of five populations. Stochastic simulations of population growth revealed patterns indicative of bet hedging via seed banking, particularly in the annual populations: variance in fitness and fitness in the average environment were lower with seed banking than without, whereas long‐run stochastic mean fitness was higher with seed banking than without across a wide range of probabilities of the wet year. This represents a novel, unusually rigorous demonstration of bet hedging from field data.