A null model for the distribution of fitness effects of mutations.

The distribution of fitness effects (DFE) of new mutations is key to our understanding of many evolutionary processes. Theoreticians have developed several models to help understand the patterns seen in empirical DFEs. Many such models reproduce the broad patterns seen in empirical DFEs but these models often rely on structural assumptions that cannot be tested empirically. Here, we investigate how much of the underlying "microscopic" biological processes involved in the mapping of new mutations to fitness can be inferred from "macroscopic" observations of the DFE. We develop a null model by generating random genotype-to-fitness maps and show that the null DFE is that with the largest possible information entropy. We further show that, subject to one simple constraint, this null DFE is a Gompertz distribution. Finally, we illustrate how the predictions of this null DFE match empirically measured DFEs from several datasets, as well as DFEs simulated from Fisher's geometric model. This suggests that a match between models and empirical data is often not a very strong indication of the mechanisms underlying the mapping of mutation to fitness.

The evolution of age-specific choosiness when mating.

Mate choice is a crucial element of many processes in evolutionary biology. Empirical research has shown that mating preference and choosiness often change with age. Understanding the evolutionary causes of patterns of age-specific choosiness is challenging because different mechanisms can give rise to the same pattern. Instead of focusing on the optimal age-specific choosiness strategy given fitness trade-offs, we approach this question from a more general standpoint and ask how the strength of selection on choosiness changes with the age at which it is expressed. We show that the strength of selection on a modifier of choosiness at a given age depends on the relative contribution of this age class to the pool of offspring but does not depend directly on the strength of selection on fitness components at the age affected by the modifier. We illustrate our results by contrasting two life histories from the literature. We further show how mutation-selection balance at the choosiness locus can shape age-specific choosiness. Our results provide new insights for understanding the evolution of choosiness throughout life, with implications for understanding the evolution of mate choice and reproductive isolation.

Fluctuations in lifetime selection in an autocorrelated environment.

Most natural environments vary stochastically and are temporally autocorrelated. Previous theory investigating the effects of environmental autocorrelation on evolution mostly assumed that total fitness resulted from a single selection episode. Yet organisms are likely to experience selection repeatedly along their life, in response to possibly different environmental states. We model the evolution of a quantitative trait in organisms with non-overlapping generations undergoing several episodes of selection in a randomly fluctuating and autocorrelated environment. We show that the evolutionary dynamics depends not directly on fluctuations of the environment, but instead on those of an effective phenotypic optimum that integrates the effects of all selection episodes within each generation. The variance and autocorrelation of the integrated optimum shape the variance and predictability of selection, with substantial qualitative and quantitative deviations from previous predictions considering a single selection episode per generation. We also investigate the consequence of multiple selection episodes per generation on population load. In particular, we identify a new load resulting from within-generation fluctuating selection, generating the death of individuals without significance for the evolutionary dynamics. Our study emphasizes how taking into account fluctuating selection within lifetime unravels new properties of evolutionary dynamics, with crucial implications notably with respect to responses to global changes.

Maladaptive Shifts in Life History in a Changing Environment.

Many species facing climate change have complex life cycles, with individuals in different stages differing in their sensitivity to a changing climate and their contribution to population growth. We use a quantitative genetics model to predict the dynamics of adaptation in a stage-structured population confronted with a steadily changing environment. Our model assumes that different optimal phenotypic values maximize different fitness components, consistent with many empirical observations. In a constant environment, the population evolves toward an equilibrium phenotype, which represents the best compromise given the trade-off between vital rates. In a changing environment, however, the mean phenotype in the population will lag behind this optimal compromise. We show that this lag may result in a shift along the trade-off between vital rates, with negative consequences for some fitness components but, less intuitively, improvements in some others. Complex eco-evolutionary dynamics can emerge in our model due to feedbacks between population demography and adaptation. Because of such feedback loops, selection may favor further shifts in life history in the same direction as those caused by maladaptive lags. These shifts in life history could be wrongly interpreted as adaptations to the new environment, while in reality they only reflect the inability of the population to adapt fast enough.

The Roles of Sexual and Viability Selection in the Evolution of Incomplete Reproductive Isolation: From Allopatry to Sympatry.

In recent years, theoretical models have introduced the concept that ongoing hybridization between "good" species can occur because incomplete reproductive isolation can be a selected optimum. They furthermore show that positive frequency-dependent sexual selection, which is naturally generated by some of the underlying processes that lead to assortative mating, plays a key role in the evolution of incomplete reproductive isolation. This occurs, however, through different mechanisms in sympatric versus allopatric scenarios. We investigate the evolution of incomplete reproductive isolation by sexual selection in scenarios ranging from sympatry to allopatry, to examine how these mechanisms interact. We consider an ecological scenario in which there are two habitats used during foraging and individuals can breed either within a habitat or in a common mating pool. We find that when trait divergence is maintained, sexual selection drives the evolution of choosiness in opposite ways in the common mating pool versus within each habitat. Specifically, strong choosiness is favored in the common mating pool, whereas intermediate choosiness is favored within habitat; the interaction of these forces determines whether intermediate reproductive isolation ultimately evolves in the system. We further find cases where the evolution of stronger choosiness occurs but leads to the loss of divergence. Overall, our study shows that contrasting forces on the evolution of reproductive isolation can occur in different mating areas, and we propose a new avenue for understanding the diversity in levels of reproductive isolation within and across species.

Stochastic Evolutionary Demography under a Fluctuating Optimum Phenotype.

Many natural populations exhibit temporal fluctuations in abundance that are consistent with external forcing by a randomly changing environment. As fitness emerges from an interaction between the phenotype and the environment, such demographic fluctuations probably include a substantial contribution from fluctuating phenotypic selection. We study the stochastic population dynamics of a population exposed to random (plus possibly directional) changes in the optimum phenotype for a quantitative trait that evolves in response to this moving optimum. We derive simple analytical predictions for the distribution of log population size over time both transiently and at stationarity under Gompertz density regulation. These predictions are well matched by population- and individual-based simulations. The log population size is approximately reverse gamma distributed, with a negative skew causing an excess of low relative to high population sizes, thus increasing extinction risk relative to a symmetric (e.g., normal) distribution with the same mean and variance. Our analysis reveals how the mean and variance of log population size change with the variance and autocorrelation of deviations of the evolving mean phenotype from the optimum. We apply our results to the analysis of evolutionary rescue in a stochastic environment and show that random fluctuations in the optimum can substantially increase extinction risk by both reducing the expected growth rate and increasing the variance of population size by several orders of magnitude.

Dispersal as a source of variation in age-specific reproductive strategies in a wild population of lizards.

Dispersal syndromes describe the patterns of covariation of morphological, behavioural, and life-history traits associated with dispersal. Studying dispersal syndromes is critical to understanding the demographic and genetic consequences of movements. Among studies describing the association of life-history traits with dispersal, there is anecdotal evidence suggesting that dispersal syndromes can vary with age. Recent theory also suggests that dispersive and philopatric individuals might have different age-specific reproductive efforts. In a wild population of the common lizard (Zootoca vivipara), we investigated whether dispersive and philopatric individuals have different age-specific reproductive effort, survival, offspring body condition, and offspring sex ratio. Consistent with theoretical predictions, we found that young dispersive females have a higher reproductive effort than young philopatric females. Our results also suggest that the early high investment in reproduction of dispersive females trades-off with an earlier onset of senescence than in philopatric females. We further found that young dispersive females produce smaller offspring in lower body condition than do young philopatric females. Overall, our results provide empirical evidence that dispersive and philopatric individuals have different age-specific life-history traits.

Optimal life-history strategy differs between philopatric and dispersing individuals in a metapopulation.

Abundant empirical evidence for dispersal syndromes contrasts with the rarity of theoretical predictions about the evolution of life-history divergence between dispersing and philopatric individuals. We use an evolutionary model to predict optimal differences in age-specific reproductive effort between dispersing and philopatric individuals inhabiting the same metapopulation. In our model, only young individuals disperse, and their lifelong reproductive decisions are potentially affected by this initial event. Juvenile survival declines as density of adults and other juveniles increases. We assume a trade-off between reproduction and survival, so that different patterns of age-specific reproductive effort lead to different patterns of aging. We find that young immigrant mothers should allocate more resources to reproduction than young philopatric mothers, but these life-history differences vanish as immigrant and philopatric individuals get older. However, whether the higher early reproductive effort of immigrants results in higher fecundity depends on the postimmigration cost on fecundity. Dispersing individuals have consequently a shorter life span. Ultimately, these life-history differences are due to the fact that young dispersing individuals most often live in recently founded populations, where competition is relaxed and juvenile survival higher, favoring larger investment in offspring production at the expense of survival.

The evolution of age-specific choosiness and reproductive isolation in a model with overlapping generations.

The strength of mate choice (choosiness) often varies with age, but theory to understand this variation is scarce. Additionally, theory has investigated the evolution of choosiness in speciation scenarios but has ignored that most organisms have overlapping generations. We investigate whether speciation can result in variation of choosiness with age, and whether such variation can in turn affect speciation. We develop a population-genetic model of the evolution of choosiness in organisms with overlapping generations in the context of secondary contact between two divergent populations. We assume that females choose males that match their phenotype, such that choosiness evolves by sexual selection. We demonstrate that speciation can result in the evolution of age-specific choosiness when the mating trait is under divergent ecological selection and age is not used as a mating cue. The cause of this result is that allele frequencies differ between choosy females and males. However, we find that the evolution of age-specific choosiness does not affect the overall level of reproductive isolation compared to a case without age-structure, supporting previous speciation theory. Overall, our results connect life history and speciation theory, and the mechanisms that we highlight have implications for the understanding of the role of sex-specific selection in the evolution of choosiness.

A dynamic eco-evolutionary model predicts slow response of alpine plants to climate warming.

Withstanding extinction while facing rapid climate change depends on a species' ability to track its ecological niche or to evolve a new one. Current methods that predict climate-driven species' range shifts use ecological modelling without eco-evolutionary dynamics. Here we present an eco-evolutionary forecasting framework that combines niche modelling with individual-based demographic and genetic simulations. Applying our approach to four endemic perennial plant species of the Austrian Alps, we show that accounting for eco-evolutionary dynamics when predicting species' responses to climate change is crucial. Perennial species persist in unsuitable habitats longer than predicted by niche modelling, causing delayed range losses; however, their evolutionary responses are constrained because long-lived adults produce increasingly maladapted offspring. Decreasing population size due to maladaptation occurs faster than the contraction of the species range, especially for the most abundant species. Monitoring of species' local abundance rather than their range may likely better inform on species' extinction risks under climate change.

Maladaptation as a source of senescence in habitats variable in space and time.

In this study, we use a quantitative genetics model of structured populations to investigate the evolution of senescence in a variable environment. Adaptation to local environments depends on phenotypic traits whose optimal values vary with age and with environmental conditions. We study different scenarios of environmental heterogeneity, where the environment changes abruptly, gradually, or cyclically with time and where the environment is heterogeneous in space with different populations connected by migration. The strength of selection decreases with age, which predicts slower adaptation of traits expressed late in the life cycle, potentially generating stronger senescence in habitats where selection changes in space or in time. This prediction is however complicated by the fact that the genetic variance also increases with age. Using numerical calculations, we found that the rate of senescence is generally increased when the environment varies. In particular, migration between different habitats is a source of senescence in heterogeneous landscapes. We also show that the rate of senescence can vary transiently when the population is not at equilibrium, with possible implications for experimental evolution and the study of invasive species. Our results highlight the need to study age-specific adaptation, as a changing environment can have a different impact on different age classes.