Is Evolution in Response to Extreme Events Good for Population Persistence?

AbstractClimate change is predicted to increase the severity of environmental perturbations, including storms and droughts, which act as strong selective agents. These extreme events are often of finite duration (pulse disturbances). Hence, while evolution during an extreme event may be adaptive, the resulting phenotypic changes may become maladaptive when the event ends. Using individual-based models and analytic approximations that fuse quantitative genetics and demography, we explore how heritability and phenotypic variance affect population size and extinction risk in finite populations under an extreme event of fixed duration. Since more evolution leads to greater maladaptation and slower population recovery following an extreme event, greater heritability can increase extinction risk when the extreme event is short. Alternatively, when an extreme event is sufficiently long, heritability often helps a population persist. We also find that when events are severe, the buffering effect of phenotypic variance can outweigh the increased load it causes.

Ecological limits to evolutionary rescue.

Environments change, for both natural and anthropogenic reasons, which can threaten species persistence. Evolutionary adaptation is a potentially powerful mechanism to allow species to persist in these changing environments. To determine the conditions under which adaptation will prevent extinction (evolutionary rescue), classic quantitative genetics models have assumed a constantly changing environment. They predict that species traits will track a moving environmental optimum with a lag that approaches a constant. If fitness is negative at this lag, the species will go extinct. There have been many elaborations of these models incorporating increased genetic realism. Here, we review and explore the consequences of four ecological complications: non-quadratic fitness functions, interacting density- and trait-dependence, species interactions and fundamental limits to adaptation. We show that non-quadratic fitness functions can result in evolutionary tipping points and existential crises, as can the interaction between density- and trait-dependent mortality. We then review the literature on how interspecific interactions affect adaptation and persistence. Finally, we suggest an alternative theoretical framework that considers bounded environmental change and fundamental limits to adaptation. A research programme that combines theory and experiments and integrates across organizational scales will be needed to predict whether adaptation will prevent species extinction in changing environments. This article is part of the theme issue 'Integrative research perspectives on marine conservation'.

Cooperation can promote rescue or lead to evolutionary suicide during environmental change.

The adaptation of populations to changing conditions may be affected by interactions between individuals. For example, when cooperative interactions increase fecundity, they may allow populations to maintain high densities and thus keep track of moving environmental optima. Simultaneously, changes in population density alter the marginal benefits of cooperative investments, creating a feedback loop between population dynamics and the evolution of cooperation. Here we model how the evolution of cooperation interacts with adaptation to changing environments. We hypothesize that environmental change lowers population size and thus promotes the evolution of cooperation, and that this, in turn, helps the population keep up with the moving optimum. However, we find that the evolution of cooperation can have qualitatively different effects, depending on which fitness component is reduced by the costs of cooperation. If the costs decrease fecundity, cooperation indeed speeds adaptation by increasing population density; if, in contrast, the costs decrease viability, cooperation may instead slow adaptation by lowering the effective population size, leading to evolutionary suicide. Thus, cooperation can either promote or-counterintuitively-hinder adaptation to a changing environment. Finally, we show that our model can also be generalized to other social interactions by discussing the evolution of competition during environmental change.

Genetic Signatures of Evolutionary Rescue by a Selective Sweep.

One of the most useful models in population genetics is that of a selective sweep and the consequent hitch-hiking of linked neutral alleles. While variations on this model typically assume constant population size, many instances of strong selection and rapid adaptation in nature may co-occur with complex demography. Here, we extend the hitch-hiking model to evolutionary rescue, where adaptation and demography not only co-occur but are intimately entwined. Our results show how this feedback between demography and evolution determines-and restricts-the genetic signatures of evolutionary rescue, and how these differ from the signatures of sweeps in populations of constant size. In particular, we find rescue to harden sweeps from standing variance or new mutation (but not from migration), reduce genetic diversity both at the selected site and genome-wide, and increase the range of observed Tajima's D values. For a given initial rate of population decline, the feedback between demography and evolution makes all of these differences more dramatic under weaker selection, where bottlenecks are prolonged. Nevertheless, it is likely difficult to infer the co-incident timing of the sweep and bottleneck from these simple signatures, never mind a feedback between them. Temporal samples spanning contemporary rescue events may offer one way forward.

Genetic Paths to Evolutionary Rescue and the Distribution of Fitness Effects Along Them.

The past century has seen substantial theoretical and empirical progress on the genetic basis of adaptation. Over this same period, a pressing need to prevent the evolution of drug resistance has uncovered much about the potential genetic basis of persistence in declining populations. However, we have little theory to predict and generalize how persistence-by sufficiently rapid adaptation-might be realized in this explicitly demographic scenario. Here, we use Fisher's geometric model with absolute fitness to begin a line of theoretical inquiry into the genetic basis of evolutionary rescue, focusing here on asexual populations that adapt through de novo mutations. We show how the dominant genetic path to rescue switches from a single mutation to multiple as mutation rates and the severity of the environmental change increase. In multi-step rescue, intermediate genotypes that themselves go extinct provide a "springboard" to rescue genotypes. Comparing to a scenario where persistence is assured, our approach allows us to quantify how a race between evolution and extinction leads to a genetic basis of adaptation that is composed of fewer loci of larger effect. We hope this work brings awareness to the impact of demography on the genetic basis of adaptation.

Parallel genetic evolution and speciation from standing variation.

Adaptation often proceeds from standing variation, and natural selection acting on pairs of populations is a quantitative continuum ranging from parallel to divergent. Yet, it is unclear how the extent of parallel genetic evolution during adaptation from standing variation is affected by the difference in the direction of selection between populations. Nor is it clear whether the availability of standing variation for adaptation affects progress toward speciation in a manner that depends on the difference in the direction of selection. We conducted a theoretical study investigating these questions and have two primary findings. First, the extent of parallel genetic evolution between two populations rapidly declines as selection changes from fully parallel toward divergent, and this decline is steeper in organisms with more traits (i.e., greater dimensionality). This rapid decline happens because small differences in the direction of selection greatly reduce the fraction of alleles that are beneficial in both populations. For example, populations adapting to optima separated by an angle of 33° might have only 50% of potentially beneficial alleles in common. Second, relative to when adaptation is from only new mutation, adaptation from standing variation improves hybrid fitness under parallel selection and reduces hybrid fitness under divergent selection. Under parallel selection, genetic parallelism from standing variation reduces the phenotypic segregation variance in hybrids, thereby increasing mean fitness in the parental environment. Under divergent selection, larger pleiotropic effects of alleles fixed from standing variation cause maladaptive transgressive phenotypes when combined in hybrids. Adaptation from standing genetic variation therefore slows progress toward speciation under parallel selection and facilitates progress toward speciation under divergent selection.

Evolutionarily stable communities: a framework for understanding the role of trait evolution in the maintenance of diversity.

Biological diversity depends on the interplay between evolutionary diversification and ecological mechanisms allowing species to coexist. Current research increasingly integrates ecology and evolution over a range of timescales, but our common conceptual framework for understanding species coexistence requires better incorporation of evolutionary processes. Here, we focus on the idea of evolutionarily stable communities (ESCs), which are theoretical endpoints of evolution in a community context. We use ESCs as a unifying framework to highlight some important but under-appreciated theoretical results, and we review empirical research relevant to these theoretical predictions. We explain how, in addition to generating diversity, evolution can also limit diversity by reducing the effectiveness of coexistence mechanisms. The coevolving traits of competing species may either diverge or converge, depending on whether the number of species in the community is low (undersaturated) or high (oversaturated) relative to the ESC. Competition in oversaturated communities can lead to extinction or neutrally coexisting, ecologically equivalent species. It is critical to consider trait evolution when investigating fundamental ecological questions like the strength of different coexistence mechanisms, the feasibility of ecologically equivalent species, and the interpretation of different patterns of trait dispersion.

An evolutionary tipping point in a changing environment.

Populations can persist in directionally changing environments by evolving. Quantitative genetic theory aims to predict critical rates of environmental change beyond which populations go extinct. Here, we point out that all current predictions effectively assume the same specific fitness function. This function causes selection on the standing genetic variance of quantitative traits to become increasingly strong as mean trait values depart from their optima. Hence, there is no bound on the rate of evolution and persistence is determined by the critical rate of environmental change at which populations cease to grow. We then show that biologically reasonable changes to the underlying fitness function can impose a qualitatively different extinction threshold. In particular, inflection points caused by weakening selection create local extrema in the strength of selection and thus in the rate of evolution. These extrema can produce evolutionary tipping points, where long-run population growth rates drop from positive to negative values without ever crossing zero. Generic early-warning signs of tipping points are found to have little power to detect imminent extinction, and require hard-to-gather data. Furthermore, we show how evolutionary tipping points produce evolutionary hysteresis, creating extinction debts.

When Predators Help Prey Adapt and Persist in a Changing Environment.

To persist in a changing world, populations must adapt. The ability to adapt is influenced by interactions with other species, such as predators. Recent experiments and theory suggest that selective pressures arising from predation may help prey adapt phenotypically to changing environments, but how this influences persistence remains unclear. In particular, it has not yet been shown whether predator-induced adaptation can outweigh predator-imposed reductions in population size, allowing prey to persist when they would otherwise go extinct. Here we examine if (and if so, how) predation can enhance the ability of prey to persist in a directionally changing environment. To do so, we extend a single-species quantitative-genetics framework that predicts rates of environmental change beyond which populations go extinct. While we assume predation decreases prey density, we find that predators can indeed help prey persist if they sufficiently increase prey adaptedness (decrease phenotypic lag). We show two ways this can occur: (1) the selective push, in which predators consume maladapted individuals and thus add selection that pushes the mean prey trait toward its optimum; and (2) the evolutionary hydra effect, when predation reduces prey density and thereby increases prey birthrate, allowing more selective events per unit time and effectively reducing generation time. We also discuss how our results apply more broadly to sources of mortality beyond predation.

Warming-Induced Changes to Body Size Stabilize Consumer-Resource Dynamics.

Both body size and temperature directly influence consumer-resource dynamics. There is also widespread empirical evidence for the temperature-size rule (TSR), which creates a negative relationship between temperature and body size. However, it is not known how the TSR affects community dynamics. Here we integrate temperature- and size-dependent models to include indirect effects of warming, through changes in body size, to answer the question, How does the TSR affect the predicted response of consumer-resource systems to warming? We find that the TSR is expected to maintain consumer-resource biomass ratios and buffer the community from extinctions under warming. While our results are limited to conditions where organisms are below their thermal optimum, they hold under a range of realistic temperature-size responses and are robust to the type of functional response. Our analyses suggest that the widely observed TSR may reduce the impacts of warming on consumer-resource systems.

Migratory orientation in a narrow avian hybrid zone.

BACKGROUND: Zones of contact between closely related taxa with divergent migratory routes, termed migratory divides, have been suggested as areas where hybrid offspring may have intermediate and inferior migratory routes, resulting in low fitness of hybrids and thereby promoting speciation. In the Rocky Mountains of Canada there is a narrow hybrid zone between Audubon's and myrtle warblers that is likely maintained by selection against hybrids. Band recoveries and isotopic studies indicate that this hybrid zone broadly corresponds to the location of a possible migratory divide, with Audubon's warblers migrating south-southwest and myrtle warblers migrating southeast. We tested a key prediction of the migratory divide hypothesis: that genetic background would be predictive of migratory orientation among warblers in the center of the hybrid zone. METHODS: We recorded fall migratory orientation of wild-caught migrating warblers in the center of the hybrid zone as measured by video-based monitoring of migratory restlessness in circular orientation chambers. We then tested whether there was a relationship between migratory orientation and genetic background, as measured using a set of species-specific diagnostic genetic markers. RESULTS: We did not detect a significant association between orientation and genetic background. There was large variation among individuals in orientation direction. Mean orientation was towards the NE, surprising for birds on fall migration, but aligned with the mountain valley in which the study took place. CONCLUSIONS: Only one other study has directly analyzed migratory orientation among naturally-produced hybrids in a migratory divide. While the other study showed an association between genetic background and orientation, we did not observe such an association in yellow-rumped warblers. We discuss possible reasons, including the possibility of a lack of a strong migratory divide in this hybrid zone and/or methodological limitations that may have prevented accurate measurements of long-distance migratory orientation.

Fitness-valley crossing with generalized parent-offspring transmission.

Simple and ubiquitous gene interactions create rugged fitness landscapes composed of coadapted gene complexes separated by "valleys" of low fitness. Crossing such fitness valleys allows a population to escape suboptimal local fitness peaks to become better adapted. This is the premise of Sewall Wright's shifting balance process. Here we generalize the theory of fitness-valley crossing in the two-locus, bi-allelic case by allowing bias in parent-offspring transmission. This generalization extends the existing mathematical framework to genetic systems with segregation distortion and uniparental inheritance. Our results are also flexible enough to provide insight into shifts between alternate stable states in cultural systems with "transmission valleys". Using a semi-deterministic analysis and a stochastic diffusion approximation, we focus on the limiting step in valley crossing: the first appearance of the genotype on the new fitness peak whose lineage will eventually fix. We then apply our results to specific cases of segregation distortion, uniparental inheritance, and cultural transmission. Segregation distortion favouring mutant alleles facilitates crossing most when recombination and mutation are rare, i.e., scenarios where crossing is otherwise unlikely. Interactions with more mutable genes (e.g., uniparental inherited cytoplasmic elements) substantially reduce crossing times. Despite component traits being passed on poorly in the previous cultural background, small advantages in the transmission of a new combination of cultural traits can greatly facilitate a cultural transition. While peak shifts are unlikely under many of the common assumptions of population genetic theory, relaxing some of these assumptions can promote fitness-valley crossing.