Stephanie M. Carlson

It's about time: the temporal dynamics of phenotypic selection in the wild.

Selection is a central process in nature. Although our understanding of the strength and form of selection has increased, a general understanding of the temporal dynamics of selection in nature is lacking. Here, we assembled a database of temporal replicates of selection from studies of wild populations to synthesize what we do (and do not) know about the temporal dynamics of selection. Our database contains 5519 estimates of selection from 89 studies, including estimates of both direct and indirect selection as well as linear and nonlinear selection. Morphological traits and studies focused on vertebrates were well-represented, with other traits and taxonomic groups less well-represented. Overall, three major features characterize the temporal dynamics of selection. First, the strength of selection often varies considerably from year to year, although random sampling error of selection coefficients may impose bias in estimates of the magnitude of such variation. Second, changes in the direction of selection are frequent. Third, changes in the form of selection are likely common, but harder to quantify. Although few studies have identified causal mechanisms underlying temporal variation in the strength, direction and form of selection, variation in environmental conditions driven by climatic fluctuations appear to be common and important.

Human predators outpace other agents of trait change in the wild

The observable traits of wild populations are continually shaped and reshaped by the environment and numerous agents of natural selection, including predators. In stark contrast with most predators, humans now typically exploit high proportions of prey populations and target large, reproductive-aged adults. Consequently, organisms subject to consistent and strong ‘harvest selection’ by fishers, hunters, and plant harvesters may be expected to show particularly rapid and dramatic changes in phenotype. However, a comparison of the rate at which phenotypic changes in exploited taxa occurs relative to other systems has never been undertaken. Here, we show that average phenotypic changes in 40 human-harvested systems are much more rapid than changes reported in studies examining not only natural (n = 20 systems) but also other human-driven (n = 25 systems) perturbations in the wild, outpacing them by >300% and 50%, respectively. Accordingly, harvested organisms show some of the most abrupt trait changes ever observed in wild populations, providing a new appreciation for how fast phenotypes are capable of changing. These changes, which include average declines of almost 20% in size-related traits and shifts in life history traits of nearly 25%, are most rapid in commercially exploited systems and, thus, have profound conservation and economic implications. Specifically, the widespread potential for transitively rapid and large effects on size- or life history-mediated ecological dynamics might imperil populations, industries, and ecosystems.

A review of quantitative genetic components of fitness in salmonids: implications for adaptation to future change

Salmonine fishes are commonly subjected to strong, novel selective pressures due to anthropogenic activities and global climate change, often resulting in population extinction. Consequently, there is considerable interest in predicting the long‐term evolutionary trajectories of extant populations. Knowledge of the genetic architecture of fitness traits is integral to making these predictions. We reviewed the published, peer‐reviewed literature for estimates of heritability and genetic correlation for fitness traits in salmonine fishes with two broad goals in mind: summarization of published data and testing for differences among categorical variables (e.g., species, life history type, experimental conditions). Balanced coverage of variables was lacking and estimates for wild populations and behavioral traits were nearly absent. Distributions of heritability estimates were skewed toward low values and distributions of genetic correlations toward large, positive values, suggesting that significant potential for evolution of traits exists. Furthermore, experimental conditions had a direct effect on h2 estimates, and other variables had more complex effects on h2 and rG estimates, suggesting that available estimates may be insufficient for use in models to predict evolutionary change in wild populations. Given this and other inherent complicating factors, making accurate predictions of the evolutionary trajectories of salmonine fishes will be a difficult task.

Synthetic analyses of phenotypic selection in natural populations: lessons, limitations and future directions

There are now thousands of estimates of phenotypic selection in natural populations, resulting in multiple synthetic reviews of these data. Here we consider several major lessons and limitations emerging from these syntheses, and how they may guide future studies of selection in the wild. First, we review past analyses of the patterns of directional selection. We present new meta-analyses that confirm differences in the direction and magnitude of selection for different types of traits and fitness components. Second, we describe patterns of temporal and spatial variation in directional selection, and their implications for cumulative selection and directional evolution. Meta-analyses suggest that sampling error contributes importantly to observed temporal variation in selection, and indicate that evidence for frequent temporal changes in the direction of selection in natural populations is limited. Third, we review the apparent lack of evidence for widespread stabilizing selection, and discuss biological and methodological explanations for this pattern. Finally, we describe how sampling error, statistical biases, choice of traits, fitness measures and selection metrics, environmental covariance and other factors may limit the inferences we can draw from analyses of selection coefficients. Current standardized selection metrics based on simple parametric statistical models may be inadequate for understanding patterns of non-linear selection and complex fitness surfaces. We highlight three promising areas for expanding our understanding of selection in the wild: (1) field studies of stabilizing selection, selection on physiological and behavioral traits, and the ecological causes of selection; (2) new statistical models and methods that connect phenotypic variation to population demography and selection; and (3) availability of the underlying individual-level data sets from past and future selection studies, which will allow comprehensive modeling of selection and fitness variation within and across systems, rather than meta-analyses of standardized selection metrics.

Evolutionary rescue in a changing world.

Evolutionary rescue occurs when adaptive evolutionary change restores positive growth to declining populations and prevents extinction. Here we outline the diagnostic features of evolutionary rescue and distinguish this phenomenon from demographic and genetic rescue. We then synthesize the rapidly accumulating theoretical and experimental studies of evolutionary rescue, highlighting the demographic, genetic, and extrinsic factors that affect the probability of rescue. By doing so, we clarify the factors to target through management and conservation. Additionally, we identify several putative cases of evolutionary rescue in nature, but conclude that compelling evidence remains elusive. We conclude with a horizon scan of where the field might develop, highlighting areas of potential application, and suggest areas where experimental evaluation will help to evaluate theoretical predictions.

Trait changes in a harvested population are driven by a dynamic tug-of-war between natural and harvest selection

Selective harvest of large individuals should alter natural adaptive landscapes and drive evolution toward reduced somatic growth and increased reproductive investment. However, few studies have simultaneously considered the relative importance of artificial and natural selection in driving trait changes in wild populations. Using 50 years of individual-based data on Windermere pike (Esox lucius), we show that trait changes tracked the adaptive peak, which moved in the direction imposed by the dominating selective force. Individual lifetime somatic growth decreased at the start of the time series because harvest selection was strong and natural selection was too weak to override the strength of harvest selection. However, natural selection favoring fast somatic growth strengthened across the time series in parallel with the increase in pike abundance and, presumably, cannibalism. Harvest selection was overridden by natural selection when the fishing effort dwindled, triggering a rapid increase in pike somatic growth. The two selective forces appear to have acted in concert during only one short period of prey collapse that favored slow-growing pike. Moreover, increased somatic growth occurred concurrently with a reduction in reproductive investment in young and small female pike, indicating a tradeoff between growth and reproduction. The age-specific amplitude of this change paralleled the age-specific strength of harvest pressure, suggesting that reduced investment was also a response to increased life expectancy. This is the first study to demonstrate that a consideration of both natural selection and artificial selection is needed to fully explain time-varying trait dynamics in harvested populations.

The spatial patterns of directional phenotypic selection.

Local adaptation, adaptive population divergence and speciation are often expected to result from populations evolving in response to spatial variation in selection. Yet, we lack a comprehensive understanding of the major features that characterise the spatial patterns of selection, namely the extent of variation among populations in the strength and direction of selection. Here, we analyse a data set of spatially replicated studies of directional phenotypic selection from natural populations. The data set includes 60 studies, consisting of 3937 estimates of selection across an average of five populations. We performed meta-analyses to explore features characterising spatial variation in directional selection. We found that selection tends to vary mainly in strength and less in direction among populations. Although differences in the direction of selection occur among populations they do so where selection is often weakest, which may limit the potential for ongoing adaptive population divergence. Overall, we also found that spatial variation in selection appears comparable to temporal (annual) variation in selection within populations; however, several deficiencies in available data currently complicate this comparison. We discuss future research needs to further advance our understanding of spatial variation in selection.

Differences in the temporal dynamics of phenotypic selection among fitness components in the wild

The balance of selection acting through different fitness components (e.g. fecundity, mating success, survival) determines the potential tempo and trajectory of adaptive evolution. Yet the extent to which the temporal dynamics of phenotypic selection may vary among fitness components is poorly understood. Here, we compiled a database of 3978 linear selection coefficients from temporally replicated studies of selection in wild populations to address this question. Across studies, we find that multi-year selection through mating success and fecundity is stronger than selection through survival, but varies less in direction. We also report that selection through mating success varies more in long-term average strength than selection through either survival or fecundity. The consistency in direction and stronger long-term average strength of selection through mating success and fecundity suggests that selection through these fitness components should cause more persistent directional evolution relative to selection through survival. Similar patterns were apparent for the subset of studies that evaluated the temporal dynamics of selection on traits simultaneously using several different fitness components, but few such studies exist. Taken together, these results reveal key differences in the temporal dynamics of selection acting through different fitness components, but they also reveal important limitations in our understanding of how selection drives adaptive evolution.

Recent shifts in the occurrence, cause, and magnitude of animal mass mortality events

Significance Mass mortality events (MMEs), the rapid, catastrophic die-off of organisms, are an example of a rare event affecting natural populations. Individual reports of MMEs clearly demonstrate their ecological and evolutionary importance, yet our understanding of the general features characterizing such events is limited. Here, we conducted the first, to our knowledge, quantitative analysis of MMEs across the animal kingdom, and as such, we were able to explore novel patterns, trends, and features associated with MMEs. Our analysis uncovered the surprising finding that there have been recent shifts in the magnitudes of MMEs and their associated causes. Our database allows the recommendation of improvements for data collection in ways that will enhance our understanding of how MMEs relate to ongoing perturbations to ecosystems. Mass mortality events (MMEs) are rapidly occurring catastrophic demographic events that punctuate background mortality levels. Individual MMEs are staggering in their observed magnitude: removing more than 90% of a population, resulting in the death of more than a billion individuals, or producing 700 million tons of dead biomass in a single event. Despite extensive documentation of individual MMEs, we have no understanding of the major features characterizing the occurrence and magnitude of MMEs, their causes, or trends through time. Thus, no framework exists for contextualizing MMEs in the wake of ongoing global and regional perturbations to natural systems. Here we present an analysis of 727 published MMEs from across the globe, affecting 2,407 animal populations. We show that the magnitude of MMEs has been intensifying for birds, fishes, and marine invertebrates; invariant for mammals; and decreasing for reptiles and amphibians. These shifts in magnitude proved robust when we accounted for an increase in the occurrence of MMEs since 1940. However, it remains unclear whether the increase in the occurrence of MMEs represents a true pattern or simply a perceived increase. Regardless, the increase in MMEs appears to be associated with a rise in disease emergence, biotoxicity, and events produced by multiple interacting stressors, yet temporal trends in MME causes varied among taxa and may be associated with increased detectability. In addition, MMEs with the largest magnitudes were those that resulted from multiple stressors, starvation, and disease. These results advance our understanding of rare demographic processes and their relationship to global and regional perturbations to natural systems.

Transportation of Pacific salmon carcasses from streams to riparian forests by bears

Predation on Pacific salmon by bears (genus Ursus L., 1758) can be an important ecosystem process because the spatial distribution of carcasses largely determines whether marine-derived nutrients cycle through aquatic or terrestrial pathways. Direct observations on three streams in southeastern Alaska indicated that 49% of the pink (Oncorhynchus gorbuscha (Walbaum, 1792)) and chum (Oncorhynchus keta (Walbaum in Artedi, 1792)) salmon killed by bears were carried into the forest. The tendency of bears to transport carcasses was independent of the sex and species of salmon, but unspawned fish were more often transported than fish that had completed spawning. Data on tagged sockeye salmon (Oncorhynchus nerka (Walbaum in Artedi, 1792)) in one southwestern Alaska stream indicated that 42.6% of the killed salmon were transported, and that higher percentages were transported in years when salmon densities were greater. At six other streams, on average, 68.1% of the sockeye salmon killed were apparently transporte...