Adam M. Siepielski

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.

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.

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.

Precipitation drives global variation in natural selection

Climate-driven selection Climate change will fundamentally alter many aspects of the natural world. To understand how species may adapt to this change, we must understand which aspects of the changing climate exert the most powerful selective forces. Siepielski et al. looked at studies of selection across species and regions and found that, across biomes, the strongest sources of selection were precipitation and transpiration changes. Importantly, local and regional climate change explained patterns of selection much more than did global change. Science, this issue p. 959 Local and regional climate changes in rainfall explain patterns of species selection across biomes more than global change. Climate change has the potential to affect the ecology and evolution of every species on Earth. Although the ecological consequences of climate change are increasingly well documented, the effects of climate on the key evolutionary process driving adaptation—natural selection—are largely unknown. We report that aspects of precipitation and potential evapotranspiration, along with the North Atlantic Oscillation, predicted variation in selection across plant and animal populations throughout many terrestrial biomes, whereas temperature explained little variation. By showing that selection was influenced by climate variation, our results indicate that climate change may cause widespread alterations in selection regimes, potentially shifting evolutionary trajectories at a global scale.

NONCONSUMPTIVE PREDATOR‐DRIVEN MORTALITY CAUSES NATURAL SELECTION ON PREY

Predators frequently exert natural selection through differential consumption of their prey. However, predators may also cause prey mortality through nonconsumptive effects, which could cause selection if different prey phenotypes are differentially susceptible to this nonconsumptive mortality. Here we present an experimental test of this hypothesis, which reveals that nonconsumptive mortality imposed by predatory dragonflies causes selection on their damselfly prey favoring increased activity levels. These results are consistent with other studies of predator‐driven selection, however, they reveal that consumption alone is not the only mechanism by which predators can exert selection on prey. Uncovering this mechanism also suggests that prey defensive traits may represent adaptations to not only avoid being consumed, but also for dealing with other sources of mortality caused by predators. Demonstrating selection through both consumptive and nonconsumptive predator mortality provides us with insight into the diverse effects of predators as an evolutionary force.

Experimental Evidence for an Eco-Evolutionary Coupling between Local Adaptation and Intraspecific Competition

Determining how adaptive evolution can be coupled to ecological processes is key for developing a more integrative understanding of the demographic factors that regulate populations. Intraspecific competition is an especially important ecological process because it generates negative density dependence in demographic rates. Although ecological factors are most often investigated to determine the strength of density dependence, evolutionary processes such as local adaptation could also feed back to shape variation in the strength of density dependence among populations. Using an experimental approach with damselflies, a predaceous aquatic insect, we find evidence that both density-dependent intraspecific competition and local adaptation can reduce per capita growth rates. In some cases, the effects of local adaptation on reducing per capita growth rates exceeded the ecological competitive effects of a doubling of density. However, we also found that these ecological and evolutionary properties of populations are coupled, and we offer two interpretations of the causes underlying this pattern: (1) the strength of density-dependent competition depends on the extent of local adaptation, or (2) the extent of local adaptation is shaped by the strength of density-dependent competition. Regardless of the underlying causal pathway, these results show how eco-evolutionary dynamics can affect a key demographic process regulating populations.

Adaptive evolution to novel predators facilitates the evolution of damselfly species range shifts

Most species have evolved adaptations to reduce the chances of predation. In many cases, adaptations to coexist with one predator generate tradeoffs in the ability to live with other predators. Consequently, the ability to live with one predator may limit the geographic distributions of species, such that adaptive evolution to coexist with novel predators may facilitate range shifts. In a case study with Enallagma damselflies, we used a comparative phylogenetic approach to test the hypothesis that adaptive evolution to live with a novel predator facilitates range size shifts. Our results suggest that the evolution of Enallagma shifting from living in ancestral lakes with fish as top predators, to living in lakes with dragonflies as predators, may have facilitated an increase in their range sizes. This increased range size likely arose because lakes with dragonflies were widespread, but unavailable as a habitat throughout much of the evolutionary history of Enallagma because they were historically maladapted to coexist with dragonfly predators. Additionally, the traits that have evolved as defenses against dragonflies also likely enhanced damselfly dispersal abilities. While many factors underlie the evolutionary history of species ranges, these results suggest a role for the evolution of predator‐prey interactions.

Predator olfactory cues generate a foraging–predation trade-off through prey apprehension

Most animals are faced with the challenge of securing food under the risk of predation. This frequently generates a trade-off whereby animals respond to predator cues with reduced movement to avoid predation at the direct cost of reduced foraging success. However, predators may also cause prey to be apprehensive in their foraging activities, which would generate an indirect ‘apprehension cost’. Apprehension arises when a forager redirects attention from foraging tasks to predator detection and incurs a cost from such multi-tasking, because the forager ends up making more mistakes in its foraging tasks as a result. Here, we test this apprehension cost hypothesis and show that damselflies miss a greater proportion of their prey during foraging bouts in response to both olfactory cues produced by conspecifics that have only viewed a fish predator and olfactory cues produced directly by fish. This reduced feeding efficiency is in addition to the stereotypical anti-predator response of reduced activity, which we also observed. These results show that costs associated with anti-predator responses not only arise through behavioural alterations that reduce the risk of predation, but also from the indirect costs of apprehension and multi-tasking that can reduce feeding efficiency under the threat of predation.

Climate extremes are associated with invertebrate taxonomic and functional composition in mountain lakes

Abstract Climate change is expected to increase climate variability and the occurrence of extreme climatic events, with potentially devastating effects on aquatic ecosystems. However, little is known about the role of climate extremes in structuring aquatic communities or the interplay between climate and local abiotic and biotic factors. Here, we examine the relative influence of climate and local abiotic and biotic conditions on biodiversity and community structure in lake invertebrates. We sampled aquatic invertebrates and measured environmental variables in 19 lakes throughout California, USA, to test hypotheses of the relationship between climate, local biotic and environmental conditions, and the taxonomic and functional structure of aquatic invertebrate communities. We found that, while local biotic and abiotic factors such as habitat availability and conductivity were the most consistent predictors of alpha diversity, extreme climate conditions such as maximum summer temperature and dry‐season precipitation were most often associated with multivariate taxonomic and functional composition. Specifically, sites with high maximum temperatures and low dry‐season precipitation housed communities containing high abundances of large predatory taxa. Furthermore, both climate dissimilarity and abiotic dissimilarity determined taxonomic turnover among sites (beta diversity). These findings suggest that while local‐scale environmental variables may predict alpha diversity, climatic variability is important to consider when projecting broad‐scale aquatic community responses to the extreme temperature and precipitation events that are expected for much of the world during the next century.

Opportunistic data reveal widespread species turnover in Enallagma damselflies at biogeographical scales

An information tradeoff exists between systematic presence/absence surveys and purely opportunistic (presence-only) records for investigating the geography of community structure. Opportunistic species occurrence data may be of relatively limited quality, but typically involves numerous observations and species. Given the quality-quantity tradeoff, what can opportunistic data reveal about spatial patterns in community structure? Here we explore opportunistic data in describing geographic patterns of species composition, using over 4,600 occurrence records of Enallagma damselflies in the United States. We tested phylogenetic scale (genus level, Enallagma major clades, Enallagma subclades) and spatial extent (U.S. vs. watershed regions), hypothesizing that nonrandom structure is more likely at larger spatial extents. We also used three sets of systematic presence/absence surveys as a benchmark for validating opportunistic presence-only records. Null model analysis of matrix coherence and species replacements showed many cases of nonrandom structure and widespread species turnover. This outcome was repeated across spatial and environmental gradients and community composition scenarios. Turnover dominated across the U.S. and two watersheds spanning biogeographic boundaries, but random assemblages were prevalent in a third watershed with limited longitudinal extent. Turnover also pervaded each level of phylogeny. Opportunistic presence-only datasets showed identical patterns as systematic presence/absence datasets. These results indicate that extensive opportunistic data can be used to detect species turnover, especially at geographic scales where range margins are crossed. This article is protected by copyright. All rights reserved.