When and how can we predict adaptive responses to climate change?

Predicting if, when, and how populations can adapt to climate change constitutes one of the greatest challenges in science today. Here, we build from contributions to the special issue on evolutionary adaptation to climate change, a survey of its authors, and recent literature to explore the limits and opportunities for predicting adaptive responses to climate change. We outline what might be predictable now, in the future, and perhaps never even with our best efforts. More accurate predictions are expected for traits characterized by a well-understood mapping between genotypes and phenotypes and traits experiencing strong, direct selection due to climate change. A meta-analysis revealed an overall moderate trait heritability and evolvability in studies performed under future climate conditions but indicated no significant change between current and future climate conditions, suggesting neither more nor less genetic variation for adapting to future climates. Predicting population persistence and evolutionary rescue remains uncertain, especially for the many species without sufficient ecological data. Still, when polled, authors contributing to this special issue were relatively optimistic about our ability to predict future evolutionary responses to climate change. Predictions will improve as we expand efforts to understand diverse organisms, their ecology, and their adaptive potential. Advancements in functional genomic resources, especially their extension to non-model species and the union of evolutionary experiments and "omics," should also enhance predictions. Although predicting evolutionary responses to climate change remains challenging, even small advances will reduce the substantial uncertainties surrounding future evolutionary responses to climate change.

Macroecological predictors of evolutionary and plastic potential do not apply at microgeographic scales for a freshwater cladoceran under climate change.

Rapid evolutionary adaptation could reduce the negative impacts of climate change if sufficient heritability of key traits exists under future climate conditions. Plastic responses to climate change could also reduce negative impacts. Understanding which populations are likely to respond via evolution or plasticity could therefore improve estimates of extinction risk. A large body of research suggests that the evolutionary and plastic potential of a population can be predicted by the degree of spatial and temporal climatic variation it experiences. However, we know little about the scale at which these relationships apply. Here, we test if spatial and temporal variation in temperature affects genetic variation and plasticity of fitness and a key thermal tolerance trait (critical thermal maximum; CTmax) at microgeographic scales using a metapopulation of Daphnia magna in freshwater rock pools. Specifically, we ask if (a) there is a microgeographic adaptation of CTmax and fitness to differences in temperature among the pools, (b) pools with greater temporal temperature variation have more genetic variation or plasticity in CTmax or fitness, and (c) increases in temperature affect the heritability of CTmax and fitness. Although we observed genetic variation and plasticity in CTmax and fitness, and differences in fitness among pools, we did not find support for the predicted relationships between temperature variation and genetic variation or plasticity. Furthermore, the genetic variation and plasticity we observed in CTmax are unlikely sufficient to reduce the impacts of climate change. CTmax plasticity was minimal and heritability was 72% lower when D. magna developed at the higher temperatures predicted under climate change. In contrast, the heritability of fitness increased by 53% under warmer temperatures, suggesting an increase in overall evolutionary potential unrelated to CTmax under climate change. More research is needed to understand the evolutionary and plastic potential under climate change and how that potential will be altered in future climates.

Population genomic structure of a widespread, urban-dwelling mammal: The eastern grey squirrel (Sciurus carolinensis).

Urbanization is a persistent and widespread driver of global environmental change, potentially shaping evolutionary processes due to genetic drift and reduced gene flow in cities induced by habitat fragmentation and small population sizes. We tested this prediction for the eastern grey squirrel (Sciurus carolinensis), a common and conspicuous forest-dwelling rodent, by obtaining 44K SNPs using reduced representation sequencing (ddRAD) for 403 individuals sampled across the species' native range in eastern North America. We observed moderate levels of genetic diversity, low levels of inbreeding, and only a modest signal of isolation-by-distance. Clustering and migration analyses show that estimated levels of migration and genetic connectivity were higher than expected across cities and forested areas, specifically within the eastern portion of the species' range dominated by urbanization, and genetic connectivity was less than expected within the western range where the landscape is fragmented by agriculture. Landscape genetic methods revealed greater gene flow among individual squirrels in forested regions, which likely provide abundant food and shelter for squirrels. Although gene flow appears to be higher in areas with more tree cover, only slight discontinuities in gene flow suggest eastern grey squirrels have maintained connected populations across urban areas in all but the most heavily fragmented agricultural landscapes. Our results suggest urbanization shapes biological evolution in wildlife species depending strongly on the composition and habitability of the landscape matrix surrounding urban areas.

A global horizon scan for urban evolutionary ecology.

Research on the evolutionary ecology of urban areas reveals how human-induced evolutionary changes affect biodiversity and essential ecosystem services. In a rapidly urbanizing world imposing many selective pressures, a time-sensitive goal is to identify the emergent issues and research priorities that affect the ecology and evolution of species within cities. Here, we report the results of a horizon scan of research questions in urban evolutionary ecology submitted by 100 interdisciplinary scholars. We identified 30 top questions organized into six themes that highlight priorities for future research. These research questions will require methodological advances and interdisciplinary collaborations, with continued revision as the field of urban evolutionary ecology expands with the rapid growth of cities.

Asynchrony, density dependence, and persistence in an amphibian.

Understanding drivers of metapopulation dynamics remains a critical challenge for ecology and conservation. In particular, the degree of synchrony in metapopulation dynamics determines how resilient a metapopulation is to a widespread disturbance. In this study, we used 21 years of egg mass count data across 64 nonpermanent freshwater ponds in Connecticut, USA to evaluate patterns of abundance and growth and to assess regional as well as local factors in shaping the population dynamics of wood frogs (Rana sylvatica = Lithobates sylvaticus). In particular, we asked whether a species known to undergo metapopulation dynamics exhibited spatial synchrony in abundances. With the exception of a single year when breeding took place during severe drought conditions, our analyses revealed no evidence of synchrony despite close proximity (mean minimum distance < 300 m) of breeding ponds across the 3213-ha study area. Instead, local, pond-scale conditions best predicted patterns of abundance and population growth rate. We found negative density dependence on population growth rate within ponds as well as evidence that larger neighboring pond populations had a negative effect on focal ponds. Beyond density, pond depth was a critical predictor; deeper ponds supported larger populations. Drought conditions and warm winters negatively affected populations. Overall, breeding ponds vary in critical ways that either support larger, more persistent populations or smaller populations that are not represented by breeding pairs in some years. The infrequency of spatial synchrony in this system is surprising and suggests greater resilience to stressors than would have been expected if dynamics were strongly synchronized. More generally, understanding the characteristics of systems that determine synchronous population dynamics will be critical to predicting which species are more or less resilient to widespread disturbances like land conversion or climate change.

Cool microrefugia accumulate and conserve biodiversity under climate change.

A major challenge in climate change biology is to explain why the impacts of climate change vary around the globe. Microclimates could explain some of this variation, but climate change biologists often overlook microclimates because they are difficult to map. Here, we map microclimates in a freshwater rock pool ecosystem and evaluate how accounting for microclimates alters predictions of climate change impacts on aquatic invertebrates. We demonstrate that average maximum temperature during the growing season can differ by 9.9-11.6°C among microclimates less than a meter apart and this microclimate variation might increase by 21% in the future if deeper pools warm less than shallower pools. Accounting for this microclimate variation significantly alters predictions of climate change impacts on aquatic invertebrates. Predictions that exclude microclimates predict low future occupancy (0.08-0.32) and persistence probabilities (2%-73%) for cold-adapted taxa, and therefore predict decreases in gamma richness and a substantial shift toward warm-adapted taxa in local communities (i.e., thermophilization). However, predictions incorporating microclimates suggest cool locations will remain suitable for cold-adapted taxa in the future, no change in gamma richness, and 825% less thermophilization. Our models also suggest that cool locations will become suitable for warm-adapted taxa and will therefore accumulate biodiversity in the future, which makes cool locations essential for biodiversity conservation. Simulated protection of the 10 coolest microclimates (9% of locations on the landscape) results in a 100% chance of conserving all focal taxa in the future. In contrast, protecting the 10 currently most biodiverse locations, a commonly employed conservation strategy, results in a 3% chance of conserving all focal taxa in the future. Our study suggests that we must account for microclimates if we hope to understand the future impacts of climate change and design effective conservation strategies to limit biodiversity loss.

Microgeographic evolution of metabolic physiology in a salamander metapopulation.

The Metabolic Theory of Ecology explains ecological variation spanning taxonomic organization, space, and time based on universal physiological relationships. The theory depends on two core parameters: the normalization constant, a mass-independent measure of metabolic rate expected to be invariant among similar species, and the scaling coefficient, a measure of metabolic change with body mass commonly assumed to follow the universal 3/4 scaling law. However, emerging evidence for adaptive microevolution of metabolic rates led us to hypothesize that metabolic rate might exhibit evolved variation among populations on microgeographic scales. To evaluate our hypothesis, we explored evidence for evolved variation in the scaling coefficient and normalization constant within a spotted salamander (Ambystoma maculatum) metapopulation in Connecticut, USA. We measured standard metabolic rate in common-garden raised spotted salamanders from 22 different populations and tested for the effects of six ecological variables suspected in advance to select for divergent physiology. We found that metabolic rate rose with body mass with a log-log slope of 0.97 that was statistically different from the expected 3/4 scaling law. Although we found no evidence for interpopulation variation in the scaling coefficient, we found evidence for interpopulation variation in the normalization constants among populations. Metabolic variation was best explained by differences in population density among ponds. Our results provide mixed support for Metabolic Theory of Ecology assumptions about parameter invariance and illustrate how fundamental physiological processes such as metabolic rate can evolve across microgeographic spatial scales.

Balancing selection and drift in a polymorphic salamander metapopulation.

Understanding how genetic variation is maintained in a metapopulation is a longstanding problem in evolutionary biology. Historical resurveys of polymorphisms have offered efficient insights about evolutionary mechanisms, but are often conducted on single, large populations, neglecting the more comprehensive view afforded by considering all populations in a metapopulation. Here, we resurveyed a metapopulation of spotted salamanders (Ambystoma maculatum) to understand the evolutionary drivers of frequency variation in an egg mass colour polymorphism. We found that this metapopulation was demographically, phenotypically and environmentally stable over the last three decades. However, further analysis revealed evidence for two modes of evolution in this metapopulation-genetic drift and balancing selection. Although we cannot identify the balancing mechanism from these data, our findings present a clear view of contemporary evolution in colour morph frequency and demonstrate the importance of metapopulation-scale studies for capturing a broad range of evolutionary dynamics.

Adaptation reduces competitive dominance and alters community assembly.

A growing body of theory predicts that evolution of an early-arriving species in a new environment can produce a competitive advantage against later arriving species, therefore altering community assembly (i.e. the community monopolization hypothesis). Applications of the community monopolization hypothesis are increasing. However, experimental tests of the hypothesis are rare. Here, we provide a rare experimental demonstration of the community monopolization hypothesis using two archaeal species. We first expose one species to low- and high-temperature environments for 135 days. Populations in the high-temperature treatment evolved a 20% higher median performance when grown at high temperature. We then demonstrate that early arrival and adaptation reduce the abundance of a late-arriving species in the high-temperature environment by 63% relative to when both species arrive simultaneously and neither species is adapted to high temperature. These results are consistent with the community monopolization hypothesis and suggest that adaptation can reduce competitive dominance to alter community assembly. Hence, community monopolization might be much more common in nature than previously assumed. Our results strongly support the idea that patterns of biodiversity might often stem from a race between local adaptation and colonization of pre-adapted species.

Socio-eco-evolutionary dynamics in cities.

Cities are uniquely complex systems regulated by interactions and feedbacks between nature and human society. Characteristics of human society-including culture, economics, technology and politics-underlie social patterns and activity, creating a heterogeneous environment that can influence and be influenced by both ecological and evolutionary processes. Increasing research on urban ecology and evolutionary biology has coincided with growing interest in eco-evolutionary dynamics, which encompasses the interactions and reciprocal feedbacks between evolution and ecology. Research on both urban evolutionary biology and eco-evolutionary dynamics frequently focuses on contemporary evolution of species that have potentially substantial ecological-and even social-significance. Still, little work fully integrates urban evolutionary biology and eco-evolutionary dynamics, and rarely do researchers in either of these fields fully consider the role of human social patterns and processes. Because cities are fundamentally regulated by human activities, are inherently interconnected and are frequently undergoing social and economic transformation, they represent an opportunity for ecologists and evolutionary biologists to study urban "socio-eco-evolutionary dynamics." Through this new framework, we encourage researchers of urban ecology and evolution to fully integrate human social drivers and feedbacks to increase understanding and conservation of ecosystems, their functions and their contributions to people within and outside cities.

Microgeographic divergence of functional responses among salamanders under antagonistic selection from apex predators.

A predator's functional response determines predator-prey interactions by describing the relationship between the number of prey available and the number eaten. Its shape and parameters fundamentally govern the dynamic equilibrium of predator-prey interactions and their joint abundances. Yet, estimates of these key parameters generally assume stasis in space and time and ignore the potential for local adaptation to alter feeding responses and the stability of trophic dynamics. Here, we evaluate if functional responses diverge among populations of spotted salamander (Ambystoma maculatum) larvae that face antagonistic selection on feeding strategies based on their own risk of predation. Common garden experiments revealed that spotted salamander from ponds with varying predation risks differed in their functional responses, suggesting an evolutionary response. Applying mechanistic equations, we discovered that the combined changes in attack rates, handling times and shape of the functional response enhanced feeding rate in environments with high densities of gape-limited predators. We suggest how these parameter changes could alter community equilibria and other emergent properties of food webs. Community ecologists might often need to consider how local evolution at fine scales alters key relationships in ways that alter local diversity patterns, food web dynamics, resource gradients and community responses to disturbance.

Seasonality and uncertainty in global COVID-19 growth rates.

The virus causing COVID-19 has spread rapidly worldwide and threatens millions of lives. It remains unknown, as of April 2020, whether summer weather will reduce its spread, thereby alleviating strains on hospitals and providing time for vaccine development. Early insights from laboratory studies and research on related viruses predicted that COVID-19 would decline with higher temperatures, humidity, and ultraviolet (UV) light. Using current, fine-scaled weather data and global reports of infections, we develop a model that explains 36% of the variation in maximum COVID-19 growth rates based on weather and demography (17%) and country-specific effects (19%). UV light is most strongly associated with lower COVID-19 growth. Projections suggest that, without intervention, COVID-19 will decrease temporarily during summer, rebound by autumn, and peak next winter. Validation based on data from May and June 2020 confirms the generality of the climate signal detected. However, uncertainty remains high, and the probability of weekly doubling rates remains >20% throughout summer in the absence of social interventions. Consequently, aggressive interventions will likely be needed despite seasonal trends.

Evolutionary origins for ecological patterns in space.

Historically, many biologists assumed that evolution and ecology acted independently because evolution occurred over distances too great to influence most ecological patterns. Today, evidence indicates that evolution can operate over a range of spatial scales, including fine spatial scales. Thus, evolutionary divergence across space might frequently interact with the mechanisms that also determine spatial ecological patterns. Here, we synthesize insights from 500 eco-evolutionary studies and develop a predictive framework that seeks to understand whether and when evolution amplifies, dampens, or creates ecological patterns. We demonstrate that local adaptation can alter everything from spatial variation in population abundances to ecosystem properties. We uncover 14 mechanisms that can mediate the outcome of evolution on spatial ecological patterns. Sometimes, evolution amplifies environmental variation, especially when selection enhances resource uptake or patch selection. The local evolution of foundation or keystone species can create ecological patterns where none existed originally. However, most often, we find that evolution dampens existing environmental gradients, because local adaptation evens out fitness across environments and thus counteracts the variation in associated ecological patterns. Consequently, evolution generally smooths out the underlying heterogeneity in nature, making the world appear less ragged than it would be in the absence of evolution. We end by highlighting the future research needed to inform a fully integrated and predictive biology that accounts for eco-evolutionary interactions in both space and time.

Developmental temperature influences color polymorphism but not hatchling size in a woodland salamander.

Phenotypic plasticity can be an important adaptive response to climate change, particularly for dispersal-limited species. Temperature frequently alters developmental and phenotypic traits including morphology, behavior, and reproductive cycles. We often lack crucial information about if and how thermal conditions during development will interact with genetic responses and facilitate persistence or adaptation under climate change. Polymorphic species offer an ideal test for this, as alternative morphs often confer differential adaptive advantages. However, few studies have examined the effects of incubation temperature on color expression or development in polymorphic taxa. Here we test if developmental temperature mediates morph frequency in the polymorphic salamander Plethodon cinereus. Although previous research suggests geographic variation in morph proportions results from differential climate adaptation, it remains unknown if plasticity also contributes to this variation. We used a split-clutch common garden experiment to determine the effects of developmental temperature on the color and development of P. cinereus. Our results indicate developmental temperature affects coloration in P. cinereus, either via plasticity or differential mortality, with eggs incubated at warmer temperatures yielding a higher proportion of unstriped individuals than those from cooler temperatures. This temperature response may contribute to the spatial variation in morph frequencies in natural populations. Surprisingly, we found neither temperature nor egg size affected hatchling size. Our study provides important insights into the potential for climate-induced responses to preserve diversity in dispersal-limited species, like P. cinereus, and enable time for adaptive evolution.

Maladapted Prey Subsidize Predators and Facilitate Range Expansion.

Dispersal of prey from predator-free patches frequently supplies a trophic subsidy to predators by providing more prey than are produced locally. Prey arriving from predator-free patches might also have evolved weaker defenses against predators and thus enhance trophic subsidies by providing easily captured prey. Using local models assuming a linear or accelerating trade-off between defense and population growth rate, we demonstrate that immigration of undefended prey increased predator abundances and decreased defended prey through eco-evolutionary apparent competition. In individual-based models with spatial structure, explicit genetics, and gene flow along an environmental gradient, prey became maladapted to predators at the predator's range edge, and greater gene flow enhanced this maladaptation. The predator gained a subsidy from these easily captured prey, which enhanced its abundance, facilitated its persistence in marginal habitats, extended its range extent, and enhanced range shifts during environmental changes, such as climate change. Once the predator expanded, prey adapted to it and the advantage disappeared, resulting in an elastic predator range margin driven by eco-evolutionary dynamics. Overall, the results indicate a need to consider gene flow-induced maladaptation and species interactions as mutual forces that frequently determine ecological and evolutionary dynamics and patterns in nature.

Regional neutrality evolves through local adaptive niche evolution.

Biodiversity in natural systems can be maintained either because niche differentiation among competitors facilitates stable coexistence or because equal fitness among neutral species allows for their long-term cooccurrence despite a slow drift toward extinction. Whereas the relative importance of these two ecological mechanisms has been well-studied in the absence of evolution, the role of local adaptive evolution in maintaining biological diversity through these processes is less clear. Here we study the contribution of local adaptive evolution to coexistence in a landscape of interconnected patches subject to disturbance. Under these conditions, early colonists to empty patches may adapt to local conditions sufficiently fast to prevent successful colonization by other preadapted species. Over the long term, the iteration of these local-scale priority effects results in niche convergence of species at the regional scale even though species tend to monopolize local patches. Thus, the dynamics evolve from stable coexistence through niche differentiation to neutral cooccurrence at the landscape level while still maintaining strong local niche segregation. Our results show that neutrality can emerge at the regional scale from local, niche-based adaptive evolution, potentially resolving why ecologists often observe neutral distribution patterns at the landscape level despite strong niche divergence among local communities.

The road to higher permanence and biodiversity in exurban wetlands.

Exurban areas are expanding throughout the world, yet their effects on local biodiversity remain poorly understood. Wetlands, in particular, face ongoing and substantial threats from exurban development. We predicted that exurbanization would reduce the diversity of wetland amphibian and invertebrate communities and that more spatially aggregated residential development would leave more undisturbed natural land, thereby promoting greater local diversity. Using structural equation models, we tested a series of predictions about the direct and indirect pathways by which exurbanization extent, spatial pattern, and wetland characteristics might affect diversity patterns in 38 wetlands recorded during a growing season. We used redundancy, indicator species, and nested community analyses to evaluate how exurbanization affected species composition. In contrast to expectations, we found higher diversity in exurban wetlands. We also found that housing aggregation did not significantly affect diversity. Exurbanization affected biodiversity indirectly by increasing roads and development, which promoted permanent wetlands with less canopy cover and more aquatic vegetation. These pond characteristics supported greater diversity. However, exurbanization was associated with fewer temporary wetlands and fewer of the species that depend on these habitats. Moreover, the best indicator species for an exurban wetland was the ram's head snail, a common disease vector in disturbed ponds. Overall, results suggest that exurbanization is homogenizing wetlands into more permanent water bodies. These more permanent, exurban ponds support higher overall animal diversity, but exclude temporary wetland specialists. Conserving the full assemblage of wetland species in expanding exurban regions throughout the world will require protecting and creating temporary wetlands.