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.

Population expansion, divergence, and persistence in Western Fence Lizards (Sceloporus occidentalis) at the northern extreme of their distributional range.

Population dynamics within species at the edge of their distributional range, including the formation of genetic structure during range expansion, are difficult to study when they have had limited time to evolve. Western Fence Lizards (Sceloporus occidentalis) have a patchy distribution at the northern edge of their range around the Puget Sound, Washington, where they almost exclusively occur on imperiled coastal habitats. The entire region was covered by Pleistocene glaciation as recently as 16,000 years ago, suggesting that populations must have colonized these habitats relatively recently. We tested for population differentiation across this landscape using genome-wide SNPs and morphological data. A time-calibrated species tree supports the hypothesis of a post-glacial establishment and subsequent population expansion into the region. Despite a strong signal for fine-scale population genetic structure across the Puget Sound with as many as 8-10 distinct subpopulations supported by the SNP data, there is minimal evidence for morphological differentiation at this same spatiotemporal scale. Historical demographic analyses suggest that populations expanded and diverged across the region as the Cordilleran Ice Sheet receded. Population isolation, lack of dispersal corridors, and strict habitat requirements are the key drivers of population divergence in this system. These same factors may prove detrimental to the future persistence of populations as they cope with increasing shoreline development associated with urbanization.

The legacy of predator threat shapes prey foraging behaviour.

Predators exert strong selection on prey foraging behaviour such that prey responses may reflect a combination of ancestral effects of predators (genetic and nongenetic transgenerational effects), past individual experience with predators (phenotypic plasticity), and current exposure to predators (behavioural response). However, the importance of these factors in shaping prey foraging behaviour is not well understood. To test the relative effects of ancestry, prior experience, and current exposure, we measured foraging rates and food size preference of different ancestry and exposure groups of Western mosquitofish in the presence and absence of immediate threat from predatory largemouth bass. Our results confirm that mosquitofish had lower foraging rate in the immediate presence of predator threat. Mosquitofish also foraged at a lower rate if they had ancestry with predators, regardless of immediate threat. In contrast, individual prior experience with predators only caused reduced foraging rates in the immediate presence of a predator. This suggests that phenotypic plasticity could carry a lower risk of maladaptive antipredator responses-i.e., reduced food intake-in the complete absence of a predator. Finally, in the presence of a predator, mosquitofish with both ancestry and experience with predators consumed larger, presumably more energetically valuable, food items. Overall, our results show that non-consumptive effects of predators on prey behaviour can persist within and across generations, such that the legacy of past predator exposure-or "the ghost of predation past"-may continue to shape prey behaviour even when predators are no longer around.

Conserving intraspecific variation for nature's contributions to people.

The rapid loss of intraspecific variation is a hidden biodiversity crisis. Intraspecific variation, which includes the genomic and phenotypic diversity found within and among populations, is threatened by local extinctions, abundance declines, and anthropogenic selection. However, biodiversity assessments often fail to highlight this loss of diversity within species. We review the literature on how intraspecific variation supports critical ecological functions and nature's contributions to people (NCP). Results show that the main categories of NCP (material, non-material, and regulating) are supported by intraspecific variation. We highlight new strategies that are needed to further explore these connections and to make explicit the value of intraspecific variation for NCP. These strategies will require collaboration with local and Indigenous groups who possess critical knowledge on the relationships between intraspecific variation and ecosystem function. New genomic methods provide a promising set of tools to uncover hidden variation. Urgent action is needed to document, conserve, and restore the intraspecific variation that supports nature and people. Thus, we propose that the maintenance and restoration of intraspecific variation should be raised to a major global conservation objective.

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.

Adaptive Evolution in Cities: Progress and Misconceptions.

Current narratives suggest that urban adaptation - the adaptive evolution of organisms to cities - is pervasive across taxa and cities. However, in reviewing hundreds of studies, we find only six comprehensive examples of species adaptively evolving to urbanization. We discuss the utility and shortcomings of methods for studying urban adaptation. We then review diverse systems offering preliminary evidence for urban adaptation and outline a research program for advancing its study. Urban environments constitute diverse, interacting selective agents that test the limits of adaptation. Understanding urban adaptation therefore offers unique opportunities for addressing fundamental questions in evolutionary biology and for better conserving biodiversity in cities. However, capitalizing on these opportunities requires appropriate research methods and dissemination of accurate narratives.

The ecological and evolutionary consequences of systemic racism in urban environments.

Urban areas are dynamic ecological systems defined by interdependent biological, physical, and social components. The emergent structure and heterogeneity of urban landscapes drives biotic outcomes in these areas, and such spatial patterns are often attributed to the unequal stratification of wealth and power in human societies. Despite these patterns, few studies have effectively considered structural inequalities as drivers of ecological and evolutionary outcomes and have instead focused on indicator variables such as neighborhood wealth. In this analysis, we explicitly integrate ecology, evolution, and social processes to emphasize the relationships that bind social inequities-specifically racism-and biological change in urbanized landscapes. We draw on existing research to link racist practices, including residential segregation, to the heterogeneous patterns of flora and fauna observed by urban ecologists. In the future, urban ecology and evolution researchers must consider how systems of racial oppression affect the environmental factors that drive biological change in cities. Conceptual integration of the social and ecological sciences has amassed considerable scholarship in urban ecology over the past few decades, providing a solid foundation for incorporating environmental justice scholarship into urban ecological and evolutionary research. Such an undertaking is necessary to deconstruct urbanization's biophysical patterns and processes, inform equitable and anti-racist initiatives promoting justice in urban conservation, and strengthen community resilience to global environmental change.

Climate-driven habitat change causes evolution in Threespine Stickleback.

Climate change can shape evolution directly by altering abiotic conditions or indirectly by modifying habitats, yet few studies have investigated the effects of climate-driven habitat change on contemporary evolution. We resampled populations of Threespine Stickleback (Gasterosteus aculeatus) along a latitudinal gradient in California bar-built estuaries to examine their evolution in response to changing climate and habitat. We took advantage of the strong association between stickleback lateral plate phenotypes and Ectodysplasin A (Eda) genotypes to infer changes in allele frequencies over time. Our results show that over time the frequency of low-plated alleles has generally increased and heterozygosity has decreased. Latitudinal patterns in stickleback plate phenotypes suggest that evolution at Eda is a response to climate-driven habitat transformation rather than a direct consequence of climate. As climate change has reduced precipitation and increased temperature and drought, bar-built estuaries have transitioned from lotic (flowing-water) to lentic (still-water) habitats, where the low-plated allele is favoured. The low-plated allele has achieved fixation at the driest, hottest southernmost sites, a trend that is progressing northward with climate change. Climate-driven habitat change is therefore causing a reduction in genetic variation that may hinder future adaptation for populations facing multiple threats.

The ecological importance of intraspecific variation.

Human activity is causing wild populations to experience rapid trait change and local extirpation. The resulting effects on intraspecific variation could have substantial consequences for ecological processes and ecosystem services. Although researchers have long acknowledged that variation among species influences the surrounding environment, only recently has evidence accumulated for the ecological importance of variation within species. We conducted a meta-analysis comparing the ecological effects of variation within a species (intraspecific effects) with the effects of replacement or removal of that species (species effects). We evaluated direct and indirect ecological responses, including changes in abundance (or biomass), rates of ecological processes and changes in community composition. Our results show that intraspecific effects are often comparable to, and sometimes stronger than, species effects. Species effects tend to be larger for direct ecological responses (for example, through consumption), whereas intraspecific effects and species effects tend to be similar for indirect responses (for example, through trophic cascades). Intraspecific effects are especially strong when indirect interactions alter community composition. Our results summarize data from the first generation of studies examining the relative ecological effects of intraspecific variation. Our conclusions can help inform the design of future experiments and the formulation of strategies to quantify and conserve biodiversity.

Ecological and evolutionary effects of stickleback on community structure.

Species' ecology and evolution can have strong effects on communities. Both may change concurrently when species colonize a new ecosystem. We know little, however, about the combined effects of ecological and evolutionary change on community structure. We simultaneously examined the effects of top-predator ecology and evolution on freshwater community parameters using recently evolved generalist and specialist ecotypes of three-spine stickleback (Gasterosteus aculeatus). We used a mesocosm experiment to directly examine the effects of ecological (fish presence and density) and evolutionary (phenotypic diversity and specialization) factors on community structure at lower trophic levels. We evaluated zooplankton biomass and composition, periphyton and phytoplankton chlorophyll-a concentration, and net primary production among treatments containing different densities and diversities of stickleback. Our results showed that both ecological and evolutionary differences in the top-predator affect different aspects of community structure and composition. Community structure, specifically the abundance of organisms at each trophic level, was affected by stickleback presence and density, whereas composition of zooplankton was influenced by stickleback diversity and specialization. Primary productivity, in terms of chlorophyll-a concentration and net primary production was affected by ecological but not evolutionary factors. Our results stress the importance of concurrently evaluating both changes in density and phenotypic diversity on the structure and composition of communities.

Goldilocks Meets Santa Rosalia: An Ephemeral Speciation Model Explains Patterns of Diversification Across Time Scales.

Understanding the rate at which new species form is a key question in studying the evolution of life on earth. Here we review our current understanding of speciation rates, focusing on studies based on the fossil record, phylogenies, and mathematical models. We find that speciation rates estimated from these different studies can be dramatically different: some studies find that new species form quickly and often, while others find that new species form much less frequently. We suggest that instead of being contradictory, differences in speciation rates across different scales can be reconciled by a common model. Under the "ephemeral speciation model", speciation is very common and very rapid but the new species produced almost never persist. Evolutionary studies should therefore focus on not only the formation but also the persistence of new species.

Evolutionary diversification in stickleback affects ecosystem functioning.

Explaining the ecological causes of evolutionary diversification is a major focus of biology, but surprisingly little has been said about the effects of evolutionary diversification on ecosystems. The number of species in an ecosystem and their traits are key predictors of many ecosystem-level processes, such as rates of productivity, biomass sequestration and decomposition. Here we demonstrate short-term ecosystem-level effects of adaptive radiation in the threespine stickleback (Gasterosteus aculeatus) over the past 10,000 years. These fish have undergone recent parallel diversification in several lakes in coastal British Columbia, resulting in the formation of two specialized species (benthic and limnetic) from a generalist ancestor. Using a mesocosm experiment, we demonstrate that this diversification has strong effects on ecosystems, affecting prey community structure, total primary production, and the nature of dissolved organic materials that regulate the spectral properties of light transmission in the system. However, these ecosystem effects do not simply increase in their relative strength with increasing specialization and species richness; instead, they reflect the complex and indirect consequences of ecosystem engineering by sticklebacks. It is well known that ecological factors influence adaptive radiation. We demonstrate that adaptive radiation, even over short timescales, can have profound effects on ecosystems.