Effects of urban-induced mutations on ecology, evolution and health.

Increasing evidence suggests that urbanization is associated with higher mutation rates, which can affect the health and evolution of organisms that inhabit cities. Elevated pollution levels in urban areas can induce DNA damage, leading to de novo mutations. Studies on mutations induced by urban pollution are most prevalent in humans and microorganisms, whereas studies of non-human eukaryotes are rare, even though increased mutation rates have the potential to affect organisms and their populations in contemporary time. Our Perspective explores how higher mutation rates in urban environments could impact the fitness, ecology and evolution of populations. Most mutations will be neutral or deleterious, and higher mutation rates associated with elevated pollution in urban populations can increase the risk of cancer in humans and potentially other species. We highlight the potential for urban-driven increased deleterious mutational loads in some organisms, which could lead to a decline in population growth of a wide diversity of organisms. Although beneficial mutations are expected to be rare, we argue that higher mutation rates in urban areas could influence adaptive evolution, especially in organisms with short generation times. Finally, we explore avenues for future research to better understand the effects of urban-induced mutations on the fitness, ecology and evolution of city-dwelling organisms.

Urban evolutionary ecology brings exaptation back into focus.

The contribution of pre-existing phenotypic variation to evolution in novel environments has long been appreciated. Nevertheless, evolutionary ecologists have struggled with communicating these aspects of the adaptive process. In 1982, Gould and Vrba proposed terminology to distinguish character states shaped via natural selection for the roles they currently serve ('adaptations') from those shaped under preceding selective regimes ('exaptations'), with the intention of replacing the inaccurate 'preadaptation'. Forty years later, we revisit Gould and Vrba's ideas which, while often controversial, continue to be widely debated and highly cited. We use the recent emergence of urban evolutionary ecology as a timely opportunity to reintroduce the ideas of Gould and Vrba as an integrated framework to understand contemporary evolution in novel environments.

Genome-wide parallelism underlies contemporary adaptation in urban lizards.

Urbanization drastically transforms landscapes, resulting in fragmentation, degradation, and the loss of local biodiversity. Yet, urban environments also offer opportunities to observe rapid evolutionary change in wild populations that survive and even thrive in these novel habitats. In many ways, cities represent replicated "natural experiments" in which geographically separated populations adaptively respond to similar selection pressures over rapid evolutionary timescales. Little is known, however, about the genetic basis of adaptive phenotypic differentiation in urban populations nor the extent to which phenotypic parallelism is reflected at the genomic level with signatures of parallel selection. Here, we analyzed the genomic underpinnings of parallel urban-associated phenotypic change in Anolis cristatellus, a small-bodied neotropical lizard found abundantly in both urbanized and forested environments. We show that phenotypic parallelism in response to parallel urban environmental change is underlain by genomic parallelism and identify candidate loci across the Anolis genome associated with this adaptive morphological divergence. Our findings point to polygenic selection on standing genetic variation as a key process to effectuate rapid morphological adaptation. Identified candidate loci represent several functions associated with skeletomuscular development, morphology, and human disease. Taken together, these results shed light on the genomic basis of complex morphological adaptations, provide insight into the role of contingency and determinism in adaptation to novel environments, and underscore the value of urban environments to address fundamental evolutionary questions.

Moving past the challenges and misconceptions in urban adaptation research.

Although the field of urban evolutionary ecology has recently expanded, much progress has been made in identifying adaptations that arise as a result of selective pressures within these unique environments. However, as studies within urban environments have rapidly increased, researchers have recognized that there are challenges and opportunities in characterizing urban adaptation. Some of these challenges are a consequence of increased direct and indirect human influence, which compounds long-recognized issues with research on adaptive evolution more generally. In this perspective, we discuss several common research challenges to urban adaptation related to (1) methodological approaches, (2) trait-environment relationships and the natural history of organisms, (3) agents and targets of selection, and (4) habitat heterogeneity. Ignoring these challenges may lead to misconceptions and further impede our ability to draw conclusions regarding evolutionary and ecological processes in urban environments. Our goal is to first shed light on the conceptual challenges of conducting urban adaptation research to help avoid the propagation of these misconceptions. We further summarize potential strategies to move forward productively to construct a more comprehensive picture of urban adaptation, and discuss how urban environments also offer unique opportunities and applications for adaptation research.

Geometric Morphometrics Reveal Shape Differences in the Toes of Urban Lizards.

Urbanization, despite its destructive effects on natural habitats, offers species an opportunity to colonize novel niches. Previous research found that urban Anolis lizards in Puerto Rico had increased adhesive toepad area and more ventral toepad scales, traits that are likely adaptive and genetically based. We further investigated these phenotypic changes using geometric morphometrics to measure differences in toe shape, toepad shape, and lamellar morphology. Our results indicate that the increased toepad area of urban Anolis cristatellus lizards in Puerto Rico is not simply an isometric increase in toe size. Toes of urban populations exhibit multiple disproportional changes compared to forest lizards, with a larger proportion of the toe length covered in adhesive toepad. In addition, the toepads of urban lizards increase more in length than width. Lastly, lizards in urban populations exhibit both increased number of lamellae as well as increased spacing between individual lamellae. We also observed regional variation, with urban specimens having significantly more disparity, suggesting similar processes of urban adaptation are likely happening in parallel across the island, yet with region-specific idiosyncrasies, possibly generating more variation in toepad morphology across urban specimens as compared to forest specimens. Considering the use of geometric morphometrics, we found that specimen preparation, specifically how flat and straight toes are during imaging, to be an important factor affecting our data, more so than specimen size or any other meaningful morphological variation. In addition, we found that landmark and semilandmark data can be used to directly estimate toepad area, offering the opportunity to streamline future studies. In conclusion, our results highlight the value of considering toepad morphology in more detail beyond adhesive pad area or number of lamellae. Geometric morphometrics tools may be employed to elucidate subtle differences in shape to better allow researchers to connect changes in morphology to ecology and adhesive performance.

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.

Selection on adaptive and maladaptive gene expression plasticity during thermal adaptation to urban heat islands.

Phenotypic plasticity enables a single genotype to produce multiple phenotypes in response to environmental variation. Plasticity may play a critical role in the colonization of novel environments, but its role in adaptive evolution is controversial. Here we suggest that rapid parallel regulatory adaptation of Anolis lizards to urban heat islands is due primarily to selection for reduced and/or reversed heat-induced plasticity that is maladaptive in urban thermal conditions. We identify evidence for polygenic selection across genes of the skeletal muscle transcriptome associated with heat tolerance. Forest lizards raised in common garden conditions exhibit heat-induced changes in expression of these genes that largely correlate with decreased heat tolerance, consistent with maladaptive regulatory response to high-temperature environments. In contrast, urban lizards display reduced gene expression plasticity after heat challenge in common garden and a significant increase in gene expression change that is congruent with greater heat tolerance, a putatively adaptive state in warmer urban environments. Genes displaying maladaptive heat-induced plasticity repeatedly show greater genetic divergence between urban and forest habitats than those displaying adaptive plasticity. These results highlight the role of selection against maladaptive regulatory plasticity during rapid adaptive modification of complex systems in the wild.

Urban evolution comes into its own: Emerging themes and future directions of a burgeoning field.

Urbanization has recently emerged as an exciting new direction for evolutionary research founded on our growing understanding of rapid evolution paired with the expansion of novel urban habitats. Urbanization can influence adaptive and nonadaptive evolution in urban-dwelling species, but generalized patterns and the predictability of urban evolutionary responses within populations remain unclear. This editorial introduces the special feature "Evolution in Urban Environments" and addresses four major emerging themes, which include: (a) adaptive evolution and phenotypic plasticity via physiological responses to urban climate, (b) adaptive evolution via phenotype-environment relationships in urban habitats, (c) population connectivity and genetic drift in urban landscapes, and (d) human-wildlife interactions in urban spaces. Here, we present the 16 articles (12 empirical, 3 review, 1 capstone) within this issue and how they represent each of these four emerging themes in urban evolutionary biology. Finally, we discuss how these articles address previous questions and have now raised new ones, highlighting important new directions for the field.

Parallel selection on thermal physiology facilitates repeated adaptation of city lizards to urban heat islands.

Only recently have we begun to understand the ecological and evolutionary effects of urbanization on species, with studies revealing drastic impacts on community composition, gene flow, behaviour, morphology and physiology. However, our understanding of how adaptive evolution allows species to persist, and even thrive, in urban landscapes is still nascent. Here, we examine phenotypic, genomic and regulatory impacts of urbanization on a widespread lizard, the Puerto Rican crested anole (Anolis cristatellus). We find that urban lizards endure higher environmental temperatures and display greater heat tolerance than their forest counterparts. A single non-synonymous polymorphism within a protein synthesis gene (RARS) is associated with heat tolerance plasticity within urban heat islands and displays parallel signatures of selection in cities. Additionally, we identify groups of differentially expressed genes between habitats showing elevated genetic divergence in multiple urban-forest comparisons. These genes display evidence of adaptive regulatory evolution within cities and disproportionately cluster within regulatory modules associated with heat tolerance. This study provides evidence of temperature-mediated selection in urban heat islands with repeatable impacts on physiological evolution at multiple levels of biological hierarchy.

Phylogenetic signal and evolutionary correlates of urban tolerance in a widespread neotropical lizard clade.

Urbanization is intensifying worldwide, and while some species tolerate and even exploit urban environments, many others are excluded entirely from this new habitat. Understanding the factors that underlie tolerance of urbanization is thus of rapidly growing importance. Here, we examine urban tolerance across a diverse group of lizards: Caribbean members of the neotropical genus Anolis. Our analyses reveal that urban tolerance has strong phylogenetic signal, suggesting that closely related species tend to respond similarly to urban environments. We propose that this characteristic of urban tolerance in anoles may be used to forecast the possible responses of species to increasing urbanization. In addition, we identified several key ecological and morphological traits that tend to be associated with tolerance in Anolis. Specifically, species experiencing hot and dry conditions in their natural environment and those that maintain higher body temperatures tend to have greater tolerance of urban habitats. We also found that tolerance of urbanization is positively associated with toepad lamella number and negatively associated with ventral scale density and relative hindlimb length. The identification of factors that predispose a species to be more or less urban tolerant can provide a starting point for conservation and sustainable development in our increasingly urbanized world.

A roadmap for urban evolutionary ecology.

Urban ecosystems are rapidly expanding throughout the world, but how urban growth affects the evolutionary ecology of species living in urban areas remains largely unknown. Urban ecology has advanced our understanding of how the development of cities and towns change environmental conditions and alter ecological processes and patterns. However, despite decades of research in urban ecology, the extent to which urbanization influences evolutionary and eco-evolutionary change has received little attention. The nascent field of urban evolutionary ecology seeks to understand how urbanization affects the evolution of populations, and how those evolutionary changes in turn influence the ecological dynamics of populations, communities, and ecosystems. Following a brief history of this emerging field, this Perspective article provides a research agenda and roadmap for future research aimed at advancing our understanding of the interplay between ecology and evolution of urban-dwelling organisms. We identify six key questions that, if addressed, would significantly increase our understanding of how urbanization influences evolutionary processes. These questions consider how urbanization affects nonadaptive evolution, natural selection, and convergent evolution, in addition to the role of urban environmental heterogeneity on species evolution, and the roles of phenotypic plasticity versus adaptation on species' abundance in cities. Our final question examines the impact of urbanization on evolutionary diversification. For each of these six questions, we suggest avenues for future research that will help advance the field of urban evolutionary ecology. Lastly, we highlight the importance of integrating urban evolutionary ecology into urban planning, conservation practice, pest management, and public engagement.

Linking locomotor performance to morphological shifts in urban lizards.

Urban habitats are drastically modified from their natural state, creating unique challenges and selection pressures for organisms that reside in them. We compared locomotor performance of Anolis lizards from urban and forest habitats on tracks differing in angle and substrate, and found that using artificial substrates came at a cost: lizards ran substantially slower and frequently lost traction on man-made surfaces compared to bark. We found that various morphological traits were positively correlated with sprint speed and that these same traits were significantly larger in urban compared to forest lizards. We found that urban lizards ran faster on both man-made and natural surfaces, suggesting similar mechanisms improve locomotor performance on both classes of substrate. Thus, lizards in urban areas may be under selection to run faster on all flat surfaces, while forest lizards face competing demands of running, jumping and clinging to narrow perches. Novel locomotor challenges posed by urban habitats likely have fitness consequences for lizards that cannot effectively use man-made surfaces, providing a mechanistic basis for observed phenotypic shifts in urban populations of this species.

Divergent habitat use of two urban lizard species.

Faunal responses to anthropogenic habitat modification represent an important aspect of global change. In Puerto Rico, two species of arboreal lizard, Anolis cristatellus and A. stratulus, are commonly encountered in urban areas, yet seem to use the urban habitat in different ways. In this study, we quantified differences in habitat use between these two species in an urban setting. For each species, we measured habitat use and preference, and the niche space of each taxon, with respect to manmade features of the urban environment. To measure niche space of these species in an urban environment, we collected data from a total of six urban sites across four different municipalities on the island of Puerto Rico. We quantified relative abundance of both species, their habitat use, and the available habitat in the environment to measure both microhabitat preference in an urban setting, as well as niche partitioning between the two different lizards. Overall, we found that the two species utilize different portions of the urban habitat. Anolis stratulus tends to use more "natural" portions of the urban environment (i.e., trees and other cultivated vegetation), whereas A. cristatellus more frequently uses anthropogenic structures. We also found that aspects of habitat discrimination in urban areas mirror a pattern measured in prior studies for forested sites in which A. stratulus was found to perch higher than A. cristatellus and preferred lower temperatures and greater canopy cover. In our study, we found that the multivariate niche space occupied by A. stratulus did not differ from the available niche space in natural portions of the urban environment and in turn represented a subset of the niche space occupied by A. cristatellus. The unique niche space occupied by A. cristatellus corresponds to manmade aspects of the urban environment generally not utilized by A. stratulus. Our results demonstrate that some species are merely tolerant of urbanization while others utilize urban habitats in novel ways. This finding has implications for long-term persistence in urban habitats and suggests that loss of natural habitat elements may lead to nonrandom species extirpations as urbanization intensifies.

Phenotypic shifts in urban areas in the tropical lizard Anolis cristatellus.

Urbanization is an increasingly important dimension of global change, and urban areas likely impose significant natural selection on the species that reside within them. Although many species of plants and animals can survive in urban areas, so far relatively little research has investigated whether such populations have adapted (in an evolutionary sense) to their newfound milieu. Even less of this work has taken place in tropical regions, many of which have experienced dramatic growth and intensification of urbanization in recent decades. In the present study, we focus on the neotropical lizard, Anolis cristatellus. We tested whether lizard ecology and morphology differ between urban and natural areas in three of the most populous municipalities on the island of Puerto Rico. We found that environmental conditions including temperature, humidity, and substrate availability differ dramatically between neighboring urban and natural areas. We also found that lizards in urban areas use artificial substrates a large proportion of the time, and that these substrates tend to be broader than substrates in natural forest. Finally, our morphological data showed that lizards in urban areas have longer limbs relative to their body size, as well as more subdigital scales called lamellae, when compared to lizards from nearby forested habitats. This shift in phenotype is exactly in the direction predicted based on habitat differences between our urban and natural study sites, combined with our results on how substrates are being used by lizards in these areas. Findings from a common-garden rearing experiment using individuals from one of our three pairs of populations provide evidence that trait differences between urban and natural sites may be genetically based. Taken together, our data suggest that anoles in urban areas are under significant differential natural selection and may be evolutionarily adapting to their human-modified environments.