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

Abstract 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.

the context of biological studies and give a brief history of research on urban evolutionary biology. We then provide an overview of current themes within urban evolution in light of the research presented in this issue. We end with a look to emerging themes and challenges for future research.

| What is urbanization?
For the purpose of this special issue, we operationally define urban areas as dense human populations, typified by cities and the infrastructure associated with these areas (e.g., buildings, roads, and landscape changes). Beyond this simple definition, the process of urban development (i.e., urbanization) is inherently multidimensional and, in some respects, difficult to define. Yet, there are changes to the natural environment that researchers generally agree characterize urban ecosystems. Urban environments tend to have increased impervious surfaces, higher human population density, elevated temperatures (i.e., the urban heat island effect), higher pollution levels, and highly fragmented habitats. These dramatic changes to the natural landscape present novel challenges for organisms.
Consequently, urbanization can affect eco-evolutionary dynamics, including adaptive and nonadaptive evolution of urban populations, as well as feedbacks onto ecosystems.
Urbanization is not a uniform process, and urban areas (hereafter called "cities" for simplicity) can vary substantially from one another.
The following are a few examples of the local characteristics that vary within and between cities: the age of a city, the extent and pattern of development, policies on urban planning, control of urban wildlife, regional societal practices, and historical and contemporary socioeconomic patterns (including structural racism). This topic has received substantial attention recently, and we recommend Szulkin et al., 2020 (chapter 2), Schell, Dyson, et al. (2020), and the UN's 2018 report on global urbanization for more in-depth discussion of how to define and measure urbanization. The specific aspects of urban environmental change that are most relevant to the evolution of a particular species are likely to vary and should be chosen carefully to reflect the specific characteristics of a city and biology of a focal organism, as is reflected by the diverse metrics used to characterize urban environments in this special issue (Figure 1).

| Urban evolution: current state of knowledge
The nascent field of urban evolutionary biology has in recent years provided myriad examples of evolutionary changes associated with urbanization in a wide variety of taxa and at all levels of biological hierarchy (i.e., functional, phenotypic, regulatory, genomic). The exponential growth of this field has yielded important insights into fundamental ecological and evolutionary questions Santangelo et al., 2018;Szulkin et al., 2020). As empirical examples of evolutionary change have accumulated, so too have the retrospective syntheses, providing important perspectives on key themes and future directions for the field.
Additionally, these syntheses indicate that when evaluating adaptive and nonadaptive evolution, heterogeneity across the landscape and other landscape features are important factors to consider (Lambert & Donihue, 2020;Miles et al., 2019;Rivkin et al., 2019;Schell, 2018; F I G U R E 1 Researchers use a wide variety of metrics to describe urban habitats, and different metrics are appropriate for different species and to address different questions. The 12 empirical papers in this special issue used the following metrics to describe urbanization and to analyze phenotypic and genotypic variation: land cover and use, impervious surface cover (ISA) and roads, temperature, human population density, built-up land cover, and proximity to the city center or within metropolitan boundaries (gray boxes indicate the metric(s) used in each study)   Schmidt et al., 2020;Szulkin et al., 2020). While each of these reviews, syntheses, and even special issues repeatedly highlight these common themes, there is not yet consensus of how urbanization is shaping evolution. Indeed, the field of urban evolutionary biology is still in its infancy, with the majority of the empirical research and theoretical research published in the last 10 years .
Due to the rapid growth of urban evolutionary biology, there are many questions that have yet to be addressed. The most pertinent of these outstanding questions ask: Are the evolutionary responses to urbanization predictable? Specifically, what is the prevalence of convergence at the genetic and phenotypic level across urban environments and among different species? If we are able to identify the drivers of evolution and predict responses to urbanization, then perhaps we will be better able to apply this information to conservation, land-use management (Alberti, 2015;Johnson & Munshi-South, 2017;Lambert & Donihue, 2020;Rivkin et al., 2019), and the intersection of human socioeconomic variables (e.g., systemic racism, poverty, health) and ecology and evolutionary change (Schell, Dyson, et al., 2020). This special issue, "Evolution in Urban Environments," takes a step in this direction by addressing these questions.

| THE S PECIAL ISSUE
The state of knowledge in the burgeoning field of urban evolutionary ecology is rapidly changing. Retrospective and prospective review papers provide valuable and continuing feedback to shape the field, but it is the results from empirical research conducted on urbandwelling organisms that are critical to answer questions, address gaps, and push the field in new directions. With this special issue, our goal is to synthesize the current state of the field, address existing gaps in knowledge, and inspire new directions of research and application.
The special issue comprises 16 papers, including 12 empirical contributions, three reviews, and one capstone perspective. The empirical studies represent diverse taxonomic groups from urbanized habitats primarily in North America and Europe, with an additional study in China. These papers represent four major themes: (a) adaptive evolution via physiological responses to urban climate, (b) adaptive evolution via phenotype-environment relationships in urban habitats, (c) population connectivity and genetic drift, and (d) human-wildlife interactions ( Figure 2). In addition, the reviews and capstone paper introduce emerging themes to help guide future research on topics as diverse as marine environments, use of natural history museum specimens, and the integration of socioeconomic processes into eco-evolutionary dynamics ( Figure 2). We provide a brief summary of these contributions in the sections below and conclude with an assessment of the progress the papers in this special issue make in addressing questions and gaps previously identi- . We conclude with a forward-looking assessment that identifies the directions the field is heading to address remaining gaps in knowledge. Previous studies have established that urban organisms are able to tolerate elevated temperatures typical of urban environments and have found both phenotypically plastic and genetic underpinnings for this variation Campbell-Staton et al., 2020;Diamond et al., 2018). Yilmaz et al. (2020) add to this growing body of evidence for thermal adaptation by exploring phenotypic plasticity and adaptive evolution of both heat and cold tolerance, as well as

F I G U R E 2
We identified four focal topics from the empirical contributions (population genetics-yellow, trait-environment relationships-pink, human-wildlife interactions-purple, physiology-blue) as well as emerging themes from the reviews and capstone paper (green). These five themes are presented here with the top 19 words from the abstracts, with word size relative to the prevalence across the abstracts in each group rgi g Th Emerging Themes

T r a i t t v v v i r o t t R a t t i o h i p T r a i t -E n v i r o n m e n t R e l a t i o n s h i p s
desiccation tolerance, in the terrestrial isopod Oniscus asellus. Urban isopods exhibited evolved differences in increased heat tolerance compared to their rural counterparts, but not in cold or desiccation tolerance. Unlike many urban organisms, urban isopods exhibited no phenotypic plasticity in heat tolerance, but did exhibit a phenotypically plastic response of diminished cold tolerance. Although no directional shifts in body size or desiccation tolerance were observed between urban and rural populations in either "cool" or "hot" rearing conditions, larger individuals exhibited improved desiccation tolerance.
Little is known about consequences of elevated urban temperatures beyond thermal tolerance. Tüzün and Stoks (2020)  maladaptive physiological responses to urbanization may arise in response to the urban heat island effect, perhaps if selection is acting on correlated traits (e.g., heat tolerance). Alternatively, elevated metabolic rates may confer adaptive benefits in unanticipated ways.

| Phenotype-environment relationships
Environmental change associated with urbanization can be a potent driver of natural selection and the evolution of urban-adapted phenotypes. Studying the associations between landscape features (e.g., impervious surface, fragmentation, urban versus rural habitats) and genomic variation, phenotypes and/or fitness of organisms, can provide insight into the evolutionary processes (e.g., natural selection) and responses (e.g., adaptive evolution) caused by urban environmental change (Santangelo et al., 2020). This special feature  (2020) identified putatively adaptive epigenetic markers in blood and liver tissue of fledgling great tits. DNA methylation sites in the liver were enriched within regulatory regions, suggesting that there is gene expression variation in metabolic processes between urban and forest birds that may increase fitness.

| Population genetic patterns associated with urbanization
Gene flow and genetic drift may be influenced by urbanization either through "urban fragmentation" or "urban facilitation," which encap- Whereas amphibians are highly susceptible to habitat fragmentation, flying animals may be able to avoid many of the barriers that terrestrial animals face. Three studies in this special issue address the issue of the relationship between dispersal ability and gene flow. Ballare and Jha (2020) found that urban and agricultural areas do not restrict gene flow in carpenter bees at a regional scale. However, there is evidence of fine-scale population structure as individuals in close proximity are more related to one another than by chance alone, an effect that is likely a consequence of high philopatry.

| Human-wildlife interactions
Human-wildlife interactions are an inherent part of urban areas, and these interactions have the potential to shape the evolutionary trajectories of urban wildlife. As humans concentrate in urban environments, some wildlife becomes locally extinct, whereas others find refuge in urban parks, backyards, and other green spaces.
Additionally, some organisms known as human commensals (e.g., brown rats, house mice, cockroaches) accompany humans as they move around the globe (Bonhomme & Searle, 2012;Puckett et al., 2016;Vargo et al., 2014), not only surviving but dependent on human-dominated landscapes. Together, these processes lead to a distinct mix of native and non-native organisms in every urban environment.
Socio-political policies and traditions also contribute to the extent of urban-wildlife interactions and its evolutionary impacts. Although rats are continuously distributed across the urban environment, rat family groups cluster within city blocks. However, this spatial distribution of rats in the urban environment does not correlate with patterns of pathogen prevalence, indicating that a specific rat genotype does not confer protection against pathogen infection.

| Emerging themes
The majority of urban evolutionary research to date has focused on terrestrial ecosystems. Yet, our waterways are impacted directly and indirectly by anthropogenic activity and urbanization. Highlighting this emerging and understudied area of urban evolutionary study, Another underutilized and rich resource for urban evolutionary research can be found in natural history collections. Shultz et al. (2020) propose that natural history collections are critical for contemporary and future urban evolution studies. These collections allow researchers to directly compare organisms over time to understand phenotypic and genotypic consequences of urbanization.
In their review, Shultz et al. (2020) discuss how museum collections can be leveraged and how they have been used to study urban evolution to date. The authors conclude that museum collections are infrequently used despite the great potential for the study of museum specimens to drive the urban evolution field in new and exciting directions. Nevertheless, the use of museum specimens in urban evolutionary research is hindered by deposition and archiving patterns, leading the authors to make recommendations for best practices moving forward so that future researchers can best use this important window into the past. in urban environments, and proposes a "socio-eco-evolutionary" framework for studying urban ecosystems.  Shultz et al. (2020) and demonstrates the need for museum collections across all six human-inhabited continents to actively collect specimens from urban and nonurban areas to document current organisms and provide a wealth of samples for future scientists to ask questions about. Addressing these gaps will greatly advance our understanding of urban evolutionary biology.

| CON CLUS ION
The research presented here also emphasizes four emerging In addition, we would specifically like to highlight human-wildlife interactions, because ultimately, cities are designed for human needs but are inherently interconnected to local wildlife. Building on these themes will help advance our understanding of the multifarious socio-eco-evolutionary processes that drive human-wildlife interactions to better serve both humans and urban organisms.

ACK N OWLED G EM ENTS
We would like to thank all of the authors that contributed to this special issue.

DATA AVA I L A B I L I T Y S TAT E M E N T
This manuscript does not have associated data.