Multivariate phenotypic divergence along an urbanization gradient.

Evidence suggests that natural populations can evolve to better tolerate the novel environmental conditions associated with urban areas. Studies of adaptive divergence in urban areas often examine one or a few traits at a time from populations residing only at the most extreme urban and nonurban habitats. Thus, whether urbanization drives divergence in many traits simultaneously in a manner that varies with the degree of urbanization remains unclear. To address this gap, we generated seed families of white clover (Trifolium repens) collected from 27 populations along an urbanization gradient in Toronto, Canada, grew them in a common garden, and measured 14 phenotypic traits. Families from urban sites had evolved later phenology and germination, larger flowers, thinner stolons, reduced cyanogenesis, greater biomass and greater seed set. Pollinator observations revealed near-complete turnover of pollinator morphological groups along the urbanization gradient, which may explain some of the observed divergences in floral traits and phenology. Our results suggest that adaptation to urban environments involves multiple traits.

Variation in pollinator-mediated plant reproduction across an urbanization gradient.

Urbanization alters the landscape, degrades and fragments habitats, and can have a profound effect on species interactions. Plant-pollinator networks may be particularly sensitive to urbanization, because plants and their insect pollinators have been shown to respond to urbanization both positively and negatively. To better understand the relationship between urbanization, pollinator behavior, and season on pollinator-mediated plant reproduction, we created 30 experimental plant populations along an urbanization gradient in the Greater Toronto Area, Canada. To test how urbanization affects plant reproduction and between-patch pollen dispersal, we created a standard hermaphroditic plant patch at each site, and a male-sterile plant patch at a subset of sites. We measured plant reproduction in the early and late summer in each of 2 years. Plants in urban sites produced significantly fewer flowers than plants in the nonurban sites, whereas seed number per plant either increased or decreased with urbanization, depending on the season. Experimental populations in urban sites also exhibited reduced pollen dispersal between patches. Pollen dispersal between patches was greatest early in the summer and declined with increased impervious surface and proximity to the city. Together, our results are likely caused by variation in environmental conditions and pollinator services across the urban gradient, resulting in pollen limitation and pollen dispersal differences among sites. Our work adds to the small but growing body of literature on urban plant-pollinator interactions and suggests that responses to urbanization are context-dependent.

Gene flow and genetic drift in urban environments.

Evidence is growing that human modification of landscapes has dramatically altered evolutionary processes. In urban population genetic studies, urbanization is typically predicted to act as a barrier that isolates populations of species, leading to increased genetic drift within populations and reduced gene flow between populations. However, urbanization may also facilitate dispersal among populations, leading to higher genetic diversity within, and lower differentiation between, urban populations. We reviewed the literature on nonadaptive urban evolution to evaluate the support for each of these urban fragmentation and facilitation models. In a review of the literature with supporting quantitative analyses of 167 published urban population genetics studies, we found a weak signature of reduced within-population genetic diversity and no evidence of consistently increased between-population genetic differentiation associated with urbanization. In addition, we found that urban landscape features act as barriers or conduits to gene flow, depending on the species and city in question. Thus, we speculate that dispersal ability of species and environmental heterogeneity between cities contributes to the variation exhibited in our results. However, >90% of published studies reviewed here showed an association of urbanization with genetic drift or gene flow, highlighting the strong impact of urbanization on nonadaptive evolution. It is clear that species biology and city heterogeneity obscure patterns of genetic drift and gene flow in a quantitative analysis. Thus, we suggest that future research makes comparisons of multiple cities and nonurban habitats, and takes into consideration species' natural history, environmental variation, spatial modelling and marker selection.

The evolution of city life.

Urbanization represents a dominant and growing form of disturbance to Earth's natural ecosystems, affecting biodiversity and ecosystem services on a global scale. While decades of research have illuminated the effects of urban environmental change on the structure and function of ecological communities in cities, only recently have researchers begun exploring the effects of urbanization on the evolution of urban populations. The 15 articles in this special feature represent the leading edge of urban evolutionary biology and address existing gaps in our knowledge. These gaps include: (i) the absence of theoretical models examining how multiple evolutionary mechanisms interact to affect evolution in urban environments; (ii) a lack of data on how urbanization affects natural selection and local adaptation; (iii) poor understanding of whether urban areas consistently affect non-adaptive and adaptive evolution in similar ways across multiple cities; (iv) insufficient data on the genetic and especially genomic signatures of urban evolutionary change; and (v) limited understanding of the evolutionary processes underlying the origin of new human commensals. Using theory, observations from natural populations, common gardens, genomic data and cutting-edge population genomic and landscape genetic tools, the papers in this special feature address these gaps and highlight the power of urban evolutionary biology as a globally replicated 'experiment' that provides a powerful approach for understanding how human altered environments affect evolution.

Why is gynodioecy a rare but widely distributed sexual system? Lessons from the Lamiaceae.

Gynodioecy, a sexual system where females and hermaphrodites co-occur, is found in << 1% of angiosperm species. To understand why gynodioecy is rare, we need to understand why females are maintained in some lineages, but not in others. We modelled the evolution of gynodioecy in the Lamiaceae, and investigated whether transition rates between gynodioecious and nongynodioecious states varied across the family. We also investigated whether the evolution of gynodioecy was correlated with the evolution of a herbaceous growth form and temperate distribution. Transition rates differed between Lamiaceae subfamilies. In the Nepetoideae, there were many transitions towards gynodioecy (n = 11), but also many reversions to nongynodioecy (n = 29). In addition, a herbaceous growth form, but not a temperate distribution, affected the rate of transitions both towards and away from gynodioecy; transitions towards gynodioecy occurred ˜16 times more frequently and transitions away from gynodioecy occurred ˜11 times more frequently in herbaceous lineages than in woody lineages. Within the Lamiaceae, lineages in which gynodioecy has frequently evolved also have a high rate of reversions to the nongynodioecious state. Consequently, to understand why gynodioecy is rare, we need to understand why sexual systems are more evolutionarily labile in some lineages than in others.

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.

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.

Urbanization alters interactions between Darwin's finches and Tribulus cistoides on the Galápagos Islands.

Emerging evidence suggests that humans shape the ecology and evolution of species interactions. Islands are particularly susceptible to anthropogenic disturbance due to the fragility of their ecosystems; however, we know little about the susceptibility of species interactions to urbanization on islands. To address this gap, we studied how the earliest stages of urban development affect interactions between Darwin's finches and its key food resource, Tribulus cistoides, in three towns on the Galápagos Islands. We measured variation in mericarp predation rates, mericarp morphology, and finch community composition using population surveys, experimental manipulations, and finch observations conducted in habitats within and outside of each town. We found that both seed and mericarp removal rates were higher in towns than natural habitats. We also found that selection on mericarp size and defense differed between habitats in the survey and experimental populations and that towns supported smaller and less diverse finch communities than natural habitats. Together, our results suggest that even moderate levels of urbanization can alter ecological interactions between Darwin's finches and T. cistoides, leading to modified natural selection on T. cistoides populations. Our study demonstrates that trophic interactions on islands may be susceptible to the anthropogenic disturbance associated with urbanization. Despite containing the highest diversity in the world, studies of urbanization are lacking from the tropics. Our study identified signatures of urbanization on species interactions in a tropical island ecosystem and suggests that changes to the ecology of species interactions has the potential to alter evolution in urban environments.

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.

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.

Frequency-dependent fitness in gynodioecious Lobelia siphilitica.

Selection is frequency dependent when an individual's fitness depends on the frequency of its phenotype. Frequency-dependent selection should be common in gynodioecious plants, where individuals are female or hermaphroditic; if the fitness of females is limited by the availability of pollen to fertilize their ovules, then they should have higher fitness when rare than when common. To test whether the fitness of females is frequency dependent, we manipulated the sex ratio in arrays of gynodioecious Lobelia siphilitica. To test whether fitness was frequency dependent because of variation in pollen availability, we compared open-pollinated and supplemental hand-pollinated plants. Open-pollinated females produced more seeds when they were rare than when they were common, as expected if fitness is negatively frequency dependent. However, hand-pollinated females also produced more seeds when they were rare, indicating that variation in pollen availability was not the cause of frequency-dependent fitness. Instead, fitness was frequency dependent because both hand- and open-pollinated females opened more flowers when they were rare than when they were common. This plasticity in the rate of anthesis could cause fitness to be frequency dependent even when reproduction is not pollen limited, and thus expand the conditions under which frequency-dependent selection operates in gynodioecious species.