A roadmap for urban evolutionary ecology

Abstract

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.

Keywords: citizen science; community engagement; eco‐evolutionary feedback; gene flow; landscape genetics; urban evolution; urban socioecology.

Figure 1

Number of publications (1980–2017) that include the terms “urban ecology” or “urban evolution” (no studies could be found before 1995), combined with word clouds of the most popular keywords in abstracts of urban evolutionary ecology studies from 1995 to 2017. The left axis (black) displays the number of urban evolution publications per year and corresponds to the stacked bars. Each bar is broken down into the proportion of studies which attributed the mechanism of evolution to genetic drift (light gray), gene flow (gray), selection (dark gray), and mutation (black). The right axis (dark green) displays the number of urban ecology publications by year and corresponds to the light green shaded portion with dark green dashed line. The solid red horizontal line indicates the maximum number of urban evolution publications per year relative to urban ecology publications. Inset: proportion of species studied that belong to the taxonomic groups shown; data taken from Supporting Information Table S1 of Johnson and Munshi‐South (2017)

Figure 2

Examples of organisms in which urban evolutionary ecology has been studied. (a) Peromyscus leucopus (white‐footed mouse; photo credit: J. Richardson), (b) Linaria vulgaris (yellow toadflax; photograph credit: A. Longley), (c) Crepis sancta (holy hawksbeard; photograph credit: G. Przetak), (d) Anolis cristatellus (crested anole; photograph credit: K. Winchell), (e) Trifolium repens (white clover; photograph credit: J. Santangelo), (f) Temnothorax curvispinosus (acorn ant; photograph credit: L. Nichols), (g) Turdus merula (common blackbird; photograph credit: Wikimedia Commons), and (h) Culex pipens f. molestus (house mosquito; photograph credit: Wikimedia Commons)

Figure 3

Convergent evolution can occur at phenotypic and genetic levels. At the highest level (organism performance), there are few solutions that would result in high fitness, leading to a large amount of parallel adaptation. But there are several different traits that could aid in that performance and even more potential genetic changes that could result in each trait shift. Each of those genetic changes in turn could be affected through multiple different genotypes. At the lowest level (genetic), many different genotypes can produce the same phenotype, decreasing the probability of observing parallelism at this level. For example, at the gene level: Fundulus heteroclitus (mummichog) at polluted sites differed in the same genes (but different haplotypes) related to pollution tolerance (Reid et al., 2016). At the trait level: in Anolis cristatellus (crested anole) and Trifolium repens (white clover), the same trait changes (morphology in anoles, cyanogenesis in T. repens) were observed in multiple urban populations (Thompson et al., 2016; Winchell et al., 2016). At the whole‐organism performance level: Temnothorax curvispinosus (acorn ant) exhibited a similar change in thermal performance in multiple urban populations (Diamond et al., 2018)

Figure 4

Studies in urban evolutionary ecology offer opportunities to engage the public. The level of engagement can range from passive learning (a), to the donation of private lands for experiments (b), to active community participation in data collection (c). The images show three examples of how authors of the present article have included the community in their past research. (a) Passive learning: Gorton used signs with QR codes linking to the project website to educate the public about evolution in urban environments. (b) Use of private land: Rivkin used yard space provided by homeowners in the Greater Toronto Area to conduct “backyard evolution” experiments. (c) Community science: de Keyzer recruited community scientists to collect spatially extensive phenology data across the large urban area of Toronto, Canada