Gene flow and genetic drift in urban environments Miles, Lindsay S.; Rivkin, L. Ruth; Johnson, Marc T. J. ...
Molecular ecology,
September 2019, 2019-09-00, 20190901, Volume:
28, Issue:
18
Journal Article
Peer reviewed
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.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
As urbanization drastically alters the natural landscape and generates novel habitats within cities, the potential for changes to gene flow for urban-dwelling species increases. The western black ...widow spider (
) is a medically relevant urban adapter pest species, for which we have previously identified population genetic signatures consistent with urbanization facilitating gene flow, likely due to human-mediated transport. Here, in an analysis of 1.9 million genome-wide SNPs, we contrast broad-scale geographical analyses of 10 urban and 11 non-urban locales with fine-scale within-city analyses including 30 urban locales across the western USA. These hierarchical datasets enable us to test hypotheses of how urbanization impacts multiple urban cities and their genetic connectivity at different spatial scales. Coupled fine-scale and broad-scale analyses reveal contrasting patterns of high and low genetic differentiation among locales within cities as a result of low and high genetic connectivity, respectively, of these cities to the overall population network. We discuss these results as they challenge the use of cities as replicates of urban eco-evolution, and have implications for conservation and human health in a rapidly growing urban habitat.
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BFBNIB, NMLJ, NUK, PNG, SAZU, UL, UM, UPUK
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.
The impact of urbanization on biodiversity has been well documented, yet research into the complex dynamics of ecological and evolutionary processes in urban areas is still in its infancy.When novel research challenges emerge, a horizon scan exercise is an integrated approach that brings together global interdisciplinary-minded individuals to identify future research questions that can influence new collaborations and funding agenda.Our horizon scan identified 30 questions for future research in urban evolutionary ecology covering themes in fundamental ecological and evolutionary processes, temporal and spatial scales, sustainability, climate change, sociopolitical and ethical considerations, and innovation in technology.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Urban fragmentation can reduce gene flow that isolates populations, reduces genetic diversity and increases population differentiation, all of which have negative conservation implications. ...Alternatively, gene flow may actually be increased among urban areas consistent with an urban facilitation model. In fact, urban adapter pests are able to thrive in the urban environment and may be experiencing human‐mediated transport. Here, we used social network theory with a population genetic approach to investigate the impact of urbanization on genetic connectivity in the Western black widow spider, as an urban pest model of human health concern. We collected genomewide single nucleotide polymorphism variation from mitochondrial and nuclear double‐digest RAD (ddRAD) sequence data sets from 210 individuals sampled from 11 urban and 10 nonurban locales across its distribution of the Western United States. From urban and nonurban contrasts of population, phylogenetic, and network analyses, urban locales have higher within‐population genetic diversity, lower between‐population genetic differentiation and higher estimates of genetic connectivity. Social network analyses show that urban locales not only have more connections, but can act as hubs that drive connectivity among nonurban locales, which show signatures of historical isolation. These results are consistent with an urban facilitation model of gene flow and demonstrate the importance of sampling multiple cities and markers to identify the role that urbanization has had on larger spatial scales. As the urban landscape continues to grow, this approach will help determine what factors influence the spread and adaptation of pests, like the venomous black widow spider, in building policies for human and biodiversity health.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
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.
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FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
A roadmap for urban evolutionary ecology Rivkin, L. Ruth; Santangelo, James S.; Alberti, Marina ...
Evolutionary Applications,
March 2019, Volume:
12, Issue:
3
Journal Article
Peer reviewed
Open access
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.
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FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
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.
In this perspective, we highlight four key challenges to conducting research on adaptive evolution in urban environments. Although these challenges are not unique to urban environments, the increased human dimension can exacerbate these challenges or introduce new applications to adaptation research. Failure to appreciate these challenges can introduce biases and misconceptions, constraining the potential of urban adaptation research to shed light on evolutionary processes generally.
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FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Urbanization drastically alters landscapes in ways that can threaten local biodiversity. Although species loss has been well documented in urban habitats, why some species persist and not others, and ...how species interactions change remain poorly understood, especially for species with specialized niche requirements. Here, we test the hypothesis that urbanization disrupts specialized plant–herbivore interactions, and these effects vary according to the characteristics of both cities and the features of the organisms themselves. To test this hypothesis, we surveyed milkweed specialist herbivore communities in the early and late growing season of the common milkweed (Asclepias syriaca) across six cities that varied in size by two orders of magnitude. Four results are most important to answering our research questions: (1) the abundance of herbivore species was higher in urban than in rural habitats, whereas leaf herbivory was higher in rural than in urban habitats, and these effects varied between seasons and among cities; (2) the higher species diversity and abundance are likely due to a few species being more associated with rural habitats and other species more common in urban habitats, and thus, urbanization alters insect community composition; (3) the species with the lowest dispersal abilities, Rhyssomatus lineaticollis and Liriomyza asclepiadis, were those that were most strongly affected by urbanization, with R. lineaticollis less abundant and L. asclepiadis more abundant in urban areas; and (4) urbanization influenced plant–herbivore interactions by reducing herbivory, but it did not alter species interactions among herbivorous insects. Biodiversity loss, particularly declines of habitat and host specialists, in urban areas remains a critical concern for conservation. Our results indicate that at least some specialist herbivores are more abundant in urban areas than in rural areas and that species interactions remain intact.
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FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
As human‐induced change eliminates natural habitats, it impacts genetic diversity and population connectivity for local biodiversity. The South African Cape Floristic Region (CFR) is the most diverse ...extratropical area for plant biodiversity, and much of its habitat is protected as a UNESCO World Heritage site. There has long been great interest in explaining the underlying factors driving this unique diversity, especially as much of the CFR is endangered by urbanization and other anthropogenic activity. Here, we use a population and landscape genetic analysis of SNP data from the CFR endemic plant Leucadendron salignum or “common sunshine conebush” as a model to address the evolutionary and environmental factors shaping the vast CFR diversity. We found that high population structure, along with relatively deeper and older genealogies, is characteristic of the southwestern CFR, whereas low population structure and more recent lineage coalescence depict the eastern CFR. Population network analyses show genetic connectivity is facilitated in areas of lower elevation and higher seasonal precipitation. These population genetic signatures corroborate CFR species‐level patterns consistent with high Pleistocene biome stability and landscape heterogeneity in the southwest, but with coincident instability in the east. Finally, we also find evidence of human land‐usage as a significant gene flow barrier, especially in severely threatened lowlands where genetic connectivity has been historically the highest. These results help identify areas where conservation plans can prioritize protecting high genetic diversity threatened by contemporary human activities within this unique cultural UNESCO site.
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FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
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