The evolution of city life Santangelo, James S; Rivkin, L Ruth; Johnson, Marc T J
Proceedings - Royal Society. Biological sciences/Proceedings - Royal Society. Biological Sciences,
08/2018, Volume:
285, Issue:
1884
Journal Article
Peer reviewed
Open access
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.
There is increasing evidence that environmental change associated with urbanization can drive rapid adaptation. However, most studies of urban adaptation have focused on coarse urban vs. rural ...comparisons or sampled along a single urban–rural environmental gradient, thereby ignoring the role that within‐city environmental heterogeneity might play in adaptation to urban environments.
In this study, we examined fine‐scale variation in the presence of hydrogen cyanide (HCN)—a potent anti‐herbivore defence—and its two underlying genes (Ac and Li) between park green spaces and surrounding suburban habitats for five city parks in the Greater Toronto Area.
We show that fine‐scale urbanization has driven the formation of micro‐clines in HCN on a scale of <2 km, though the presence and strength of micro‐clines varied across parks. Interestingly, these micro‐clines were driven by lower HCN frequencies inside park green spaces, and are therefore in the opposite direction to that predicted based on previously described patterns of HCN frequency change along urban–rural gradients.
Synthesis: These results suggest larger scale, adaptive urban–rural clines occur across a complex matrix of environmental heterogeneity within cities that drives fine‐scale adaptive microclines of varying strengths and directions.
These results suggest larger scale, adaptive urban–rural clines occur across a complex matrix of environmental heterogeneity within cities that drives fine‐scale adaptive microclines of varying strengths and directions.
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.
Urban environments offer the opportunity to study the role of adaptive and non-adaptive evolutionary processes on an unprecedented scale. While the presence of parallel clines in heritable phenotypic ...traits is often considered strong evidence for the role of natural selection, non-adaptive evolutionary processes can also generate clines, and this may be more likely when traits have a non-additive genetic basis due to epistasis. In this paper, we use spatially explicit simulations modelled according to the cyanogenesis (hydrogen cyanide, HCN) polymorphism in white clover (Trifolium repens) to examine the formation of phenotypic clines along urbanization gradients under varying levels of drift, gene flow and selection. HCN results from an epistatic interaction between two Mendelian-inherited loci. Our results demonstrate that the genetic architecture of this trait makes natural populations susceptible to decreases in HCN frequencies via drift. Gradients in the strength of drift across a landscape resulted in phenotypic clines with lower frequencies of HCN in strongly drifting populations, giving the misleading appearance of deterministic adaptive changes in the phenotype. Studies of heritable phenotypic change in urban populations should generate null models of phenotypic evolution based on the genetic architecture underlying focal traits prior to invoking selection's role in generating adaptive differentiation.
Pollinators and herbivores can both affect the evolutionary diversification of plant reproductive traits. However, plant defences frequently alter antagonistic and mutualistic interactions, and ...therefore, variation in plant defences may alter patterns of herbivore‐ and pollinator‐mediated selection on plant traits. We tested this hypothesis by conducting a common garden field experiment using 50 clonal genotypes of white clover (Trifolium repens) that varied in a Mendelian‐inherited chemical antiherbivore defence—the production of hydrogen cyanide (HCN). To evaluate whether plant defences alter herbivore‐ and/or pollinator‐mediated selection, we factorially crossed chemical defence (25 cyanogenic and 25 acyanogenic genotypes), herbivore damage (herbivore suppression) and pollination (hand pollination). We found that herbivores weakened selection for increased inflorescence production, suggesting that large displays are costly in the presence of herbivores. In addition, herbivores weakened selection on flower size but only among acyanogenic plants, suggesting that plant defences reduce the strength of herbivore‐mediated selection. Pollinators did not independently affect selection on any trait, although pollinators weakened selection for later flowering among cyanogenic plants. Overall, cyanogenic plant defences consistently increased the strength of positive directional selection on reproductive traits. Herbivores and pollinators both strengthened and weakened the strength of selection on reproductive traits, although herbivores imposed ~2.7× stronger selection than pollinators across all traits. Contrary to the view that pollinators are the most important agents of selection on reproductive traits, our data show that selection on reproductive traits is driven primarily by variation in herbivory and plant defences in this system.
The extent to which species can adapt to spatiotemporal climatic variation in their native and introduced ranges remains unresolved. To address this, we examined how clines in cyanogenesis (hydrogen ...cyanide HCN production—an antiherbivore defense associated with decreased tolerance to freezing) have shifted in response to climatic variation in space and time over a 60‐year period in both the native and introduced ranges of Trifolium repens. HCN production is a polymorphic trait controlled by variation at two Mendelian loci (Ac and Li). Using phenotypic assays, we estimated within‐population frequencies of HCN production and dominant alleles at both loci (i.e., Ac and Li) from 10,575 plants sampled from 131 populations on five continents, and then compared these frequencies to those from historical data collected in the 1950s. There were no clear relationships between changes in the frequency of HCN production, Ac, or Li and changes in temperature between contemporary and historical samples. We did detect evidence of continued evolution to temperature gradients in the introduced range, whereby the slope of contemporary clines for HCN and Ac in relation to winter temperature became steeper than historical clines and more similar to native clines. These results suggest that cyanogenesis clines show no clear changes through time in response to global warming, but introduced populations continue to adapt to their contemporary environments.
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 (
) 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.
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.
Urbanisation is occurring globally, leading to dramatic environmental changes that are altering the ecology and evolution of species. In particular, the expansion of human infrastructure and the loss ...and fragmentation of natural habitats in cities is predicted to increase genetic drift and reduce gene flow by reducing the size and connectivity of populations. Alternatively, the 'urban facilitation model' suggests that some species will have greater gene flow into and within cities leading to higher diversity and lower differentiation in urban populations. These alternative hypotheses have not been contrasted across multiple cities. Here, we used the genomic data from the GLobal Urban Evolution project (GLUE), to study the effects of urbanisation on non-adaptive evolutionary processes of white clover (Trifolium repens) at a global scale. We found that white clover populations presented high genetic diversity and no evidence of reduced N
linked to urbanisation. On the contrary, we found that urban populations were less likely to experience a recent decrease in effective population size than rural ones. In addition, we found little genetic structure among populations both globally and between urban and rural populations, which showed extensive gene flow between habitats. Interestingly, white clover displayed overall higher gene flow within urban areas than within rural habitats. Our study provides the largest comprehensive test of the demographic effects of urbanisation. Our results contrast with the common perception that heavily altered and fragmented urban environments will reduce the effective population size and genetic diversity of populations and contribute to their isolation.
Abstract
White clover (Trifolium repens L.; Fabaceae) is an important forage and cover crop in agricultural pastures around the world and is increasingly used in evolutionary ecology and genetics to ...understand the genetic basis of adaptation. Historically, improvements in white clover breeding practices and assessments of genetic variation in nature have been hampered by a lack of high-quality genomic resources for this species, owing in part to its high heterozygosity and allotetraploid hybrid origin. Here, we use PacBio HiFi and chromosome conformation capture (Omni-C) technologies to generate a chromosome-level, haplotype-resolved genome assembly for white clover totaling 998 Mbp (scaffold N50 = 59.3 Mbp) and 1 Gbp (scaffold N50 = 58.6 Mbp) for haplotypes 1 and 2, respectively, with each haplotype arranged into 16 chromosomes (8 per subgenome). We additionally provide a functionally annotated haploid mapping assembly (968 Mbp, scaffold N50 = 59.9 Mbp), which drastically improves on the existing reference assembly in both contiguity and assembly accuracy. We annotated 78,174 protein-coding genes, resulting in protein BUSCO completeness scores of 99.6% and 99.3% against the embryophyta_odb10 and fabales_odb10 lineage datasets, respectively.
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