Biology subjects

Santangelo, J. S.

Publications and source records attributed to Santangelo, J. S..

7 recordsLinked to original sources

bioRxiv2024

Structural variants underlie parallel adaptation following global invasion

Rapid adaptation during invasion has historically been considered limited and unpredictable. We leverage whole-genome sequencing of >2600 plants across six continents to investigate the relative roles of colonization history and adaptation during the worldwide invasion of Trifolium repens. Introduced populations contain high levels of genetic variation with independent colonization histories evident on different continents. Five large structural variants on three chromosomes exist as standing genetic variation within the native range, and exhibit strong signatures of parallel climate-associated adaptation across continents. Common gardens in the native and introduced ranges demonstrate that three structural variants exhibit patterns of selection consistent with local adaptation across each range. Our results provide strong evidence that rapid and parallel adaptation during invasion is caused by large-effect structural variants introduced throughout the world. Significance StatementBiological invasions occur over short timescales and introductions are often hypothesized to include limited genetic diversity, making the role of adaptation in invasion success controversial. We demonstrate that the invasion of a human-commensal species, Trifolium repens, likely stems from multiple, diverse introductions with significant evidence of climate-associated adaptation following introduction. The genetic basis of adaptation is most strongly linked to five chromosomal rearrangements that each span hundreds of genes - matching theoretical predictions that large-effect variants are key to the initial stages of adaptation to novel environments. Chromosomal rearrangements have remarkably parallel signatures of adaptation across different introductions despite initial colonization from different areas of Europe. Our study highlights the impact of globalization and rapid adaptation for the invasion success of human commensal species.

evolutionary biology↗

bioRxiv2024

Comparing approaches to quantify urbanization on a multicontinental scale

Urbanization is an increasingly prevalent driver of environmental, ecological, and evolutionary change in both terrestrial and aquatic systems, and it is important that our sampling designs accurately capture this urban environmental change. Common approaches to sampling urban environments include: urban-nonurban transects, which sample along urbanization gradients; random points, which sample locations at random within an area of interest; and systematic points, which sample locations based on a regularly-spaced grid from a predetermined starting point within the area of interest. Presently, we lack a comparative analysis of the efficacy of these different sampling designs in capturing variation in urban environments. Here, we compare the environmental variation captured by transect- and point-based sampling designs in 136 cities across six continents. We quantified and compared a common set of environmental variables for each sampling design, with variables capturing landcover, climate, and socioeconomic facets of urban environments. Mean landcover and socioeconomic metrics consistently differed among sampling designs, in contrast to climate variables that primarily varied among cities. Additionally, changes in environmental variables with distance from the city centre depended on the sampling design, with this distance-by-sampling design interaction present in 27%-51% of cities, depending on the environmental variable. This implies that the rate of environmental change along urban-nonurban gradients frequently depends on the sampling design used. We also examined potential causes of deviations between transect- and point-based sampling designs and identified human population density and city area as common predictors of deviations between transect- and point-sampling designs. Our results show that sampling design can dictate how the urban environment is characterized, with sampling design as important - or more important - as the selected environmental variable. We further developed R code so researchers can implement these methods as they develop and validate sampling designs in novel or unstudied urban environments.

ecology↗

bioRxiv2023

Does urbanization lead to parallel demographic shifts across the world in a cosmopolitan plant?

Urbanization 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 urbanization 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 a reduction in Ne linked to urbanization. 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 one of the largest comprehensive tests of demographic effects of urbanization and our results contrast 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.

evolutionary biology↗

bioRxiv2022

The effects of environmental heterogeneity within cities on the evolution of clines

O_LIThere 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. C_LIO_LIIn this study, we examined fine-scale variation in the presence of HCN--a potent anti-herbivore defense--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. C_LIO_LIWe 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. C_LIO_LISynthesis: 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. C_LI

evolutionary biology↗

bioRxiv2019

Multivariate phenotypic divergence along an urbanization gradient

A growing body of evidence suggests that natural populations can evolve to better tolerate the novel environmental conditions associated with urban areas. Invariably, studies of adaptive divergence in urban areas examine only one or a few traits at a time from populations residing only at the most extreme urban and nonurban habitats. Thus, whether urbanization is driving 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, and grew them up to measure multiple phenotypic traits in a common garden. Overall, urban populations had later phenology and germination, larger flowers, thinner stolons, reduced cyanogenesis, greater biomass, and were more attractive to pollinators. Pollinator observations revealed near complete turnover between urban and nonurban sites, which may explain some of the observed divergence in floral traits and phenology. Our results suggest that adaptation to urban environments involves multiple organismal traits.

evolutionary biology↗

bioRxiv2019

Predicting the strength of urban-rural clines in a Mendelian polymorphism along a latitudinal gradient

Cities are emerging as models for addressing the fundamental question of whether populations evolve in parallel to similar environments. Here, we examine the environmental factors that drive parallel evolutionary urban-rural clines in a Mendelian trait -- the cyanogenic antiherbivore defense of white clover (Trifolium repens). We sampled over 700 urban and rural clover populations across 16 cities along a latitudinal transect in eastern North America. In each population, we quantified the frequency of genotypes that produce hydrogen cyanide (HCN), and in a subset of the cities we estimated the frequency of the alleles at the two genes (CYP79D15 and Li) that epistatically interact to produce HCN. We then tested the hypothesis that winter environmental conditions cause the evolution of clines in HCN by comparing the strength of clines among cities located along a gradient of winter temperatures and frost exposure. Overall, half of the cities exhibited urban-rural clines in the frequency of HCN, whereby urban populations evolved lower HCN frequencies. The weakest clines in HCN occurred in cities with the lowest temperatures but greatest snowfall, supporting the hypothesis that snow buffers plants against winter frost and constrains the formation of clines. By contrast, the strongest clines occurred in the warmest cities where snow and frost are rare, suggesting that alternative selective agents are maintaining clines in warmer cities. Additionally, some clines were driven by evolution at only CYP79D15, consistent with stronger and more consistent selection on this locus than on Li. Together, our results demonstrate that both the agents and targets of selection vary across cities and highlight urban environments as large-scale models for disentangling the causes of parallel evolution in nature.\n\nImpact SummaryUnderstanding whether independent populations evolve in the same way (i.e., in parallel) when subject to similar environments remains an important problem in evolutionary biology. Urban environments are a model for addressing the extent of parallel evolution in nature due to their convergent environments (e.g. heat islands, pollution, fragmentation), such that two distant cities are often more similar to one another than either is to nearby nonurban habitats. In this paper, we used white clover (Trifolium repens) as a model to study the drivers of parallel evolution in response to urbanization. We collected >11,000 plants from urban and rural habitats across 16 cities in eastern North America to examine how cities influence the evolution of a Mendelian polymorphism for an antiherbivore defense trait - hydrogen cyanide (HCN). This trait had previously been shown to exhibit adaptive evolution to winter temperature gradients at continental scales. Here we tested the hypothesis that winter environmental conditions cause changes in the frequency of HCN between urban and rural habitats. We found that half of all cities had lower frequency of HCN producing genotypes relative to rural habitats, demonstrating that cities drive parallel losses of HCN in eastern North America. We then used environmental data to understand why cities vary in the extent to which they drive reduction in HCN frequencies. The warmest cities showed the greatest reductions in HCN frequencies in urban habitats, while colder, snowier cities showed little change in HCN between urban and rural habitats. This suggests that snow weakens the strength of natural selection against HCN in cities. However, it additionally suggests alternative ecological or evolutionary mechanisms drive the strong differences in HCN between urban and rural habitats in the warmest cities. Overall, our work highlights urban environments as powerful, large-scale models for disentangling the causes of parallel and non-parallel evolution in nature.

evolutionary biology↗

bioRxiv2018

Modern spandrels: The roles of genetic drift, gene flow and natural selection in the formation of parallel clines

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 (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 selections role in generating adaptive differentiation.

evolutionary biology↗