James S. Santangelo

1 The coast redwood ( Sequoia sempervirens ) is a long-lived, hexaploid conifer of high ecological, cultural, and economic value whose range has been greatly reduced by historical logging [1]. Effective restoration and conservation depend on understanding patterns of genetic differentiation across the redwood range to delineate populations for management prioritization. Yet, past range-wide studies provided only a partial picture of population structure in coast redwood as they relied on a limited set of genetic markers [2, 3] or limited sampling, as sequencing was done on the same range-wide provenance collection [4, 5]. Here, we analyze 334,029 SNPs from a new range-wide set of 224 individuals using a dosage-based approach that accounts for polyploidy. Principal coordinates and clustering analyses reveal clear latitudinal structure, with a steeper break south of San Francisco Bay. Outlier SNP analysis identified new candidate loci involved in salinity tolerance, climate stress response, and nutrient uptake, suggesting potential local adaptation. These results point to the central role of geography in shaping genetic variation in coast redwood and give scientific basis for designing new conservation and management strategies aimed at preserving the species’ genetic diversity into the future.

The role of rapid adaptation during species invasions has historically been minimized with the assumption that introductions consist of few colonists and limited genetic diversity. While overwhelming evidence suggests that rapid adaptation is more prevalent than originally assumed, the demographic and adaptive processes underlying successful invasions remain unresolved. Here we leverage a large whole-genome sequence dataset to investigate the relative roles of colonization history and adaptation during the worldwide invasion of the forage crop, Trifolium repens (Fabaceae). We show that introduced populations encompass high levels of genetic variation with little evidence of bottlenecks. Independent colonization histories on different continents are evident from genome-wide population structure. Five haploblocks—large haplotypes with limited recombination—on three chromosomes exist as standing genetic variation within the native and introduced ranges and exhibit strong signatures of parallel climate-associated adaptation across continents. Field experiments in the native and introduced ranges demonstrate that three of the haploblocks strongly affect fitness and exhibit patterns of selection consistent with local adaptation across each range. Our results provide strong evidence that large-effect structural variants contribute substantially to rapid and parallel adaptation of an introduced species throughout the world.

Urbanization is increasingly recognized as a powerful force of evolutionary change. However, anthropogenic sources of selection can often be similarly strong and multifarious in rural habitats, and whether selection differs in either strength or its targets between habitats is rarely considered. Despite numerous examples of phenotypic differentiation between urban and rural populations, we still lack an understanding of the genes enabling adaptation to these contrasting habitats. In this study, we conducted whole genome sequencing of 120 urban, suburban, and rural white clover plants from Toronto, Canada, and used these data to identify urban and rural signatures of positive selection. We found evidence for selection in genomic regions involved in abiotic stress tolerance and growth/development in both urban and rural populations, and clinal change in allele frequencies at SNPs within these regions. Patterns of allele frequency and haplotype differentiation suggest that most sweeps are incomplete, and our strongest signals of selective sweeps overlap known large-effect structural variants. These results highlight how both urban and rural habitats are driving ongoing selection in Toronto white clover populations, and motivate future work disentangling the genetic architecture of ecologically important phenotypes underlying adaptation to contemporary anthropogenic habitats.

Climate change increasingly drives local population dynamics, shifts geographic distributions, and threatens persistence. Gene flow and rapid adaptation could rescue declining populations yet are seldom integrated into forecasts. We modeled eco-evolutionary dynamics under preindustrial, contemporary, and projected climates using up to 9 years of fitness data from 102,272 transplants (115 source populations) of Boechera stricta in five common gardens. Climate change endangers locally adapted populations and reduces genotypic variation in long-term population growth rate, suggesting limited adaptive potential. Upslope migration could stabilize high-elevation populations and preserve low-elevation ecotypes, but unassisted gene flow modeled with genomic data is too spatially restricted. Species distribution models failed to capture current dynamics and likely overestimate persistence under intermediate emissions scenarios, highlighting the importance of modeling evolutionary processes.

Urbanization is increasingly recognized as a powerful force of evolutionary change. However, anthropogenic sources of selection can often be similarly strong and mul­ tifarious in rural habitats, and whether selection differs in either strength or its targets between habitats is rarely considered. Despite numerous examples of phe­ notypic differentiation between urban and rural populations, we still lack an un­ derstanding of the genes enabling adaptation to these contrasting habitats. In this study, we conducted whole genome sequencing of 120 urban, suburban, and rural white clover plants from Toronto, Canada and used these data to identify urban and rural signatures of positive selection. We found evidence for selection in genomic regions involved in abiotic stress tolerance and growth/ development in both urban and rural populations, and clinal change in allele frequencies at SNPs within these regions. Patterns of allele frequency and haplotype differentiation suggest that most sweeps are incomplete and our strongest signals of selective sweeps overlap known large-effect structural variants. These results highlight how both urban and rural habitats are driving ongoing selection in Toronto white clover populations, and mo­ tivate future work disentangling the genetic architecture of ecologically important phenotypes underlying adaptation to contemporary anthropogenic habitats.

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 Statement Biological 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.

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.

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_e 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.

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 N _e 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.