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

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 Ne 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.

Brown rat demography reveals pre-commensal structure in eastern Asia before expansion into Southeast Asia.

Fossil evidence indicates that the globally distributed brown rat (Rattus norvegicus) originated in northern China and Mongolia. Historical records report the human-mediated invasion of rats into Europe in the 1500s, followed by global spread because of European imperialist activity during the 1600s-1800s. We analyzed 14 genomes representing seven previously identified evolutionary clusters, and tested alternative demographic models to infer patterns of range expansion, divergence times, and changes in effective population (N e) size for this globally important pest species. We observed three range expansions from the ancestral population that produced the Pacific (diverged ∼16.1 kya), eastern China (∼17.5 kya), and Southeast (SE) Asia (∼0.86 kya) lineages. Our model shows a rapid range expansion from SE Asia into the Middle East and then continued expansion into central Europe 788 yr ago (1227 AD). We observed declining N e within all brown rat lineages from 150-1 kya, reflecting population contractions during glacial cycles. N e increased since 1 kya in Asian and European, but not in Pacific, evolutionary clusters. Our results support the hypothesis that northern Asia was the ancestral range for brown rats. We suggest that southward human migration across China between the 800s-1550s AD resulted in the introduction of rats to SE Asia, from which they rapidly expanded via existing maritime trade routes. Finally, we discovered that North America was colonized separately on both the Atlantic and Pacific seaboards, by evolutionary clusters of vastly different ages and genomic diversity levels. Our results should stimulate discussions among historians and zooarcheologists regarding the relationship between humans and rats.

Commensal Rats and Humans: Integrating Rodent Phylogeography and Zooarchaeology to Highlight Connections between Human Societies.

Phylogeography and zooarchaeology are largely separate disciplines, yet each interrogates relationships between humans and commensal species. Knowledge gained about human history from studies of four commensal rats (Rattus rattus, R. tanezumi, R. exulans, and R. norvegicus) is outlined, and open questions about their spread alongside humans are identified. Limitations of phylogeographic and zooarchaeological studies are highlighted, then how integration would increase understanding of species' demographic histories and resultant inferences about human societies is discussed. How rat expansions have informed the understanding of human migration, urban settlements, trade networks, and intra- and interspecific competition is reviewed. Since each rat species is associated with different human societies, they identify unique ecological and historical/cultural conditions that influenced their expansion. Finally, priority research areas including nuclear genome based phylogeographies are identified using archaeological evidence to understand R. norvegicus expansion across China, multi-wave colonization of R. rattus across Europe, and competition between R. rattus and R. norvegicus.

Genomic analyses reveal three independent introductions of the invasive brown rat (Rattus norvegicus) to the Faroe Islands.

Population genomics offers innovative approaches to test hypotheses related to the source and timing of introduction of invasive species. These approaches are particularly appropriate to study colonization of island ecosystems. The brown rat is a cold-hardy global invasive that has reached most of the world's island ecosystems, including even highly isolated archipelagoes such as the Faroe Islands in the North Atlantic Ocean. Historic records tell of rats rafting to the southern island of Suðuroy in 1768 following a shipwreck off the coast of Scotland, then expanding across the archipelago. We investigated the demographic history of brown rats in the Faroes using 50,174 SNPs. We inferred three independent introductions of rats, including to Suðuroy, the islands of Borðoy and Viðoy, and onto Streymoy from which they expanded to Eysturoy and Vágar. All Faroese populations showed signs of strong bottlenecks and declining effective population size. We inferred that these founder events removed low frequency alleles, the exact data needed to estimate recent demographic histories. Therefore, we were unable to accurately estimate the timing of each invasion. The difficulties with demographic inference may be applicable to other invasive species, particularly those with extreme and recent bottlenecks. We identified three invasions of brown rats to the Faroe Islands that resulted in highly differentiated populations that will be useful for future studies of life history variation and genomic adaptation.

Peromyscus transcriptomics: Understanding adaptation and gene expression plasticity within and between species of deer mice.

Deer mice in the genus Peromyscus occupy nearly every terrestrial habitat in North America, and have a long history as subjects of behavioral, ecological, evolutionary, and physiological study. Recent advances in transcriptomics, the study of the complete set of RNA transcripts produced by certain cell types or under certain conditions, have contributed to the development of Peromyscus as a model system. We review the recent use of transcriptomics to investigate how natural selection and gene expression plasticity contribute to the existence of deer mice in challenging environments such as highlands, deserts, and cities across North America. Transcriptomics also holds great promise for elucidating the genetic basis of mating systems and other behaviors in Peromyscus, but has to date been underutilized for developmental biology and disease studies. Future Peromyscus studies should apply robust comparative frameworks to analyze the transcriptomics of multiple populations of the same species across varying environmental conditions, as well as multiple species that vary in traits of interest.

Gene flow and genetic drift in urban environments.

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.

Urban rat races: spatial population genomics of brown rats (Rattus norvegicus) compared across multiple cities.

Urbanization often substantially influences animal movement and gene flow. However, few studies to date have examined gene flow of the same species across multiple cities. In this study, we examine brown rats (Rattus norvegicus) to test hypotheses about the repeatability of neutral evolution across four cities: Salvador, Brazil; New Orleans, USA; Vancouver, Canada; and New York City, USA. At least 150 rats were sampled from each city and genotyped for a minimum of 15 000 genome-wide single nucleotide polymorphisms. Levels of genome-wide diversity were similar across cities, but varied across neighbourhoods within cities. All four populations exhibited high spatial autocorrelation at the shortest distance classes (less than 500 m) owing to limited dispersal. Coancestry and evolutionary clustering analyses identified genetic discontinuities within each city that coincided with a resource desert in New York City, major waterways in New Orleans, and roads in Salvador and Vancouver. Such replicated studies are crucial to assessing the generality of predictions from urban evolution, and have practical applications for pest management and public health. Future studies should include a range of global cities in different biomes, incorporate multiple species, and examine the impact of specific characteristics of the built environment and human socioeconomics on gene flow.

Spatial population genomics of the brown rat (Rattus norvegicus) in New York City.

Human commensal species such as rodent pests are often widely distributed across cities and threaten both infrastructure and public health. Spatially explicit population genomic methods provide insights into movements for cryptic pests that drive evolutionary connectivity across multiple spatial scales. We examined spatial patterns of neutral genomewide variation in brown rats (Rattus norvegicus) across Manhattan, New York City (NYC), using 262 samples and 61,401 SNPs to understand (i) relatedness among nearby individuals and the extent of spatial genetic structure in a discrete urban landscape; (ii) the geographic origin of NYC rats, using a large, previously published data set of global rat genotypes; and (iii) heterogeneity in gene flow across the city, particularly deviations from isolation by distance. We found that rats separated by ≤200 m exhibit strong spatial autocorrelation (r = .3, p = .001) and the effects of localized genetic drift extend to a range of 1,400 m. Across Manhattan, rats exhibited a homogeneous population origin from rats that likely invaded from Great Britain. While traditional approaches identified a single evolutionary cluster with clinal structure across Manhattan, recently developed methods (e.g., fineSTRUCTURE, sPCA, EEMS) provided evidence of reduced dispersal across the island's less residential Midtown region resulting in fine-scale genetic structuring (FST  = 0.01) and two evolutionary clusters (Uptown and Downtown Manhattan). Thus, while some urban populations of human commensals may appear to be continuously distributed, landscape heterogeneity within cities can drive differences in habitat quality and dispersal, with implications for the spatial distribution of genomic variation, population management and the study of widely distributed pests.

Signatures of positive selection and local adaptation to urbanization in white-footed mice (Peromyscus leucopus).

Urbanization significantly alters natural ecosystems and has accelerated globally. Urban wildlife populations are often highly fragmented by human infrastructure, and isolated populations may adapt in response to local urban pressures. However, relatively few studies have identified genomic signatures of adaptation in urban animals. We used a landscape genomic approach to examine signatures of selection in urban populations of white-footed mice (Peromyscus leucopus) in New York City. We analysed 154,770 SNPs identified from transcriptome data from 48 P. leucopus individuals from three urban and three rural populations and used outlier tests to identify evidence of urban adaptation. We accounted for demography by simulating a neutral SNP data set under an inferred demographic history as a null model for outlier analysis. We also tested whether candidate genes were associated with environmental variables related to urbanization. In total, we detected 381 outlier loci and after stringent filtering, identified and annotated 19 candidate loci. Many of the candidate genes were involved in metabolic processes and have well-established roles in metabolizing lipids and carbohydrates. Our results indicate that white-footed mice in New York City are adapting at the biomolecular level to local selective pressures in urban habitats. Annotation of outlier loci suggests selection is acting on metabolic pathways in urban populations, likely related to novel diets in cities that differ from diets in less disturbed areas.

Genomewide SNP data reveal cryptic phylogeographic structure and microallopatric divergence in a rapids-adapted clade of cichlids from the Congo River.

The lower Congo River is a freshwater biodiversity hot spot in Africa characterized by some of the world's largest rapids. However, little is known about the evolutionary forces shaping this diversity, which include numerous endemic fishes. We investigated phylogeographic relationships in Teleogramma, a small clade of rheophilic cichlids, in the context of regional geography and hydrology. Previous studies have been unable to resolve phylogenetic relationships within Teleogramma due to lack of variation in nuclear genes and discrete morphological characters among putative species. To sample more broadly across the genome, we analysed double-digest restriction-associated sequencing (ddRAD) data from 53 individuals across all described species in the genus. We also assessed body shape and mitochondrial variation within and between taxa. Phylogenetic analyses reveal previously unrecognized lineages and instances of microallopatric divergence across as little as ~1.5 km. Species ranges appear to correspond to geographic regions broadly separated by major hydrological and topographic barriers, indicating these features are likely important drivers of diversification. Mitonuclear discordance indicates one or more introgressive hybridization events, but no clear evidence of admixture is present in nuclear genomes, suggesting these events were likely ancient. A survey of female fin patterns hints that previously undetected lineage-specific patterning may be acting to reinforce species cohesion. These analyses highlight the importance of hydrological complexity in generating diversity in certain freshwater systems, as well as the utility of ddRAD-Seq data in understanding diversification processes operating both below and above the species level.

Global population divergence and admixture of the brown rat (Rattus norvegicus).

Native to China and Mongolia, the brown rat (Rattus norvegicus) now enjoys a worldwide distribution. While black rats and the house mouse tracked the regional development of human agricultural settlements, brown rats did not appear in Europe until the 1500s, suggesting their range expansion was a response to relatively recent increases in global trade. We inferred the global phylogeography of brown rats using 32 k SNPs, and detected 13 evolutionary clusters within five expansion routes. One cluster arose following a southward expansion into Southeast Asia. Three additional clusters arose from two independent eastward expansions: one expansion from Russia to the Aleutian Archipelago, and a second to western North America. Westward expansion resulted in the colonization of Europe from which subsequent rapid colonization of Africa, the Americas and Australasia occurred, and multiple evolutionary clusters were detected. An astonishing degree of fine-grained clustering between and within sampling sites underscored the extent to which urban heterogeneity shaped genetic structure of commensal rodents. Surprisingly, few individuals were recent migrants, suggesting that recruitment into established populations is limited. Understanding the global population structure of R. norvegicus offers novel perspectives on the forces driving the spread of zoonotic disease, and aids in development of rat eradication programmes.

Urbanization shapes the demographic history of a native rodent (the white-footed mouse, Peromyscus leucopus) in New York City.

How urbanization shapes population genomic diversity and evolution of urban wildlife is largely unexplored. We investigated the impact of urbanization on white-footed mice,Peromyscus leucopus,in the New York City (NYC) metropolitan area using coalescent-based simulations to infer demographic history from the site-frequency spectrum. We assigned individuals to evolutionary clusters and then inferred recent divergence times, population size changes and migration using genome-wide single nucleotide polymorphisms genotyped in 23 populations sampled along an urban-to-rural gradient. Both prehistoric climatic events and recent urbanization impacted these populations. Our modelling indicates that post-glacial sea-level rise led to isolation of mainland and Long Island populations. These models also indicate that several urban parks represent recently isolated P. leucopus populations, and the estimated divergence times for these populations are consistent with the history of urbanization in NYC.

Go forth, evolve and prosper: the genetic basis of adaptive evolution in an invasive species.

Invasive species stand accused of a familiar litany of offences, including displacing native species, disrupting ecological processes and causing billions of dollars in ecological damage (Cox 1999). Despite these transgressions, invasive species have at least one redeeming virtue--they offer us an unparalleled opportunity to investigate colonization and responses of populations to novel conditions in the invaded habitat (Elton 1958; Sakai et al. 2001). Invasive species are by definition colonists that have arrived and thrived in a new location. How they are able to thrive is of great interest, especially considering a paradox of invasion (Sax & Brown 2000): if many populations are locally adapted (Leimu & Fischer 2008), how could species introduced into new locations become so successful? One possibility is that populations adjust to the new conditions through plasticity--increasing production of allelopathic compounds (novel weapons), or taking advantage of new prey, for example. Alternatively, evolution could play a role, with the populations adapting to the novel conditions of the new habitat. There is increasing evidence, based on phenotypic data, for rapid adaptive evolution in invasive species (Franks et al. 2012; Colautti & Barrett 2013; Sultan et al. 2013). Prior studies have also demonstrated genetic changes in introduced populations using neutral markers, which generally do not provide information on adaptation. Thus, the genetic basis of adaptive evolution in invasive species has largely remained unknown. In this issue of Molecular Ecology, Vandepitte et al. (2014) provide some of the first evidence in invasive populations for molecular genetic changes directly linked to adaptation.

Online toolkits for collaborative and inclusive global research in urban evolutionary ecology.

Urban evolutionary ecology is inherently interdisciplinary. Moreover, it is a field with global significance. However, bringing researchers and resources together across fields and countries is challenging. Therefore, an online collaborative research hub, where common methods and best practices are shared among scientists from diverse geographic, ethnic, and career backgrounds would make research focused on urban evolutionary ecology more inclusive. Here, we describe a freely available online research hub for toolkits that facilitate global research in urban evolutionary ecology. We provide rationales and descriptions of toolkits for: (1) decolonizing urban evolutionary ecology; (2) identifying and fostering international collaborative partnerships; (3) common methods and freely-available datasets for trait mapping across cities; (4) common methods and freely-available datasets for cross-city evolutionary ecology experiments; and (5) best practices and freely available resources for public outreach and communication of research findings in urban evolutionary ecology. We outline how the toolkits can be accessed, archived, and modified over time in order to sustain long-term global research that will advance our understanding of urban evolutionary ecology.

Effects of urban-induced mutations on ecology, evolution and health.

Increasing evidence suggests that urbanization is associated with higher mutation rates, which can affect the health and evolution of organisms that inhabit cities. Elevated pollution levels in urban areas can induce DNA damage, leading to de novo mutations. Studies on mutations induced by urban pollution are most prevalent in humans and microorganisms, whereas studies of non-human eukaryotes are rare, even though increased mutation rates have the potential to affect organisms and their populations in contemporary time. Our Perspective explores how higher mutation rates in urban environments could impact the fitness, ecology and evolution of populations. Most mutations will be neutral or deleterious, and higher mutation rates associated with elevated pollution in urban populations can increase the risk of cancer in humans and potentially other species. We highlight the potential for urban-driven increased deleterious mutational loads in some organisms, which could lead to a decline in population growth of a wide diversity of organisms. Although beneficial mutations are expected to be rare, we argue that higher mutation rates in urban areas could influence adaptive evolution, especially in organisms with short generation times. Finally, we explore avenues for future research to better understand the effects of urban-induced mutations on the fitness, ecology and evolution of city-dwelling organisms.

Urban landscape genetics: canopy cover predicts gene flow between white-footed mouse (Peromyscus leucopus) populations in New York City.

In this study, I examine the influence of urban canopy cover on gene flow between 15 white-footed mouse (Peromyscus leucopus) populations in New York City parklands. Parks in the urban core are often highly fragmented, leading to rapid genetic differentiation of relatively nonvagile species. However, a diverse array of 'green' spaces may provide dispersal corridors through 'grey' urban infrastructure. I identify urban landscape features that promote genetic connectivity in an urban environment and compare the success of two different landscape connectivity approaches at explaining gene flow. Gene flow was associated with 'effective distances' between populations that were calculated based on per cent tree canopy cover using two different approaches: (i) isolation by effective distance (IED) that calculates the single best pathway to minimize passage through high-resistance (i.e. low canopy cover) areas, and (ii) isolation by resistance (IBR), an implementation of circuit theory that identifies all low-resistance paths through the landscape. IBR, but not IED, models were significantly associated with three measures of gene flow (Nm from F(ST) , BayesAss+ and Migrate-n) after factoring out the influence of isolation by distance using partial Mantel tests. Predicted corridors for gene flow between city parks were largely narrow, linear parklands or vegetated spaces that are not managed for wildlife, such as cemeteries and roadway medians. These results have implications for understanding the impacts of urbanization trends on native wildlife, as well as for urban reforestation efforts that aim to improve urban ecosystem processes.

DNA metabarcoding reveals that coyotes in New York City consume wide variety of native prey species and human food.

Carnivores are currently colonizing cities where they were previously absent. These urban environments are novel ecosystems characterized by habitat degradation and fragmentation, availability of human food, and different prey assemblages than surrounding areas. Coyotes (Canis latrans) established a breeding population in New York City (NYC) over the last few decades, but their ecology within NYC is poorly understood. In this study, we used non-invasive scat sampling and DNA metabarcoding to profile vertebrate, invertebrate, and plant dietary items with the goal to compare the diets of urban coyotes to those inhabiting non-urban areas. We found that both urban and non-urban coyotes consumed a variety of plants and animals as well as human food. Raccoons (Procyon lotor) were an important food item for coyotes within and outside NYC. In contrast, white-tailed deer (Odocoileus virginianus) were mainly eaten by coyotes inhabiting non-urban areas. Domestic chicken (Gallus gallus) was the human food item found in most scats from both urban and non-urban coyotes. Domestic cats (Felis catus) were consumed by urban coyotes but were detected in only a small proportion of the scats (<5%), which differs markedly from high rates of cat depredation in some other cities. In addition, we compared our genetic metabarcoding analysis to a morphological analysis of the same scat samples. We found that the detection similarity between the two methods was low and it varied depending on the type of diet item.

A global horizon scan for urban evolutionary ecology.

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.

Relatedness and demography of African forest elephants: inferences from noninvasive fecal DNA analyses.

African forest elephants (Loxodonta cyclotis) are genetically and morphologically distinct from their savannah counterparts, but their biology remains poorly understood. In this study, I use noninvasive fecal DNA analyses to examine the relatedness structure and historical demography of forest elephants at 2 sites in SW Gabon, central Africa. Pairwise relatedness values calculated between 162 elephant individuals genotyped at 8 microsatellite loci were significantly higher within spatially associated dung piles than between random pairings for one site. First- and second-order relatives were most commonly detected among dung piles from adult female pairs and adult females and juveniles. Pairwise relatedness estimates suggested that, like savannah elephants, forest groups are largely composed of adult females, their sisters, and juvenile offspring. Associations between males, and groups containing juveniles from multiple related females, were detected but at much lower frequency. Analysis of mitochondrial d-loop sequences from 70 elephant individuals identified 2 haplogroups in SW Gabon.

Genetic diversity and distinctiveness of the proboscis monkeys (Nasalis larvatus) of the Klias Peninsula, Sabah, Malaysia.

In this study, we sequenced a partial segment of the mitochondrial control region from 21 proboscis monkeys of the Klias peninsula, the last large population remaining on the west coast of Sabah, Malaysia. Our results showed that this population retains substantial genetic variation, and subpopulations from different river systems in the central and southern portions of the Klias share multiple haplotypes. We also compared our data with previously generated sequences from 2 eastern populations of proboscis monkeys in Sabah and found little evidence of regional genetic structure. Based on these results, we argue that conservation efforts should focus on restoring connectivity between central and southern Klias peninsula proboscis monkeys and discuss future analyses needed to better understand the mitochondrial structure of proboscis monkeys in Sabah.