skip to main content


Title: Urban colonization through multiple genetic lenses: The city‐fox phenomenon revisited
Abstract

Urbanization is driving environmental change on a global scale, creating novel environments for wildlife to colonize. Through a combination of stochastic and selective processes, urbanization is also driving evolutionary change. For instance, difficulty in traversing human‐modified landscapes may isolate newly established populations from rural sources, while novel selective pressures, such as altered disease risk, toxicant exposure, and light pollution, may further diverge populations through local adaptation. Assessing the evolutionary consequences of urban colonization and the processes underlying them is a principle aim of urban evolutionary ecology. In the present study, we revisited the genetic effects of urbanization on red foxes (Vulpes vulpes) that colonized Zurich, Switzerland. Through use of genome‐wide single nucleotide polymorphisms and microsatellite markers linked to the major histocompatibility complex (MHC), we expanded upon a previous neutral microsatellite study to assess population structure, characterize patterns of genetic diversity, and detect outliers associated with urbanization. Our results indicated the presence of one large evolutionary cluster, with substructure evident between geographic sampling areas. In urban foxes, we observed patterns of neutral and functional diversity consistent with founder events and reported increased differentiation between populations separated by natural and anthropogenic barriers. We additionally reported evidence of selection acting on MHC‐linked markers and identified outlier loci with putative gene functions related to energy metabolism, behavior, and immunity. We concluded that demographic processes primarily drove patterns of diversity, with outlier tests providing preliminary evidence of possible urban adaptation. This study contributes to our overall understanding of urban colonization ecology and emphasizes the value of combining datasets when examining evolutionary change in an increasingly urban world.

 
more » « less
NSF-PAR ID:
10462867
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology and Evolution
Volume:
9
Issue:
4
ISSN:
2045-7758
Page Range / eLocation ID:
p. 2046-2060
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Understanding the neutral (demographic) and adaptive processes leading to the differentiation of species and populations is a critical component of evolutionary and conservation biology. In this context, recently diverged taxa represent a unique opportunity to study the process of genetic differentiation. Northern and southern Idaho ground squirrels (Urocitellus brunneus—NIDGS, andUendemicus—SIDGS, respectively) are a recently diverged pair of sister species that have undergone dramatic declines in the last 50 years and are currently found in metapopulations across restricted spatial areas with distinct environmental pressures. Here we genotyped single‐nucleotide polymorphisms (SNPs) from buccal swabs with restriction site‐associated DNA sequencing (RADseq). With these data we evaluated neutral genetic structure at both the inter‐ and intraspecific level, and identified putatively adaptive SNPs using population structure outlier detection and genotype–environment association (GEA) analyses. At the interspecific level, we detected a clear separation between NIDGS and SIDGS, and evidence for adaptive differentiation putatively linked to torpor patterns. At the intraspecific level, we found evidence of both neutral and adaptive differentiation. For NIDGS, elevation appears to be the main driver of adaptive differentiation, while neutral variation patterns match and expand information on the low connectivity between some populations identified in previous studies using microsatellite markers. For SIDGS, neutral substructure generally reflected natural geographical barriers, while adaptive variation reflected differences in land cover and temperature, as well as elevation. These results clearly highlight the roles of neutral and adaptive processes for understanding the complexity of the processes leading to species and population differentiation, which can have important conservation implications in susceptible and threatened species.

     
    more » « less
  2. Abstract

    Genetic diversity is essential for populations to adapt to changing environments. Measures of genetic diversity are often based on selectively neutral markers, such as microsatellites. Genetic diversity to guide conservation management, however, is better reflected by adaptive markers, including genes of the major histocompatibility complex (MHC). Our aim was to assess MHC and neutral genetic diversity in two contrasting bottlenose dolphin (Tursiops aduncus) populations in Western Australia—one apparently viable population with high reproductive output (Shark Bay) and one with lower reproductive output that was forecast to decline (Bunbury). We assessed genetic variation in the two populations by sequencing the MHC class II DQB, which encompasses the functionally important peptide binding regions (PBR). Neutral genetic diversity was assessed by genotyping twenty‐three microsatellite loci.

    We confirmed that MHC is an adaptive marker in both populations. Overall, the Shark Bay population exhibited greater MHC diversity than the Bunbury population—for example, it displayed greater MHC nucleotide diversity. In contrast, the difference in microsatellite diversity between the two populations was comparatively low.

    Our findings are consistent with the hypothesis that viable populations typically display greater genetic diversity than less viable populations. The results also suggest that MHC variation is more closely associated with population viability than neutral genetic variation. Although the inferences from our findings are limited, because we only compared two populations, our results add to a growing number of studies that highlight the usefulness of MHC as a potentially suitable genetic marker for animal conservation. The Shark Bay population, which carries greater adaptive genetic diversity than the Bunbury population, is thus likely more robust to natural or human‐induced changes to the coastal ecosystem it inhabits.

     
    more » « less
  3. Abstract

    Many of the world's major cities are located in coastal zones, resulting in urban and industrial impacts on adjacent marine ecosystems. These pressures, which include pollutants, sewage, runoff and debris, temperature increases, hardened shorelines/structures, and light and acoustic pollution, have resulted in new evolutionary landscapes for coastal marine organisms. Marine environmental changes influenced by urbanization may create new selective regimes or may influence neutral evolution via impacts on gene flow or partitioning of genetic diversity across seascapes. While some urban selective pressures, such as hardened surfaces, are similar to those experienced by terrestrial species, others, such as oxidative stress, are specific to aquatic environments. Moreover, spatial and temporal scales of evolutionary responses may differ in the ocean due to the spatial extent of selective pressures and greater capacity for dispersal/gene flow. Here, we present a conceptual framework and synthesis of current research on evolutionary responses of marine organisms to urban pressures. We review urban impacts on genetic diversity and gene flow and examine evidence that marine species are adapting, or are predicted to adapt, to urbanization over rapid evolutionary time frames. Our findings indicate that in the majority of studies, urban stressors are correlated with reduced genetic diversity. Genetic structure is often increased in urbanized settings, but artificial structures can also act as stepping stones for some hard‐surface specialists, promoting range expansion. Most evidence for rapid adaptation to urban stressors comes from studies of heritable tolerance to pollutants in a relatively small number of species; however, the majority of marine ecotoxicology studies do not test directly for heritability. Finally, we highlight current gaps in our understanding of evolutionary processes in marine urban environments and present a framework for future research to address these gaps.

     
    more » « less
  4. Abstract

    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 154,770SNPs identified from transcriptome data from 48P. leucopusindividuals from three urban and three rural populations and used outlier tests to identify evidence of urban adaptation. We accounted for demography by simulating a neutralSNPdata 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.

     
    more » « less
  5. Abstract

    Understanding the genetic consequences of changes in species distributions has wide‐ranging implications for predicting future outcomes of climate change, for protecting threatened or endangered populations and for understanding the history that has led to current genetic patterns within species. Herein, we examine the genetic consequences of range expansion over a 25‐year period in a parasite (Geomydoecus aurei) that is in the process of expanding its geographic range via invasion of a novel host. By sampling the genetics of 1,935G. aureilice taken from 64 host individuals collected over this time period using 12 microsatellite markers, we test hypotheses concerning linear spatial expansion, genetic recovery time and allele surfing. We find evidence of decreasing allelic richness (AR) with increasing distance from the source population, supporting a linear, stepping stone model of spatial expansion that emphasizes the effects of repeated bottleneck events during colonization. We provide evidence of post‐bottleneck genetic recovery, with average AR of infrapopulations increasing about 30% over the 225‐generation span of time observed directly in this study. Our estimates of recovery rate suggest, however, that recovery has plateaued and that this population may not reach genetic diversity levels of the source population without further immigration from the source population. Finally, we employ a grid‐based sampling scheme in the region of ongoing population expansion and provide empirical evidence for the power of allele surfing to impart genetic structure on a population, even under conditions of selective neutrality and in a place that lacks strong barriers to gene flow.

     
    more » « less