Urbanization as a facilitator of gene flow in a human health pest

Abstract

Urban fragmentation can reduce gene flow that isolates populations, reduces genetic diversity and increases population differentiation, all of which have negative conservation implications. Alternatively, gene flow may actually be increased among urban areas consistent with an urban facilitation model. In fact, urban adapter pests are able to thrive in the urban environment and may be experiencing human-mediated transport. Here, we used social network theory with a population genetic approach to investigate the impact of urbanization on genetic connectivity in the Western black widow spider, as an urban pest model of human health concern. We collected genomewide single nucleotide polymorphism variation from mitochondrial and nuclear double-digest RAD (ddRAD) sequence data sets from 210 individuals sampled from 11 urban and 10 nonurban locales across its distribution of the Western United States. From urban and nonurban contrasts of population, phylogenetic, and network analyses, urban locales have higher within-population genetic diversity, lower between-population genetic differentiation and higher estimates of genetic connectivity. Social network analyses show that urban locales not only have more connections, but can act as hubs that drive connectivity among nonurban locales, which show signatures of historical isolation. These results are consistent with an urban facilitation model of gene flow and demonstrate the importance of sampling multiple cities and markers to identify the role that urbanization has had on larger spatial scales. As the urban landscape continues to grow, this approach will help determine what factors influence the spread and adaptation of pests, like the venomous black widow spider, in building policies for human and biodiversity health.

Gene flow and genetic drift in urban environments

“…Our third prediction, following the “urban facilitation” model, is that urbanization decreases genetic differentiation by effectively increasing gene flow among urban populations. For example, urbanization not only facilitates gene flow among urban populations, but also among nonurban populations of the Western black widow spider ( Latrodectus hesperus Chamberlin and Ivie; Miles, Johnson, et al, ). Specifically, over 1 million genome‐wide SNPs were used to estimate genetic differentiation among 10 urban and 11 nonurban populations sampled across the Western United States.…”

“…Specifically, over 1 million genome‐wide SNPs were used to estimate genetic differentiation among 10 urban and 11 nonurban populations sampled across the Western United States. Genetic differentiation ( F ST ) was significantly lower between urban pairs than nonurban pairs of populations, and genetic connectivity (measured using population network graphs) was greater among urban populations (Miles, Johnson, et al, ). One possible cause of increased connectivity among urban sites is the accidental transport of L. hesperus individuals on vehicles and in the movement of commercial fruit crops (Miles, Johnson, et al, ), all of which are consistent with the prediction that urbanization may facilitate gene flow.…”

“…For example, urban fragmentation increased genetic differentiation among urban populations of striped field mice ( Apodemus agrarius Pallas) compared with rural populations; thus, there was higher genetic differentiation at all geographic scales for urban populations, although there was no evidence of IBD ( p = .87; Gortat et al, ). However, for urban Western black widow spiders ( L. hesperus ), genetic differentiation was overall lower for urban populations than nonurban populations as a result of urban facilitation, such that even at large geographic scales, genetic differentiation was still low between urban populations, leading to a weak signature of IBD ( p = .15; Miles, Johnson, et al, ).…”

“…Studies in these unique ecoregions of rapid growth would provide further insight into the factors that contribute to variation in patterns of genetic drift and gene flow. For example, Western black widow spiders ( L. hesperus ) sampled in urban and nonurban populations across the Western United States experience urban‐facilitated gene flow, but certain cities act as “hubs” in driving gene flow (Miles, Dyer, & Verrelli, ; Miles, Johnson, et al, ). The variation in both the ecoregions and the level of urbanization of the cities sampled likely play a large role in what drives variance in gene flow among populations (Miles, Dyer, et al, ).…”

A roadmap for urban evolutionary ecology

“…Other species may colonize cities from nearby surrounding nonurban areas (Evans et al, ), and experience selection that further promotes the success of the newly established population (Mueller, Partecke, Hatchwell, Gaston, & Evans, ). Future work should aim for large‐scale sampling across multiple urban landscapes, characterize genomewide genetic variation (e.g., Combs et al, ; Mueller et al, ; Ravinet et al, ), and employ statistics in landscape and spatial population genetics to better understand the urban features and traits of organisms that affect rates of gene flow within and between cities (Beninde et al, ; Miles, Dyer, et al, ; Miles, Johnson, Dyer, & Verrelli, ).…”