Genome-wide single nucleotide polymorphism scan suggests adaptation to urbanization in an important pollinator, the red-tailed bumblebee ( Bombus lapidarius L.)

Abstract

Urbanization is considered a global threat to biodiversity; the growth of cities results in an increase in impervious surfaces, soil and air pollution, fragmentation of natural vegetation and invasion of non-native species, along with numerous environmental changes, including the heat island phenomenon. The combination of these effects constitutes a challenge for both the survival and persistence of many native species, while also imposing altered selective regimes. Here, using 110 314 single nucleotide polymorphisms generated by restriction-site-associated DNA sequencing, we investigated the genome-wide effects of urbanization on putative neutral and adaptive genomic diversity in a major insect pollinator, , collected from nine German cities and nine paired rural sites. Overall, genetic differentiation among sites was low and there was no obvious genome-wide genetic structuring, suggesting the absence of strong effects of urbanization on gene flow. We nevertheless identified several loci under directional selection, a subset of which was associated with urban land use, including the percentage of impervious surface surrounding each sampling site. Overall, our results provide evidence of local adaptation to urbanization in the face of gene flow in a highly mobile insect pollinator.

Gene flow and genetic drift in urban environments

“…For example, analyses of genome-wide SNPs in red-tailed bumblebees (Bombus lapidarius Linnaeus) across nine urban and nine nonurban sites in Germany found little evidence of population structure associated with urbanization and suggest panmixia(Theodorou et al, 2018). The authors argue their results are unsurprising given the mobility of the species and the large dispersal ranges of the queens and males(Lepais et al, 2010), all of which is consistent with the prediction that gene flow may be uninhibited by urbanization.Our second prediction, following the "urban fragmentation" model, is that urbanization increases genetic differentiation by impeding gene flow among urban populations.…”

“…Our first prediction is that genetic differentiation is unaltered in urban habitats when gene flow between populations is unaffected by urbanization, and this prediction serves as a “null model.” This pattern may be a common trend among highly mobile organisms (Medina et al, ). For example, analyses of genome‐wide SNPs in red‐tailed bumblebees ( Bombus lapidarius Linnaeus) across nine urban and nine nonurban sites in Germany found little evidence of population structure associated with urbanization and suggest panmixia (Theodorou et al, ). The authors argue their results are unsurprising given the mobility of the species and the large dispersal ranges of the queens and males (Lepais et al, ), all of which is consistent with the prediction that gene flow may be uninhibited by urbanization.…”

A roadmap for urban evolutionary ecology

“…At the trait level: in Anolis cristatellus (crested anole) and Trifolium repens (white clover), the same trait changes (morphology in anoles, cyanogenesis in T. repens) were observed in multiple urban populations (Thompson et al, 2016;Winchell et al, 2016). At the whole-organism performance level: Temnothorax curvispinosus (acorn ant) exhibited a similar change in thermal performance in multiple urban populations (Diamond et al, 2018(Diamond et al, ) et al, 2016Theodorou et al, 2018;Winchell et al, 2016;Yakub & Tiffin, 2017), yet several questions remain unresolved. First, it is important to understand why convergence is often imperfect (Bolnick, Barrett, Oke, Rennison, & Stuart, 2018) We suggest several approaches to address gaps in our understanding of the prevalence of convergent evolution among cities.…”

“…The presence of numerous pest species (e.g., rats, bedbugs, cockroaches, lice) and human commensals (e.g., pigeons, house sparrows, white clover) specifically adapted to living on or around humans indicates that species have already evolved to specialize on the environments that we create (Johnson & Munshi‐South, ; Thompson et al, ). Recent genomic evidence from Bombus lapidarius Linnaeus (red‐tailed bumblebees; Theodorou et al, ), Passer domesticus Linnaeus (house sparrows; Ravinet et al, ), and Athene cunicularia Molina (burrowing owls; Mueller et al, ) shows that this process of colonization and adaptation to human environments is ongoing. For example, house sparrows originated only 11 Kya, and their adaptation to human environments has involved adaptive evolution of starch metabolism genes, presumably in response to feeding on human‐processed foods (Ravinet et al, ).…”

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

“…The possibility for urban-rural gradients facilitating divergence has created a need for more research dedicated to assessing the evolutionary changes associated with urbanization (Alberti, 2015;Donihue & Lambert, 2015;Santangelo et al, 2018). As such, there has recently been a surge of studies examining the genetic effects of urbanization across diverse taxa, with each system providing unique insights into the processes shaping wildlife in the Anthropocene (Combs, Byers et al, 2018;Johnson, Prashad, Lavoignat, & Saini, 2018;Miles, Dyer, & Verrelli, 2018;Mueller, Kuhl et al, 2018;Theodorou et al, 2018).…”