Evolution of genomic variation in the burrowing owl in response to recent colonization of urban areas

Abstract

When a species successfully colonizes an urban habitat it can be expected that its population rapidly adapts to the new environment but also experiences demographic perturbations. It is, therefore, essential to gain an understanding of the population structure and the demographic history of the urban and neighbouring rural populations before studying adaptation at the genome level. Here, we investigate populations of the burrowing owl (Athene cunicularia), a species that colonized South American cities just a few decades ago. We assembled a high-quality genome of the burrowing owl and re-sequenced 137 owls from three urban–rural population pairs at 17-fold median sequencing coverage per individual. Our data indicate that each city was independently colonized by a limited number of founders and that restricted gene flow occurred between neighbouring urban and rural populations, but not between urban populations of different cities. Using long-range linkage disequilibrium statistics in an approximate Bayesian computation approach, we estimated consistently lower population sizes in the recent past for the urban populations in comparison to the rural ones. The current urban populations all show reduced standing variation in rare single nucleotide polymorphisms (SNPs), but with different subsets of rare SNPs in different cities. This lowers the potential for local adaptation based on rare variants and makes it harder to detect consistent signals of selection in the genome.

A roadmap for urban evolutionary ecology

“…Along with standard trait‐based assessments of vulnerability to urbanization (Bush et al, ), mapping the historical distribution and evolutionary histories of urban‐dwelling species could provide additional insight into their conservation. For example, Mueller et al () examined burrowing owls, which traditionally inhabited increasingly rare grassland habitats, but have recently established populations in three Argentinian cities. The owls have developed the novel behavior of digging their own burrows, instead of relying on the burrows of other species, which may have facilitated their colonization of urban habitats.…”

“…and Athene cunicularia Molina (burrowing owls; Mueller et al, 2018) 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, 2018).…”

The evolution of city life

“…Multiple papers show that urbanization is frequently associated with changes in natural selection [25][26][27][28], and that populations can locally adapt to urban environments at both phenotypic [27 -30,35] and genomic scales [42,43] (gap 2). Seven studies examine the repeatability of non-adaptive and adaptive evolution across cities and they find examples of both convergent and nonconvergent evolution [28,[35][36][37][38][39]42] (gap 3). Finally, multiple studies leverage the power of genomics to understand how urbanization affects non-adaptive and adaptive evolution [37 -39,41 -43] (gap 4), including how new urban species [37] and well-established human commensals arise [43] (gap 5).…”

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).…”