Great tits and the city: Distribution of genomic diversity and gene–environment associations along an urbanization gradient

Abstract

Urbanization is a growing concern challenging the evolutionary potential of wild populations by reducing genetic diversity and imposing new selection regimes affecting many key fitness traits. However, genomic footprints of urbanization have received little attention so far. Using RAD sequencing, we investigated the genomewide effects of urbanization on neutral and adaptive genomic diversity in 140 adult great tits Parus major collected in locations with contrasted urbanization levels (from a natural forest to highly urbanized areas of a city; Montpellier, France). Heterozygosity was slightly lower in the more urbanized sites compared to the more rural ones. Low but significant effect of urbanization on genetic differentiation was found, at the site level but not at the nest level, indicative of the geographic scale of urbanization impact and of the potential for local adaptation despite gene flow. Gene-environment association tests identified numerous SNPs with small association scores to urbanization, distributed across the genome, from which a subset of 97 SNPs explained up to 81% of the variance in urbanization, overall suggesting a polygenic response to selection in the urban environment. These findings open stimulating perspectives for broader applications of high-resolution genomic tools on other cities and larger sample sizes to investigate the consistency of the effects of urbanization on the spatial distribution of genetic diversity and the polygenic nature of gene-urbanization association.

Fine-grained habitat-associated genetic connectivity in an admixed population of mussels in the small isolated Kerguelen Islands

“…Inverted genetic-environment associations are predicted by the coupling hypothesis (Bierne et al 2011), which proposes that genetic-environment associations can easily be revealed by intrinsically maintained genetic backgrounds in linkage disequilibrium with local adaptation genes, and that the phase of the disequilibrium can reverse when contacts are replicated as could have happened in Southern Hemisphere mussels. Overall, these findings reinforce the idea that genetic variation can be maintained at fine geographical scales in high-dispersal organisms, as recently shown in Chilean mussels (Araneda et al 2016) or in passerine birds (Szulkin et al 2016, Perrier et al 2017. In these examples however the link with a possible history of admixture has not been investigated.…”

Repeated genomic signatures of adaptation to urbanisation in a songbird across Europe

“…Boyce and Perrins 1987; Table S1). This is in line with previous studies of the species (Perrier et al 2018;Laine et al 2016;Lemoine et al 2016;Spurgin et al 2019). In addition, the levels of heterozygosity were similar between urban and rural populations, although slightly lower in some of the urban populations (see Table S1 for details; Wilcoxon test: W=30, P = 0.377).…”

“…The majority of available studies on the genetic bases of urban adaptation have either focused on a limited number of markers and genes (J. C. Mueller et al 2013) or focused on a narrow geographical scale (Harris and Munshi-South 2017;Campbell-Staton et al 2020;Perrier et al 2018). As a result, an important gap remains in the understanding of the prevalence of convergent evolution among cities (Rivkin et al 2019), limiting the inferences that can be made on the genomic response to urbanisation.…”

“…Nonetheless, whether this is the result of a genetic response to selection or phenotypic plasticity is to a large extent still unknown. Only a few studies have previously explored the genetic patterns underlying urban adaptation in birds, finding evidence of divergence in behaviour-related genes at multiple European populations using either a candidate gene approach (J. C. Mueller et al 2013) or a low-density SNP along transects within a city (Perrier et al 2018). Furthermore, similar pathways showed divergence across three neighboring urban areas in a recently established urban-dwelling avian species in South America (Jakob C. Mueller et al n.d.).…”

Little Adaptive Potential in a Threatened Passerine Bird

“…The nucleotide diversity (p) was estimated at 0.00095 (SE ± 4.64 3 10 À6 ) and was also lower in Tiritiri Matangi (0.00088, SE ± 4.35 3 10 À6 ) than in Te Hauturuo-Toi (0.00095, SE ± 1.40 3 10 À5 ). Both of these moleculardiversity metrics were lower than any comparable (i.e., ''sequence-based'') estimates for passerine birds that we have been able to identify in the literature (see Figure 1) [7][8][9][10][11]. Note that while the only threatened species (the Florida scrub-jay) included in our comparison has the lowest nucleotide diversity of the other species, the hihi still has a diversity 2.6 times lower.…”