The great tit HapMap project: a continental-scale analysis of genomic variation in a songbird

Abstract

85A major aim of evolutionary biology is to understand why patterns of genomic variation vary among 86 populations and species. Large-scale genomic studies of widespread species are useful for studying how 87 the environment and demographic history shape patterns of genomic divergence, and with the continually 88 decreasing cost of sequencing, such studies are now becoming feasible. Here, we carry out one of the most 89 comprehensive surveys of genomic variation in a wild vertebrate to date; the great tit (Parus major) HapMap 90 project. We screened ca 500,000 SNP markers across 647 individuals from 29 populations, spanning almost 91 the entire geographic range of the European great tit subspecies. We found that genome-wide variation was 92 consistent with a recent colonisation across Europe from a single refugium in the Balkans and/or Turkey, with 93 bottlenecks and reduced genetic diversity in island populations. Differentiation across the genome was highly 94 heterogeneous, with clear "islands of differentiation" even among populations which are ostensibly panmictic. 95These islands of differentiation were consistently found in regions of low recombination, suggesting that 96 background selection can rapidly promote population differentiation among even the most recently colonised 97 populations. We also detected genomic outlier regions that were unique to peripheral great tit populations, 98 most likely as a result of recent directional selection at the range edges of this species. These "unique" 99 outlier regions contained candidate genes for morphology, thermal adaptation and colouration, supporting 100 previous research in this species, and providing avenues for future investigation. Our study suggests that 101 comprehensive screens of genomic variation in wild organisms can provide unique insights into evolution. 102Author summary 103 Studying patterns of genetic variation is a useful way of determining why populations and species differ in 104 nature. Genetic variation is shaped by natural selection, but also by the present and past size of populations, 105 the amount of migration, and by features of the genome, such as variation in recombination rate, of the 106 organism being studied. Teasing apart the effects of these different processes on genomic diversity is difficult, 107 but one way that this can be achieved is by studying genomic variation across the entire range of a species. 108 We performed a continental-scale analysis of genetic variation in the great tit -a widespread songbird that 109 has been the focus of extensive ecological research. We first used genomic data to reconstruct the historical 110 colonisation of great tits across Europe, and showed that during the last ice age, this species was likely 111 restricted to a single region in Eastern Europe, from which they spread across the continent. We then 112 studied how patterns of variation differ along the genome, and show that recombination rate is a key driver 113 of variation among all populations. Importantly, by comparing ma...

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).…”

Demographic history and genomics of local adaptation in blue tit populations

“…F ST was also in average higher in these regions. These patterns of increased divergence in regions with low recombination are commonly observed (Nachman & Payseur 2011; Cruickshank & Hahn 2014; Gagnaire et al 2018), including in other bird species (Burri et al 2015; Spurgin et al 2019). It is well documented that such increased differentiation in regions with low recombination is not necessarily due to positive selection, or at least not alone, and that it is largely influenced by the effect of recombination in interaction with background selection (Charlesworth et al 1993; Burri et al 2015; Perrier & Charmantier 2019).…”

Response to Perrier and Charmantier: On the importance of time scales when studying adaptive evolution

“…() we compared the breeding values of the United Kingdom and the Netherlands populations. As part of an ongoing effort to characterize genetic variation across the species’ distribution (the Great Tit HapMap Project; (Spurgin et al., ) we have genotyped birds from >20 European populations with the same SNP chip (Kim et al. ) as the one used in Bosse et al.…”

“…Genomic data from populations outside of the United Kingdom and the Netherlands are described elsewhere (Spurgin et al. ).…”

“…S7 of Bosse et al (2017) we compared the breeding values of the United Kingdom and the Netherlands populations. As part of an ongoing effort to characterize genetic variation across the species' distribution (the Great Tit HapMap Project; (Spurgin et al, 2019) we have genotyped birds from >20 European populations with the same SNP chip (Kim et al 2018) as the one used in Bosse et al (2017). Based on those data, here we ask whether the loci identified as being under selection in the United Kingdom could cause UK populations to have longer bills than mainland European populations.…”