Genomic basis of insularity and ecological divergence in barn owls (Tyto alba) of the Canary Islands

Abstract

Islands, and the particular organisms that populate them, have long fascinated biologists. Due to their isolation, islands offer unique opportunities to study the effect of neutral and adaptive mechanisms in determining genomic and phenotypical divergence. In the Canary Islands, an archipelago rich in endemics, the barn owl (Tyto alba), present in all the islands, is thought to have diverged into a subspecies (T. a. gracilirostris) on the eastern ones, Fuerteventura and Lanzarote. Taking advantage of 40 whole-genomes and modern population genomics tools, we provide the first look at the origin and genetic makeup of barn owls of this archipelago. We show that the Canaries hold diverse, long-standing and monophyletic populations with a neat distinction of gene pools from the different islands. Using a new method, less sensitive to structure than classical F_ST, to detect regions involved in local adaptation to insular environments, we identified a haplotype-like region likely under selection in all Canaries individuals and genes in this region suggest morphological adaptations to insularity. In the eastern islands, where the subspecies is present, genomic traces of selection pinpoint signs of adapted body proportions and blood pressure, consistent with the smaller size of this population living in a hot arid climate. In turn, genomic regions under selection in the western barn owls from Tenerife showed an enrichment in genes linked to hypoxia, a potential response to inhabiting a small island with a marked altitudinal gradient. Our results illustrate the interplay of neutral and adaptive forces in shaping divergence and early onset speciation.

Fig. 1. Population structure of barn owls from the Mediterranean Basin and the Canary Islands.

a Individual admixture proportion of each of K = 4 lineages as determined by sNMF. Black dots are located at the approximate centroid of each sampled population. Dashed lines encircle the island(s) sampled for each Canary population. The current distribution of barn owls is plotted atop the map in blue (data from IUCN: BirdLife International 2019). b PCA of the 40 individuals. Principal component (axes) one and two (left panel) and one and three (right panel) are shown, values in parenthesis indicate the percentage of variance explained by each axis. Point shape and colour denote populations according to the legend.

Fig. 2. Genomic landscape of differentiation between insular and mainland barn owls.

a Genome-wide beta comparison between individuals from the Canary Islands (EC & WC) and from the mainland (PT & IS). Each dot represents a 100 kbp window. Dashed line indicates the 5 SD threshold used to identify genomic regions of high differentiation, emphasised in red. Alternating grey colours denote different scaffolds. Shaded vertical bar highlights Scaffold 100006. b Zoom on Scaffold 100006 and, in particular, the ~15 Mb long highly differentiated genomic region (background shading) over windows of 100 kbp. From top to bottom, we see in this region a high F_ST^Can between insular and mainland barn owls, low absolute distance (d_XY) between both islands (scaled with mean = 0) and reduction of nucleotide diversity (π) among insular individuals (red line) compared to the mainland (black line). The bottom triangular matrix shows pairwise LD (r²) between groups of 100 SNP along the chromosome in insular owls. Darker pixels show higher LD. Grey triangles match each pixel in the matrix diagonal to the region it spans on the chromosome above. Red triangles indicate pixels that overlap the region of high differentiation.

Fig. 3. Ecological divergence in barn owls from the Canary Islands.

a Sampling location of Western (WC; yellow) and Eastern (EC; red) Canary individuals, off the coast of north-western Africa. Sampled islands are named. Large dots indicate individuals sampled for WGS and population genomics analyses; small transparent dots are barn owl observations used in niche analysis. Dashed lines group islands according to barn owl taxonomy. b Climatic niche occupied by the two Canary populations. The first axis varies from cold and wet to hot arid environments. c Genome-wide F_ST comparison between individuals from each Canary population. Each dot represents a 100kbp window. Alternating grey colours denote different chromosomes. Dashed line indicates the 5 SD F_ST threshold used to identify genomic regions of high differentiation overlaid with F_ST^WC, highlighted in yellow and F_ST^EC in red. Arrows denote the location of genes linked with response to hypoxia in WC; and the cluster of four genes linked to morphological ratios and the main gene related to blood pressure in EC. d Same F_ST windows and threshold as in c plotted against the difference between F_ST^WC and F_ST^EC, clearly highlight the two sets of windows putatively under local adaptation.