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 FST, 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.

Island volcanism predicts pheomelanin‐based plumage colouration in a cosmopolitan raptor

“…taxa (Losos & Ricklefs, 2009), including the studied one (Cumer et al, 2022;Machado et al, 2022). In addition, the absence of relationships with temperature and rainfall is not surprising also because departures from ecogeographical rules strongly depend on the spatial scale considered.…”

Where and when local adaptation happens: lessons from the European barn owl (Tyto alba)

“…Whole genome sequences were retrieved from the Sequence Read Archive (SRA -Bioprojects PRJNA700797, PRJNA727915 and PRJNA727977, Table S1). To avoid spurious effects caused by strong genetic divergence, we focused on the mainland populations and discarded lineages from Cyprus ( Machado, Topaloudis, et al 2021) and the Canary Islands ( (Cumer, Machado, Siverio, et al 2022).…”

“…This approach allowed us to identify genomic regions with an excess of genetic identity within a population, compared to the genetic identity observed with other populations. Compared with the remainder of the genome, this approach allows for identifying regions of the genome with specific history (i.e., selection event), an approach first implemented by (Cumer, Machado, Siverio, et al 2022). However, even if the use of genome scans to detect traces of selection is common in the literature, it presents some major caveats.…”

“…The Western Palearctic barn owl ( Tyto alba ), a nonmigratory raptor, recolonised Northern Europe at the end of the LGM from two main glacial refugia located in the Iberian Peninsula and the Italian / Greek Peninsulas (Cumer, Machado, Dumont, et al 2022). Nowadays, its range stretches from the Southwest to the Northeast of Europe (Cumer, Machado, Dumont, et al 2022).…”

“…The Western Palearctic barn owl ( Tyto alba ), a nonmigratory raptor, recolonised Northern Europe at the end of the LGM from two main glacial refugia located in the Iberian Peninsula and the Italian / Greek Peninsulas (Cumer, Machado, Dumont, et al 2022). Nowadays, its range stretches from the Southwest to the Northeast of Europe (Cumer, Machado, Dumont, et al 2022). Studies investigating the genetic structure across its range showed that populations of this species are weakly genetically differentiated (Antoniazza et al 2010; Burri et al 2016; Cumer, Machado, Dumont, et al 2022).…”