Unexpected post-glacial colonisation route explains the white colour of barn owls (Tyto alba) from the British Isles

Abstract

The climate fluctuations of the Quaternary shaped the movement of species in and out of glacial refugia. In Europe, the majority of species followed one of the described traditional postglacial recolonization routes from the southern peninsulas towards the north. Like most organisms, barn owls are assumed to have colonized the British Isles by crossing over Doggerland, a land bridge that connected Britain to northern Europe. However, while they are dark rufous in northern Europe, barn owls in the British Isles are conspicuously white, a contrast that could suggest selective forces are at play on the islands. However, analysis of known candidate genes involved in colouration found no signature of selection. Instead, using whole genome sequences and species distribution modelling, we found that owls colonised the British Isles soon after the last glaciation, directly from a white coloured refugium in the Iberian Peninsula, before colonising northern Europe. They would have followed a yet unknown post-glacial colonization route to the Isles over a westwards path of suitable habitat in now submerged land in the Bay of Biscay, thus not crossing Doggerland. As such, they inherited the white colour of their Iberian founders and maintained it through low gene flow with the mainland that prevents the import of rufous alleles. Thus, we contend that neutral processes likely explain this contrasting white colour compared to continental owls. With the barn owl being a top predator, we expect future research will show this unanticipated route was used by other species from its paleo community.

Genomic consequences of colonisation, migration and genetic drift in barn owl insular populations of the eastern Mediterranean

“…One additional individual of the Eastern barn-owl species ( T. javanica from Singapore; Uva et al, 2018) was used as an outgroup for specific analyses. The outgroup was sequenced in Machado et al, (2021; GenBank BioProject PRJNA700797). The remaining 20 samples followed the same protocol described in (Cumer et al, 2021; Machado et al, 2021).…”

“…The outgroup was sequenced in Machado et al, (2021; GenBank BioProject PRJNA700797). The remaining 20 samples followed the same protocol described in (Cumer et al, 2021; Machado et al, 2021). In brief, we extracted genomic DNA using the DNeasy Blood & Tissue kit (Qiagen, Hilden, Germany) and prepared individually tagged 100bp “TruSeq DNA PCR-free” libraries (Illumina) following the manufacturer’s instructions.…”

“…The bioinformatics pipeline used to obtain analysis-ready SNPs from the raw sequenced of the 65 individuals plus the outgroup was the same as in (Machado et al, 2021) adapted from the Genome Analysis Toolkit (GATK) Best Practices (Van der Auwera et al 2013) to a non-model organism following the developers’ recommendations. Briefly, we trimmed the reads to 70bp length with Trimommatic v.0.36 (Bolger et al 2014) and aligned them with BWA-MEM v.0.7.15 (Li and Durbin 2009) to the barn owl reference genome (GenBank accession JAEUGV000000000; Machado et al, 2021). Then, we performed base quality score recalibration (BQSR) following the iterative approach recommended for non-model species that lack a set of “true variants” in GATK v.4.1.3 using high-confidence calls obtained from two independent callers: GATK’s HaplotypeCaller and GenotypeGVCF v.4.1.3 and ANGSD v.0.921 (Korneliussen et al 2014).…”

“…The Afro-European barn owl ( Tyto alba ) is a non-migratory bird of prey present across the African and European continents, as well as most of the surrounding islands and archipelagos (Uva, Päckert, Cibois, Fumagalli, & Roulin, 2018). In spite of being quite widespread and maintaining high gene flow overland (Antoniazza, Burri, Fumagalli, Goudet, & Roulin, 2010; Machado, Clément, Uva, Goudet, & Roulin, 2018), populations separated by water barriers appear to accumulate differentiation more quickly, with numerous insular subspecies (Burri et al, 2016; Machado et al, 2021; Uva et al, 2018). In the eastern Mediterranean, the continental European barn owl lineage meets the eastern subspecies T. a. erlangeri (W. L. Sclater, 1921) from the Levant (Burri et al, 2016; Cumer et al, 2021).…”

“…However, being closer to other Greek islands and the Greek mainland, Crete could have actually been colonised from there, which would be incompatible with it belonging to the same subspecies as Cyprus. Taking advantage of the whole genome sequences of 65 individuals and the recent publication of a high-quality reference genome (Machado et al, 2021), we address this by modelling the colonisation of both islands from the mainland. Lastly, we compare how their different demographic histories impacted their current genetic diversity and inbreeding levels.…”