Landscape and climatic variations of the Quaternary shaped multiple secondary contacts among barn owls (Tyto alba) of the Western Palearctic

Abstract

The combined actions of climatic variations and landscape barriers shape the history of natural populations. When organisms follow their shifting niches, obstacles in the landscape can lead to the splitting of populations, on which evolution will then act independently. When two such populations are reunited, secondary contact occurs in a broad range of admixture patterns, from narrow hybrid zones to the complete dissolution of lineages. A previous study suggested that barn owls colonized the Western Palearctic after the last glaciation in a ring-like fashion around the Mediterranean Sea, and conjectured an admixture zone in the Balkans. Here, we take advantage of whole-genome sequences of 94 individuals across the Western Palearctic to reveal the complex history of the species in the region using observational and modeling approaches. Even though our results confirm that two distinct lineages colonized the region, one in Europe and one in the Levant, they suggest that it predates the last glaciation and identify a narrow secondary contact zone between the two in Anatolia. Nonetheless, we also show that barn owls re-colonized Europe after the glaciation from two distinct glacial refugia: a western one in Iberia and an eastern one in Italy. Both glacial lineages now communicate via eastern Europe, in a wide and permeable contact zone. This complex history of populations enlightens the taxonomy of Tyto alba in the region, highlights the key role played by mountain ranges and large water bodies as barriers and illustrates the power of population genomics in uncovering intricate demographic patterns.

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

“…Overall, our results confirm that water bodies are strong barriers to barn owl movement (Cumer et al, 2021; Machado et al, 2021). For example, distant populations in the mainland, such as GR and IT, were much more similar to each other than any insular population, regardless of how distant each of them are (Figure 1).…”

“…In the broader context of the Western Palearctic, our study targets two islands in the region where the European and eastern lineages of barn owls meet (Cumer et al, 2021). This is clearly shown in the genomic PCA, where the mainland populations of Italy and Greece in southern Europe were opposed to that of Israel in the Levant, with insular populations placed along this west-to-east genetic gradient roughly according to their geographic position (Figure 1b, Sup Fig K=2).…”

“…A total of 67 barn owl individuals from seven populations were used in this study (Table 1; Supporting Table 1): 10 in Italy (IT), 5 in islands of the Ionian Sea (IO), 10 in Greece (GR), 11 in islands of the Aegean Sea (AE), 11 in Crete (CT), 10 in Cyprus (CY) and 10 in Israel (IS). Of these, 47 were sequenced in Cumer et al (2021; GenBank BioProject PRJNA727977; Sup. Table 1).…”

“…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.…”

“…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). Although Crete and Cyprus populations supposedly belong to T. a. erlangeri (Clements et al, 2019), the low resolution genetic data previously available was insufficient to clarify the history of each island and how they relate to the mainland.…”