Reconciling Gene Tree Discordance and Biogeography in European Crows

Reconstructing the evolutionary history of young lineages diverging with gene flow is challenging due to factors like incomplete lineage sorting, introgression, and selection causing gene tree discordance. The European crow hybrid zone between all-black carrion crows and grey-coated hooded crows exemplifies this challenge. Most of the genome in Western and Central European carrion crow populations is near-identical to hooded crows, but differs substantially from their Iberian congeners. A notable exception is a single major-effect colour-locus under sexual selection aligning with the ‘species’ tree. To understand the underlying evolutionary processes, we reconstructed the biogeographic history of the species complex. During the Pleistocene carrion and hooded crows took refuge in the Iberian Peninsula and the Middle East, respectively. Allele-sharing of all-black Western European populations with likewise black Iberian crows at the colour-locus represents the last trace of carrion crow ancestry, resisting gene flow from expanding hooded crow populations that have homogenised most of the genome. A model of colour-locus introgression from an Iberian ancestor into hooded crow populations near the Pyrenées was significantly less supported. We found no positive relationship between introgression and recombination rate consistent with the absence of genome-wide, polygenic barriers in this young species complex. Overall, this study portrays a scenario where few large-effect loci, subject to divergent sexual selection, resist rampant and asymmetric gene exchange. This study underscores the importance of integrating population demography and biogeography to accurately interpret patterns of gene tree discordance following population divergence.