"Isolation by Gentes with Asymmetric Migration" shapes the genetic structure of the common cuckoo in China.

Abstract

Amid coevolutionary arms races between brood parasitic birds and their diverse host species, the formation of host-specific races, or gentes, has drawn significant research focus. Nevertheless, numerous questions about gentes evolutionary patterns persist. Here, we investigated the potential for gentes evolution across multiple common cuckoo (Cuculus canorus) populations parasitizing diverse host species in China. Using maternal (mitochondrial and W-linked DNA) and biparental (autosomal and Z-linked DNA) markers, we found consistent clustering of cuckoo gentes (rather than geographical populations) into distinct clades in matrilineal gene trees, indicating robust differentiation. In contrast, biparental markers indicated intermixing of all gentes, suggesting asymmetric gene flow regardless of geography. Unlike the mitonuclear discordance commonly resulting from incomplete lineage sorting, adaptive introgression, or demographic disparities, the observed pattern in brood parasitic cuckoos might reflect biased host preferences between sexes. We hereby present the "Isolation by Gentes with Asymmetric Migration" model. According to this model, the maternal line differentiation of the common cuckoo in China is potentially driven by host preferences in females, whereas males maintained the integrity of the cuckoo species through random mating. To achieve this, cuckoo males could perform flexible migration among gentes or engage in early copulation with females before reaching the breeding sites, allowing female cuckoos to store sperm from various gentes. Future studies collecting additional samples from diverse cuckoo gentes with overlapping distribution and investigating the migratory and copulation patterns of each sex would enhance our understanding of sex-biased differentiation among cuckoo populations in China.