Recent secondary contact, genome-wide admixture, and limited introgression of neo-sex chromosomes between two Pacific island bird species

Secondary contact between closely related taxa represents a “moment of truth” for speciation. Removal of geographic barriers allows us to test the strength of reproductive isolation that evolved in allopatry and identify the genetic, behavioral, and/or ecological barriers that separate species in sympatry. Sex chromosomes are known to rapidly accumulate differences between species, an effect that may be exacerbated for neo-sex chromosomes because they are regions of the genome that have recently become linked to sex chromosomes and are transitioning from autosomal to sex-specific inheritance. Two closely related bird species in the honeyeater family — Myzomela cardinalis and Myzomela tristrami — carry neo-sex chromosomes and have come into recent secondary contact in the Solomon Islands after being isolated for ∼3 my. Hybrids of these two species have been observed in sympatry for at least 100 years. To determine the genetic consequences of hybridization, we use population genomic analyses of individuals sampled in allopatry and sympatry to characterize gene flow in the contact zone. Using genome-wide estimates of diversity, differentiation, and divergence, we find that the degree and direction of introgression varies dramatically across the genome. Autosomal introgression is bidirectional, with phenotypic hybrids and phenotypic parentals of both species showing admixed ancestry. On the sex and neo-sex chromosomes, the story is different. Introgression of Z is limited and neo-Z sequence shows no evidence of introgression, whereas introgression of W and neo-W is strong but highly asymmetric, moving only from the invasive M. cardinalis to the resident M. tristrami. Thus, reproductive isolation is incomplete, but sex and neo-sex chromosome regions have prevented gene flow in one (W/neo-W) or both (Z/neo-Z) directions. The recent contact between previously isolated species indicates that hybridization may permit gene flow between taxa in some genomic regions, but species divergence can be maintained by barriers to gene flow associated with rapidly evolving sex-linked regions of the genome. Author Summary When a new species colonizes an island and interacts with a closely related native species, we are provided with a rare opportunity to identify the factors that keep species distinct and the consequences of interbreeding. Regions of the genome that evolve rapidly or influence mate choice may be especially likely to act as barriers to gene flow. The red Myzomela cardinalis, birds in the honeyeater family, have recently arrived to Makira in the Solomon Islands, joining the endemic, all black Myzomela tristrami. We used population genomic analyses of individuals in geographic isolation, as well as those in geographic contact with the other species, to understand the history of these two species and the consequences of their recent range overlap on Makira. We found that regions of the genome that are sex-specific (i.e., sex chromosomes) were either limited in their ability to move between species, or only moved in one direction, from the invading M. cardinalis to the native M. tristrami. This work highlights how certain regions of the genome may be especially important in defining species boundaries and the generation and maintenance of biodiversity.