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

Abstract

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.