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

PLoS Genet. 2024 Aug 22;20(8):e1011360. doi: 10.1371/journal.pgen.1011360. eCollection 2024 Aug.

Abstract

Secondary contact between closely related taxa represents a "moment of truth" for speciation-an opportunity to test the efficacy of reproductive isolation that evolved in allopatry and to 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 that are transitioning from autosomal to sex-specific inheritance. Here we report that, in the Solomon Islands, 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 after ~1.1 my of geographic isolation. Hybrids of the two species were first observed in sympatry ~100 years ago. To determine the genetic consequences of hybridization, we use population genomic analyses of individuals sampled in allopatry and in 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. For sympatric birds, autosomal introgression is bidirectional, with phenotypic hybrids and phenotypic parentals of both species showing admixed ancestry. In other regions of the genome, however, the story is different. While introgression on the Z/neo-Z-linked sequence is limited, introgression of W/neo-W regions and mitochondrial sequence (mtDNA) is highly asymmetric, moving only from the invading M. cardinalis to the resident M. tristrami. The recent hybridization between these species has thus enabled gene flow in some genomic regions but the interaction of admixture, asymmetric mate choice, and/or natural selection has led to the variation in the amount and direction of gene flow at sex-linked regions of the genome.

MeSH terms

  • Animals
  • Birds / genetics
  • Female
  • Gene Flow*
  • Genetic Introgression*
  • Genetic Speciation
  • Genetics, Population
  • Genome / genetics
  • Hybridization, Genetic*
  • Male
  • Melanesia
  • Reproductive Isolation*
  • Sex Chromosomes* / genetics
  • Sympatry

Grants and funding

Fieldwork was funded by the Aresty Chair in Tropical Ecology and an NSF CAREER award (IOS 1137624/0643606) to JACU, and awards from the Society of Systematic Biologists, Kushlan Graduate Research Support Fund, and Jay M. Savage Graduate Research Support Fund to JMS. Additional support was provided by NSF-PRFB to EHS (2010748), and NSF-DEB 2112474 to JACU and DCP. The NSF-PRFB 2010748 funded salary for EHS and the NSF-DEB 2112474 funded salary for CAM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.