Rampant introgressive hybridization in Pogoniulus tinkerbirds (Piciformes: Lybiidae) despite millions of years of divergence

Incomplete reproductive isolation between related species of birds at contact zones is increasingly being documented. Such hybridization typically occurs between sister taxa that diverged in relatively recent times, and hybrids are most often identified based on their intermediate phenotypic characteristics and, increasingly, through genetic admixture analysis. When species have been diverging over relatively longer time scales, prezygotic isolation barriers are expected to evolve, precluding maladaptive interbreeding. Here, we examine the extent of introgressive hybridization in a pair of African barbets, the yellow-fronted tinkerbird (Pogoniulus chrysoconus extoni) and the red-fronted tinkerbird (Pogoniulus pusillus pusillus), which were not previously known to interbreed, across a contact zone in Southern Africa. Although there were significant differences in the coloration of plumage between the species, we found a pattern of extensive admixture in and around the contact zone. Nonetheless, the two species appear to have diverged > 4 Mya and might not even be sister taxa, suggesting that time of divergence alone might not be sufficient for the evolution of prezygotic reproductive barriers. Significantly more phenotypically red-fronted individuals had a P. c. extoni (yellow-fronted) genetic background than vice versa, suggesting possible asymmetry in mate preferences. Sexual selection may thus play a role in breaking down species barriers despite the extent of genetic divergence.A Marie Curie International Reintegration Grant (A.N.G.K.) and the A. P. Leventis Ornithological Research Institute (E.C.N. and B.O.O.).https://academic.oup.com/biolinnean2020-04-03hj2019Mammal Research Institut

CYP2J19 mediates carotenoid colour introgression across a natural avian hybrid zone

It has long been of interest to identify the phenotypic traits that mediate reproductive isolation between related species, and more recently, the genes that underpin them. Much work has focused on identifying genes associated with animal colour, with the candidate gene CYP2J19 identified in laboratory studies as the ketolase converting yellow dietary carotenoids to red ketocarotenoids in birds with red pigments. However, evidence that CYP2J19 explains variation between red and yellow feather coloration in wild populations of birds is lacking. Hybrid zones provide the opportunity to identify genes associated with specific traits. Here we investigate genomic regions associated with colour in red‐fronted and yellow‐fronted tinkerbirds across a hybrid zone in southern Africa. We sampled 85 individuals, measuring spectral reflectance of forecrown feathers and scoring colours from photographs, while testing for carotenoid presence with Raman spectroscopy. We performed a genome‐wide association study to identify associations with carotenoid‐based coloration, using double‐digest RAD sequencing aligned to a short‐read whole genome of a Pogoniulus tinkerbird. Admixture mapping using 104,933 single nucleotide polymorphisms (SNPs) identified a region of chromosome 8 that includes CYP2J19 as the only locus with more than two SNPs significantly associated with both crown hue and crown score, while Raman spectra provided evidence of ketocarotenoids in red feathers. Asymmetric backcrossing in the hybrid zone suggests that yellow‐fronted females mate more often with red‐fronted males than vice versa. Female red‐fronted tinkerbirds mating assortatively with red‐crowned males is consistent with the hypothesis that converted carotenoids are an honest signal of quality.DATA AVAILABILITY STATEMENT : The Pogoniulus pusillus genome assembly has been deposited at NCBI SRA in BioProject PRJNA630018, with DDRAD sequencing reads under BioProject PRJNA666541. The master VCF file and gemma and R Code have been deposited in the Dryad Digital Repository (https://doi-org.uplib.idm.oclc.org/10.5061/dryad.jm63xsj87).FP7 Marie Curie Reintegration Grant, a University of Cyprus Research Grant, an AG Leventis Foundation grant and by the AP Leventis Ornithological Research Institute, Jos, Nigeria.http://wileyonlinelibrary.com/journal/mec2021-10-15hj2021Mammal Research InstituteZoology and Entomolog