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

Abstract

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.

CYP2J19 mediates carotenoid colour introgression across a natural avian hybrid zone

“…TA B L E 2 Admixed individuals, their autosomal hybrid index, Z chromosome hybrid index, interspecific heterozygosity, mtDNA haplotype (from Nwankwo et al, 2019), and sex; the banner shows photos of forecrown for each individual except AR93119 and AR93162 [Colour The metabolic pathway for α-doradexanthin involves C 4 we find in tinkerbirds (C=C band peak at 1,524 cm −1 , compared with 1,527-1,528 cm −1 for yellow forecrown in tinkerbirds). However, C. auratus has a high proportion of the carotenoids β-carotene and zeaxanthin present in its feathers (Hudon et al, 2015), represented by increased effective conjugation lengths, in addition to lutein .…”

“…Baldassarre et al, 2014). The pusillus mitochondrial haplotype is less than one third as common as extoni in the contact zone (14/49 individuals, see Nwankwo et al (2019), supporting information). Yet female pusillus appear to put the extra effort into finding pusillus haplotype males, outnumbered by their extoni haplotype counterparts.…”

“…Pogoniulus tinkerbirds are African barbets (Lybiidae) that although omnivorous, feed primarily on fruit, especially mistletoe (Dowsett-Lemaire, 1988;Godschalk, 1985). Species in the genus differ subtly in plumage characters despite millions of years of divergence in mtDNA between currently recognized sister species (Kirschel et al, 2009(Kirschel et al, , 2018Nwankwo et al, 2018Nwankwo et al, , 2019. Pogoniulus pusillus pusillus (hereafter pusillus) and P. chrysoconus extoni (Layard, 1871) (hereafter extoni) are the subspecies of red-fronted and yellow-fronted tinkerbird, respectively, that meet at a contact zone in southern Africa (Monadjem et al, 1994).…”

“…Methods used to obtain reflectance spectra from forecrown feathers using a spectrophotometer have been described in detail (Nwankwo et al, 2019). In brief, we used a JAZ spectrometer (Ocean Optics) with a fibre-optic reflectance probe (Ocean Optics R-200) and PX…”

“…Indeed, there are potentially other pathways, with a number of examples of species with red or orange feather colour produced without the presence of ketocarotenoids (Andersson et al, 2007;Brush, 1970;. Red-fronted (Pogoniulus pusillus, Dumont, 1816) and yellow-fronted (P. chrysoconus, Temminck, 1832) tinkerbirds provide such an opportunity to investigate the genes involved in carotenoid processing because they hybridize extensively at a contact zone in southern Africa (Nwankwo et al, 2019). They differ phenotypically most noticeably in their forecrown coloration; hence their vernacular names (Figure 1).…”