Population genomics of an emergent tri‐species hybrid zone

Abstract

Isolating barriers that drive speciation are commonly studied in the context of twospecies hybrid zones. There is, however, evidence that more complex introgressive relationships are common in nature. Here, we use field observations and genomic analysis, including the sequencing and assembly of a novel reference genome, to study an emergent hybrid zone involving two colliding hybrid zones of three woodpecker species: red-breasted, red-naped, and yellow-bellied sapsuckers (Sphyrapicus ruber, S. nuchalis, and S. varius). Surveys of the area surrounding Prince George, British Columbia, Canada, show that all three species are sympatric, and Genotyping-by-Sequencing identifies hybrids from each species pair and birds with ancestry from all three species. Observations of phenotypes and genotypes of mated pairs provide evidence for assortative mating, though there is some heterospecific pairing.Hybridization is more extensive in this tri-species hybrid zone than in two di-species hybrid zones. However, there is no evidence of a hybrid swarm and admixture is constrained to contact zones, so we classify this region as a tension zone and invoke selection against hybrids as a likely mechanism maintaining species boundaries. Analysis of sapsucker age classes does not show disadvantages in hybrid survival to adulthood, so we speculate the selection upholding the tension zone may involve hybrid fecundity. Gene flow among all sapsuckers in di-species hybrid zones suggests introgression probably occurred before the formation of this tri-species hybrid zone, and might result from bridge hybridization, vagrancies, or other three-species interactions.

Semipermeable species boundaries create opportunities for gene flow and adaptive potential

“…Our findings are among the few that pertain to a mosaic hybrid zone involving multiple species. We add a new system to the groups of taxa exhibiting natural mosaic hybrid zones (Abbott & Brennan, 2014; Fraïsse et al, 2014; Rieseberg et al, 1999) and multispecies hybridisation (Banerjee et al, 2022; Grant & Grant, 2020; Heliconius Genome Consortium, 2012; Natola et al, 2022; Ottenburghs, 2019; Reutimann et al, 2020).…”

“…Hybridisation is commonly investigated between two species. However, genomic data have facilitated the detection of multispecies hybridisation in many taxa, including white oaks (Reutimann et al, 2020), birds (Grant & Grant, 2020; Natola et al, 2022; Ottenburghs, 2019), fish (Banerjee et al, 2022), and butterflies (Heliconius Genome Consortium, 2012). Multispecies hybridisation is likely to be more frequent in sympatric groups with a low degree of reproductive isolation, and one species may act as a ‘conduit’ of gene flow between two otherwise isolated species (Grant & Grant, 2020).…”

Evidence for ancient selective sweeps followed by differentiation among three species ofSphyrapicussapsuckers

“…Seventy-eight sapsucker samples were included in our WGS analysis: 10 allopatric individuals from each species, 15 hybrid zone individuals from each species cross, one putative 3-species hybrid, and two Williamson’s Sapsuckers ( Sphyrapicus thyroideus ) included as outgroups (Figure 1). We selected hybrid zone individuals to represent a continuum of admixture proportions between each species pair based on ancestry coefficient values from prior GBS research (L. Natola et al 2021, 2022, Seneviratne et al 2016). Samples were tissues from vouchered museum specimens and blood from wild-caught birds collected by Sampath Seneviratne (Seneviratne et al 2012, 2016) and included both male and female birds (Appendix C.1).…”

“…Molecular dating based on mitochondrial DNA estimates that red-breasted and red-naped sapsuckers diverged 0.32 million years ago (MYA), and their common ancestor diverged from yellow-bellied sapsuckers approximately 1.09 MYA (Weir & Schluter 2004), time frames over which there have been many cycles of glacial and interglacial periods (Menounos et al 2009). These three species hybridize where they come into contact, even forming a three-species hybrid zone (Natola et al 2022), but the limited number of hybrids in that zone show that the three forms are stable species. Given the evidence of some current gene flow (Natola et al 2022) as well as the deep genomic differentiation, it is a safe assumption that these three groups have experienced multiple cycles of geographic separation and hybridization during their path towards full species.…”

“…These three species hybridize where they come into contact, even forming a three-species hybrid zone (Natola et al 2022), but the limited number of hybrids in that zone show that the three forms are stable species. Given the evidence of some current gene flow (Natola et al 2022) as well as the deep genomic differentiation, it is a safe assumption that these three groups have experienced multiple cycles of geographic separation and hybridization during their path towards full species. Hence these sapsuckers provide an opportunity to examine the differentiation between three forms with a history of cycles of separation and contact.…”