Hybrid zone or hybrid lineage: a genomic reevaluation of Sibley's classic species conundrum in Pipilo towhees

Hybrid zones can be studied by modeling clines of trait variation (e.g., morphology, genetics) over a linear transect. Yet, hybrid zones can also be spatially complex, can shift over time, and can even lead to the formation of hybrid lineages with the right combination of dispersal and vicariance. We reassessed gradient between Collared Towhee (Pipilo ocai) and Spotted Towhee (Pipilo maculatus) in Central Mexico to test whether it conformed to a typical tension-zone cline model. By comparing historical and modern data, we found that cline centers for genetic and phenotypic traits have not shifted over the course of 70 years. This equilibrium suggests that secondary contact between these species, which originally diverged over 2 million years ago, likely dates to the Pleistocene. Given the amount of mtDNA divergence, parental ends of the cline have very low autosomal nuclear differentiation (F-ST = 0.12). Dramatic and coincident cline shifts in mtDNA and throat color suggest the possibility of sexual selection as a factor in differential introgression, while a contrasting cline shift in green back color hints at a role for natural selection. Supporting the idea of a continuum between clinal variation and hybrid lineage formation, the towhee gradient can be analyzed as one population under isolation-by-distance, as a two-population cline, and as three lineages experiencing divergence with gene flow. In the middle of the gradient, a hybrid lineage has become partly isolated, likely due to forested habitat shrinking and fragmenting as it moved upslope after the last glacial maximum and a stark environmental transition. This towhee system offers a window into the potential outcomes of hybridization across a dynamic landscape including the creation of novel genomic and phenotypic combinations and incipient hybrid lineages.

Automated summary

The study reassessed the gradient between Collared Towhee and Spotted Towhee in Central Mexico and found that the genetic and phenotypic traits of the cline centers have not shifted over 70 years, indicating the secondary contact between these species likely dates to the Pleistocene. The towhee system offers insights into the potential outcomes of hybridization across a dynamic landscape, including the formation of incipient hybrid lineages and novel genomic and phenotypic combinations.