Hybrid cline or hybrid lineage: A genomic reevaluation of Sibley’s classic species conundrum in Pipilo towhees

Hybrid zones are often described as clines of genetic and phenotypic
traits moving across species barriers through introgression. Yet, hybrid
zones can also be spatially complex and shift over time, and dispersal and
vicariance can isolate portions of a cline, potentially leading to hybrid
lineage formation. We reassessed Sibley’s (1950) gradient between Collared
Towhee (Pipilo ocai) and Spotted Towhee (P. 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 (FST = 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 hybrid
clines 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 both to forested habitat shrinking and fragmenting as it moved
upslope after the last glacial maximum and a stark environmental
transition. The 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.