Replicate avian hybrid zones reveal the progression of genetic and trait introgression through time

Abstract

Replicate hybrid zones between the same taxa provide a unique opportunity to assess the repeatability of the outcome of interspecific matings by uncovering recurrent genomic and phenotypic introgression patterns. Replicates also facilitate exploration of the causes of temporal shifts in hybrid zone structure. We sampled transects along three geographically separate hybrid zones between two avian taxa -the Lemon-rumped (Ramphocelus flammigerus icteronotus) and Flame-rumped (R. f. flammigerus) Tanagers-which hybridize in low passes across the Western Andes of Colombia. We examined environmental, phenotypic and genetic variation using reflectance spectrophotometry and genotype-by-sequencing data mapped to a high-quality de novo genome assembly, aiming to assess the repeatability and progression of introgression after hybridization. We found that all hybrid zones formed independently, showed parallel phenotypic divergence along ecological gradients, low population structure across parental ranges and similar demographic histories. Replicates also exhibited asymmetric introgression of neutral markers from the yellow icteronotus into the hybrid zone. However, the age of the hybrid zones differed, resulting in differences in the extent of geographic and genomic cline displacement from environmental transitions into the red flammigerus range. Despite heterogeneity in locus-specific introgression, the only shared introgression outliers across all hybrid zones were in a genomic region linked to plumage color. Clines for these loci were consistently narrow, suggesting a role in long-term reproductive isolation. Altogether, we showed that locus-specific introgression is largely stochastic, but the magnitude and directionality of neutral introgression can be predictable when demographic conditions are similar and for traits involved in reproductive isolation.