Geographic contact drives increased reproductive isolation in two cryptic Empidonax flycatchers.

Geographic contact between sister lineages often occurs near the final stages of speciation, but its role in speciation's completion remains debated. Reproductive isolation may be essentially complete prior to secondary contact. Alternatively, costly interactions between partially reproductively isolated species - such as maladaptive hybridization or competition for resources - may select for divergence, increasing reproductive isolation and driving speciation toward completion. Here, we use coalescent demographic modelling and whole-genome data sets to show that a period of contact and elevated hybridization between sympatric eastern North American populations of two cryptic bird species preceded a major increase in reproductive isolation between these populations within the last 10,000 years. In contrast, substantial introgression continues to the present in a western contact zone where geographic overlap is much narrower and probably of more recent origin. In the sympatric eastern region where reproductive isolation has increased, it is not accompanied by character displacement in key morphometric traits, plumage coloration, or ecological traits. While the precise trait and underlying mechanism driving increased reproductive isolation remains unknown, we discuss several possibilities and outline avenues for future research. Overall, our results highlight how demographic models can reveal the geographic context in which reproductive isolation was completed, and demonstrate how contact can accelerate the final stages of speciation.

Cytonuclear discordance in the crowned-sparrows, Zonotrichia atricapilla and Zonotrichia leucophrys.

The golden-crowned (Zonotrichia atricapilla) and white-crowned (Z. leucophrys) sparrows have been presented as a compelling case for rapid speciation. They display divergence in song and plumage with overlap in their breeding ranges implying reproductive isolation, but have almost identical mitochondrial genomes. Previous research proposed hybridization and subsequent mitochondrial introgression as an alternate explanation, but lacked robust nuclear gene trees to distinguish between introgression and incomplete lineage sorting. We test for signatures of these processes between Z. atricapilla and Z. leucophrys, and investigate the relationships among Z. leucophrys subspecies, using mitochondrial sequencing and a reduced representation nuclear genomic dataset. Contrary to the paraphyly evident in mitochondrial gene trees, we confirmed the reciprocal monophyly of Z. atricapilla and Z. leucophrys using large panels of single nucleotide polymorphisms (SNPs). The pattern of cytonuclear discordance is consistent with limited, historical hybridization and mitochondrial introgression, rather than a recent origin and incomplete lineage sorting between recent sister species. We found evidence of nuclear phylogeographic structure within Z. leucophrys with two distinct clades. Altogether, our results indicate deeper divergences between Z. atricapilla and Z. leucophrys than inferred using mitochondrial markers. Our results demonstrate the limitations of relying solely on mitochondrial DNA for taxonomy, and raise questions about the possibility of selection on the mitochondrial genome during temperature oscillations (e.g. during the Pleistocene). Historical mitochondrial introgression facilitated by past environmental changes could cause erroneous dating of lineage splitting in other taxa when based on mitochondrial DNA alone.