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Hybrid zones reveal the strength of reproductive isolation between populations undergoing speciation and are thus a key tool used in evolutionary biology research. Multiple replicate transects across the same hybrid zone offer further insight into the dynamics of hybridization in different environments, clarifying the role of extrinsic forces on the speciation process. Red-breasted and Red-naped Sapsuckers (Sphyrapicus ruber and S. nuchalis) have a long zone of contact over approximately 1,600 km from central British Columbia, Canada to central California, USA. We compared Genotyping-by-Sequencing data from three independent sapsucker hybrid zone transects to compare hybridization dynamics between the same species under variable geoclimatic conditions. We then generated geographic clines of the genomic data to compare hybrid zone widths and used Random Forest models and linear regression to assess the relationship between climate and sapsucker ancestry along each transect. Our results show variation in symmetry and directionality of back crossing, patterns often indicative of moving hybrid zones. We note variable cline widths among transects, indicating differences in the selection maintaining hybrid zone dynamics. Furthermore, Random Forest models identified different variables in close association with sapsucker ancestry across each transect. These results indicate a lack of repeatability across replicate transects and a strong influence of the local environment on hybrid zone dynamics.

Isolating barriers that drive speciation are commonly studied in the context of two-species 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 mate pair phenotypes and genotypes 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 likely occurred before the formation of this tri-species hybrid zone, and might result from bridge hybridization, vagrancies, or other three-species interactions.

Setophaga townsendi is a species of wood warbler (family Parulidae) in northwestern North America that has geographic structure in the mitochondrial and nuclear genomes: while interior populations have differentiated mitonuclear ancestry from the sister species S. occidentalis, coastal populations have a mix of inland and S. occidentalis mitonuclear ancestries. This coastal to inland transition in genomic ancestry raises the possibility of similar geographic structure in phenotypic traits, especially those involved in mate choice. Using qualitative and multivariate approaches, we investigated whether there is a sharp transition between coastal and inland populations in both song and in nuclear DNA. We find there is a shallow geographic cline in Type I song but not in Type II song. Nuclear DNA shows a gradient between coast and inland. There is little correlation between variation in song and the isolation-by-distance pattern in the nuclear DNA. Learned songbird song is shaped by both genetic and cultural processes. There has been a debate on whether song learning promotes or slows down population differentiation. By comparing the within-species variation in song and genetic structures, we can expand our understanding of the dynamic interplay between mating signals and population differentiation.

Sympatric species pairs provide researchers with the opportunity to study patterns of genomic differentiation during the late stages of speciation and to identify the genomic regions underlying reproductive isolation. The Golden-crowned Sparrow (Zonotrichia atricapilla) and the White-crowned Sparrow (Zonotrichia leucophrys) are broadly sympatric songbirds found in western North America. These sister species are phenotypically differentiated and largely reproductively isolated despite possessing similar mitochondrial genomes, likely due to recent mitochondrial introgression. We used a genotyping-by-sequencing (GBS) approach to determine the structure of nuclear genomic differentiation between these species and also between two hybridizing subspecies of Z. leucophrys, across more than 45,000 single nucleotide polymorphisms (SNPs). The two Z. leucophrys subspecies showed moderate levels of relative differentiation, as well as patterns consistent with a history of recurrent selection in both ancestral and daughter populations. Z. leucophrys and Z. atricapilla show high levels of relative differentiation and strong heterogeneity in the level of differentiation among different chromosomal regions, with a large portion of the Z chromosome showing highly elevated differentiation. Patterns of relative and absolute differentiation and linkage disequilibrium suggest a large inversion on the Z chromosome, with inversion haplotypes that segregate between Z. atricapilla and Z. leucophrys. While mitochondrial DNA differentiation is often emphasized in studies of speciation, differentiation between these Zonotrichia sparrows appears to have occurred first in the Z chromosome and secondarily in autosomes, followed by mitochondrial introgression. This putative inversion has implications for reproductive isolation between these species and adds to a growing body of evidence for the importance of inversions and the Z chromosome in speciation.

It is thought that two species can coexist if they use different resources present in the environment, yet this assumes that species are completely reproductively isolated. We simulate coexistence outcomes for two sympatric species that are ecologically differentiated but have incomplete reproductive isolation. The consequences of interbreeding crucially depend on hybrid fitness. When hybrid fitness is high, just a small rate of hybridization can lead to collapse of two species into one. Low hybrid fitness can cause population declines, making extinction of one or both species likely. High intrinsic growth rates result in higher reproductive rates when populations are below carrying capacity, reducing the probability of extinction and increasing the probability of stable coexistence at moderate levels of assortative mating and hybrid fitness. Very strong but incomplete assortative mating can induce low hybrid fitness via a mating disadvantage to rare genotypes, and this can stabilize coexistence of two species at high but incomplete levels of assortative mating. Given these results and evidence that it may take many millions of years of divergence before related species become sympatric, we postulate that coexistence of closely related species is more often limited by insufficient assortative mating than by insufficient ecological differentiation.

Comparisons of genomic variation among closely related species often show more differentiation in mitochondrial DNA (mtDNA) and sex chromosomes than in autosomes, a pattern expected due to the differing effective population sizes and evolutionary dynamics of these genomic components. Yet, introgression can cause species pairs to deviate dramatically from general differentiation trends. The yellowhammer (Emberiza citrinella) and pine bunting (E. leucocephalos) are hybridizing avian sister species that differ greatly in appearance and moderately in nuclear DNA, but that show no mtDNA differentiation. This discordance is best explained by adaptive mtDNA introgression-a process that can select for co-introgression at nuclear genes with mitochondrial functions (mitonuclear genes). To better understand these discordant differentiation patterns and characterize nuclear differentiation in this system, we investigated genome-wide differentiation between allopatric yellowhammers and pine buntings and compared it to what was seen previously in mtDNA. We found significant nuclear differentiation that was highly heterogeneous across the genome, with a particularly wide differentiation peak on the sex chromosome Z. We further investigated mitonuclear gene co-introgression between yellowhammers and pine buntings and found support for this process in the direction of pine buntings into yellowhammers. Genomic signals indicative of co-introgression were common in mitonuclear genes coding for subunits of the mitoribosome and electron transport chain complexes. Such introgression of mitochondrial DNA and mitonuclear genes provides a possible explanation for the patterns of high genomic heterogeneity in genomic differentiation seen among some species groups.