Lower survival of hybrid grosbeaks, but not towhees, suggests a molt divide disfavors hybrids.

Although avian hybrid zones in the Great Plains have been studied for almost 70 years, we know surprisingly little about the fitness costs to hybrids that keep these zones narrow. We compare age ratios in grosbeaks (Pheucticus ludovicianus and P. melanocephalus) and towhees (Pipilo erythropthalums and P. maculatus), two species pairs that differ in their life histories and molt schedules, to evaluate survival between hybrids and parentals. We then contrast molt and migratory divides as possible sources of selection against hybrids. Hybrid grosbeaks had 27%-33% lower survival relative to their parentals, whereas hybrid towhees had survival rates similar to parentals. Age ratio data for hybrid grosbeaks suggest high mortality in older birds, as expected if selection operates after the first year of life. This pattern is consistent with parental species of grosbeaks having contrasting molt schedules relative to migration, suggesting high mortality costs to hybrids driven by molt biology, which are expressed later in life. Contrasts in molt schedules are absent in towhees. While migratory divides may exist for towhees and grosbeaks, the low adult survival of hybrid grosbeaks suggest that molt may be an important and underappreciated source of selection maintaining this and other narrow avian hybrid zones.

A complex genomic architecture underlies reproductive isolation in a North American oriole hybrid zone.

Natural hybrid zones provide powerful opportunities for identifying the mechanisms that facilitate and inhibit speciation. Documenting the extent of genomic admixture allows us to discern the architecture of reproductive isolation through the identification of isolating barriers. This approach is particularly powerful for characterizing the accumulation of isolating barriers in systems exhibiting varying levels of genomic divergence. Here, we use a hybrid zone between two species-the Baltimore (Icterus galbula) and Bullock's (I. bullockii) orioles-to investigate this architecture of reproductive isolation. We combine whole genome re-sequencing with data from an additional 313 individuals amplityped at ancestry-informative markers to characterize fine-scale patterns of admixture, and to quantify links between genes and the plumage traits. On a genome-wide scale, we document several putative barriers to reproduction, including elevated peaks of divergence above a generally high genomic baseline, a large putative inversion on the Z chromosome, and complex interactions between melanogenesis-pathway candidate genes. Concordant and coincident clines for these different genomic regions further suggest the coupling of pre- and post-mating barriers. Our findings of complex and coupled interactions between pre- and post-mating barriers suggest a relatively rapid accumulation of barriers between these species, and they demonstrate the complexities of the speciation process.

Geographic variability of hybridization between red-breasted and red-naped sapsuckers.

Hybrid zones reveal the strength of reproductive isolation between populations undergoing speciation and are a key tool in evolutionary biology research. Multiple replicate transects across the same hybrid zone offer 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 Sphyrapicus nuchalis) have a long zone of contact over approximately 1,600 km from central British Columbia, Canada to central California, USA. We used Genotyping-by-Sequencing data from three independent sapsucker hybrid zone transects to compare hybridization dynamics between these species under variable geoclimatic conditions. We generated geographic clines of the genomic data to compare hybrid zone widths and used random forests models and linear regression to assess the relationship between climate and sapsucker ancestry along each transect. Our results show variation in the directionality of backcrossing, often indicative of moving hybrid zones. We note variable cline widths among transects, indicating differences in selection maintaining hybrid zone dynamics. Furthermore, random forests 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.

Historical DNA as a tool to address key questions in avian biology and evolution: A review of methods, challenges, applications, and future directions.

Museum specimens play a crucial role in addressing key questions in systematics, evolution, ecology, and conservation. With the advent of high-throughput sequencing technologies, specimens that have long been the foundation of important biological discoveries can inform new perspectives as sources of genomic data. Despite the many possibilities associated with analyzing DNA from historical specimens, several challenges persist. Using avian systems as a model, we review DNA extraction protocols, sequencing technologies, and capture methods that are helping researchers overcome some of these difficulties. We highlight empirical examples in which researchers have used these technologies to address fundamental questions related to avian conservation and evolution. Increasing accessibility to new sequencing technologies will provide researchers with tools to tap into the wealth of information contained within our valuable natural history collections.

Phenotypic and genetic introgression across a moving woodpecker hybrid zone.

In hybrid zones in which two divergent taxa come into secondary contact and interbreed, selection can maintain phenotypic diversity despite widespread genetic introgression. Red-breasted (Sphyrapicus ruber) and red-naped (S. nuchalis) sapsuckers meet and hybridize along a narrow contact zone that stretches from northern California to southern British Columbia. We found strong evidence for changes in the structure of this hybrid zone across time, with significant temporal shifts in allele frequencies and in the proportions of parental phenotypes across the landscape. In addition to these shifts, we found that differences in plumage predict genetic differences (R2  = 0.80), suggesting that plumage is a useful proxy for assessing ancestry. We also found a significant bimodal distribution of hybrids across the contact zone, suggesting that premating barriers may be driving reproductive isolation, perhaps as a result of assortative mating based on plumage differences. However, despite evidence of selection and strong patterns of population structure between parental samples, we found only weak patterns of genetic divergence. Using museum specimens and genomic data, this study of sapsuckers provides insight into the ways in which phenotypic and genetic structure have changed over a 40-year period, as well as insight into the mechanisms that may contribute to the maintenance of the hybrid zone over time.

Changing climate mediates sapsucker (Aves: Sphyrapicus) hybrid zone movement.

Hybrid zones, where two divergent taxa meet and interbreed, offer unique opportunities to investigate how climate contributes to reproductive isolation between closely related taxa and how these taxa may respond to climatic changes. Red-naped (Sphyrapicus nuchalis) and Red-breasted (Sphyrapicus ruber) sapsuckers (Aves: Picidae) hybridize along a narrow contact zone that stretches from northern California to British Columbia. The hybrid zone between these species has been studied extensively for more than 100 years and represents an excellent system for investigations of the evolution of reproductive isolation. Shifts in the proportions of phenotypes at hybrid localities since 1910 that were inferred using specimens from museum collections were confirmed using species distribution models. We predicted the historical, current, and future distributions of parental and hybrid sapsuckers using Random Forests models to quantify how climate change is affecting hybrid zone movement in the Pacific Northwest. We found observed distribution shifts of parental sapsuckers were likely the result of climate change over the past 100 years, with these shifts predicted to continue for both sapsuckers over the next 80 years. We found Red-breasted Sapsuckers are predicted to continue to expand, while Red-naped Sapsuckers are predicted to contract substantially under future climate scenarios. As a result of the predicted changes, the amount of overlap in the distribution of these sapsuckers may decrease. Using hybrid phenotypes, we found the climate niche occupied by the hybrid zone is predicted to disappear under future conditions. The disappearance of this climate niche where the two parental species come into contact and hybridize may lead to a substantial reduction in genetic introgression. Understanding the impacts of global climate change on hybrid zones may help us to better understand how speciation has been shaped by climate in the past, as well as how evolution may respond to climate change in the future.

How spatio-temporal habitat connectivity affects amphibian genetic structure.

Heterogeneous landscapes and fluctuating environmental conditions can affect species dispersal, population genetics, and genetic structure, yet understanding how biotic and abiotic factors affect population dynamics in a fluctuating environment is critical for species management. We evaluated how spatio-temporal habitat connectivity influences dispersal and genetic structure in a population of boreal chorus frogs (Pseudacris maculata) using a landscape genetics approach. We developed gravity models to assess the contribution of various factors to the observed genetic distance as a measure of functional connectivity. We selected (a) wetland (within-site) and (b) landscape matrix (between-site) characteristics; and (c) wetland connectivity metrics using a unique methodology. Specifically, we developed three networks that quantify wetland connectivity based on: (i) P. maculata dispersal ability, (ii) temporal variation in wetland quality, and (iii) contribution of wetland stepping-stones to frog dispersal. We examined 18 wetlands in Colorado, and quantified 12 microsatellite loci from 322 individual frogs. We found that genetic connectivity was related to topographic complexity, within- and between-wetland differences in moisture, and wetland functional connectivity as contributed by stepping-stone wetlands. Our results highlight the role that dynamic environmental factors have on dispersal-limited species and illustrate how complex asynchronous interactions contribute to the structure of spatially-explicit metapopulations.

Low variation in the polymorphic Clock gene poly-Q region despite population genetic structure across barn swallow (Hirundo rustica) populations.

Recent studies of several species have reported a latitudinal cline in the circadian clock gene, Clock, which influences rhythms in both physiology and behavior. Latitudinal variation in this gene may hence reflect local adaptation to seasonal variation. In some bird populations, there is also an among-individual association between Clock poly-Q genotype and clutch initiation date and incubation period. We examined Clock poly-Q allele variation in the Barn Swallow (Hirundo rustica), a species with a cosmopolitan geographic distribution and considerable variation in life-history traits that may be influenced by the circadian clock. We genotyped Barn Swallows from five populations (from three subspecies) and compared variation at the Clock locus to that at microsatellite loci and mitochondrial DNA (mtDNA). We found very low variation in the Clock poly-Q region, as >96% of individuals were homozygous, and the two other alleles at this locus were globally rare. Genetic differentiation based on the Clock poly-Q locus was not correlated with genetic differentiation based on either microsatellite loci or mtDNA sequences. Our results show that high diversity in Clock poly-Q is not general across avian species. The low Clock variation in the background of heterogeneity in microsatellite and mtDNA loci in Barn Swallows may be an outcome of stabilizing selection on the Clock locus.