Pervasive gene flow despite strong and varied reproductive barriers in swordtails.

One of the mechanisms that can lead to the formation of new species occurs through the evolution of reproductive barriers. However, recent research has demonstrated that hybridization has been pervasive across the tree of life even in the presence of strong barriers. Swordtail fishes (genus Xiphophorus) are an emerging model system for studying the interface between these barriers and hybridization. We document overlapping mechanisms that act as barriers between closely related species, X. birchmanni and X. cortezi, by combining genomic sequencing from natural hybrid populations, artificial crosses, behavioral assays, sperm performance, and developmental studies. We show that strong assortative mating plays a key role in maintaining subpopulations with distinct ancestry in natural hybrid populations. Lab experiments demonstrate that artificial F1 crosses experience dysfunction: crosses with X. birchmanni females were largely inviable and crosses with X. cortezi females had a heavily skewed sex ratio. Using F2 hybrids we identify several genomic regions that strongly impact hybrid viability. Strikingly, two of these regions underlie genetic incompatibilities in hybrids between X. birchmanni and its sister species X. malinche. Our results demonstrate that ancient hybridization has played a role in the origin of this shared genetic incompatibility. Moreover, ancestry mismatch at these incompatible regions has remarkably similar consequences for phenotypes and hybrid survival in X. cortezi × X. birchmanni hybrids as in X. malinche × X. birchmanni hybrids. Our findings identify varied reproductive barriers that shape genetic exchange between naturally hybridizing species and highlight the complex evolutionary outcomes of hybridization.

Genome evolution is surprisingly predictable after initial hybridization.

Over the past two decades, evolutionary biologists have come to appreciate that hybridization, or genetic exchange between distinct lineages, is remarkably common - not just in particular lineages but in taxonomic groups across the tree of life. As a result, the genomes of many modern species harbor regions inherited from related species. This observation has raised fundamental questions about the degree to which the genomic outcomes of hybridization are repeatable and the degree to which natural selection drives such repeatability. However, a lack of appropriate systems to answer these questions has limited empirical progress in this area. Here, we leverage independently formed hybrid populations between the swordtail fish Xiphophorus birchmanni and X. cortezi to address this fundamental question. We find that local ancestry in one hybrid population is remarkably predictive of local ancestry in another, demographically independent hybrid population. Applying newly developed methods, we can attribute much of this repeatability to strong selection in the earliest generations after initial hybridization. We complement these analyses with time-series data that demonstrates that ancestry at regions under selection has remained stable over the past ~40 generations of evolution. Finally, we compare our results to the well-studied X. birchmanni×X. malinche hybrid populations and conclude that deeper evolutionary divergence has resulted in stronger selection and higher repeatability in patterns of local ancestry in hybrids between X. birchmanni and X. cortezi.

Introgression.

Biologists have forever sought to understand how species arise and persist. Historically, species that rarely interbreed, or are reproductively isolated, were considered the norm, while those with incomplete reproductive isolation were considered less common. Over the last few decades, advances in genomics have transformed our understanding of the frequency of gene flow between species and with it our ideas about reproductive isolation in nature. These advances have uncovered a rich and often complicated history of genetic exchange between species - demonstrating that such genetic introgression is an important evolutionary process widespread across the tree of life (Figure 1).

Revisiting a classic hybrid zone: Movement of the northern flicker hybrid zone in contemporary times.

Natural hybrid zones have provided important insights into the evolutionary process, and their geographic dynamics over time can help to disentangle the underlying biological processes that maintain them. Here, we leverage replicated sampling of an identical transect across the hybrid zone between yellow-shafted and red-shafted flickers in the Great Plains to assess its stability over ∼60 years (1955-1957 to 2016-2018). We identify a ∼73-km westward shift in the hybrid zone center toward the range of the red-shafted flicker, but find no associated changes in width over our sampling period. In fact, the hybrid zone remains remarkably narrow, suggesting some kind of selective pressure maintains the zone. By comparing to previous work in the same geographic region, it appears likely that the movement in the hybrid zone has occurred in the years since the early 1980s. This recent movement may be related to changes in climate or land management practices that have allowed westward movement of yellow-shafted flickers into the Great Plains.

Two new hybrid populations expand the swordtail hybridization model system.

Natural hybridization events provide unique windows into the barriers that keep species apart as well as the consequences of their breakdown. Here, we characterize hybrid populations formed between the northern swordtail fish Xiphophorus cortezi and Xiphophorus birchmanni from collection sites on two rivers. We use simulations and new genetic reference panels to develop sensitive and accurate local ancestry calling in this novel system. Strikingly, we find that hybrid populations on both rivers consist of two genetically distinct subpopulations: a cluster of pure X. birchmanni individuals and one of phenotypically intermediate hybrids that derive ∼85-90% of their genome from X. cortezi. Simulations suggest that initial hybridization occurred ∼150 generations ago at both sites, with little evidence for contemporary gene flow between subpopulations. This population structure is consistent with strong assortative mating between individuals of similar ancestry. The patterns of population structure uncovered here mirror those seen in hybridization between X. birchmanni and its sister species, Xiphophorus malinche, indicating an important role for assortative mating in the evolution of hybrid populations. Future comparisons will provide a window into the shared mechanisms driving the outcomes of hybridization not only among independent hybridization events between the same species but also across distinct species pairs.

Extensive hybridization reveals multiple coloration genes underlying a complex plumage phenotype.

Coloration is an important target of both natural and sexual selection. Discovering the genetic basis of colour differences can help us to understand how this visually striking phenotype evolves. Hybridizing taxa with both clear colour differences and shallow genomic divergences are unusually tractable for associating coloration phenotypes with their causal genotypes. Here, we leverage the extensive admixture between two common North American woodpeckers-yellow-shafted and red-shafted flickers-to identify the genomic bases of six distinct plumage patches involving both melanin and carotenoid pigments. Comparisons between flickers across approximately 7.25 million genome-wide SNPs show that these two forms differ at only a small proportion of the genome (mean FST = 0.008). Within the few highly differentiated genomic regions, we identify 368 SNPs significantly associated with four of the six plumage patches. These SNPs are linked to multiple genes known to be involved in melanin and carotenoid pigmentation. For example, a gene (CYP2J19) known to cause yellow to red colour transitions in other birds is strongly associated with the yellow versus red differences in the wing and tail feathers of these flickers. Additionally, our analyses suggest novel links between known melanin genes and carotenoid coloration. Our finding of patch-specific control of plumage coloration adds to the growing body of literature suggesting colour diversity in animals could be created through selection acting on novel combinations of coloration genes.

Genomic differentiation and local adaptation on a microgeographic scale in a resident songbird.

Elucidating forces capable of driving species diversification in the face of gene flow remains a key goal in evolutionary biology. Song sparrows, Melospiza melodia, occur as 25 subspecies in diverse habitats across North America, are among the continent's most widespread vertebrate species, and are exemplary of many highly variable species for which the conservation of locally adapted populations may be critical to their range-wide persistence. We focus here on six morphologically distinct subspecies resident in the San Francisco Bay region, including three salt-marsh endemics and three residents in upland and riparian habitats adjacent to the Bay. We used reduced-representation sequencing to generate 2,773 SNPs to explore genetic differentiation, spatial population structure, and demographic history. Clustering separated individuals from each of the six subspecies, indicating subtle differentiation at microgeographic scales. Evidence of limited gene flow and low nucleotide diversity across all six subspecies further supports a hypothesis of isolation among locally adapted populations. We suggest that natural selection for genotypes adapted to salt marsh environments and changes in demography over the past century have acted in concert to drive the patterns of diversification reported here. Our results offer evidence of microgeographic specialization in a highly polytypic bird species long discussed as a model of sympatric speciation and rapid adaptation, and they support the hypothesis that conserving locally adapted populations may be critical to the range-wide persistence of similarly highly variable species.

Gender Differences in Student Participation in an Active-Learning Classroom.

Overwhelming evidence demonstrating the benefits of active-learning pedagogy has led to a shift in teaching that requires students to interact more in the classroom. To date, few studies have assessed whether there are gender-specific differences in participation in active-learning science, technology, engineering, and mathematics (STEM) courses, and fewer have looked across different types of classroom participation. Over two semesters, we observed an introductory biology course at a large research-intensive university and categorized student participation into seven distinct categories to identify gender gaps in participation. Additionally, we collected student grades and administered a postcourse survey that gauged student scientific self-efficacy and salience of gender identity. We found that men participated more than expected based on the class composition in most participation categories. In particular, men were strongly overrepresented in voluntary responses after small-group discussions across both semesters. Women in the course reported lower scientific self-efficacy and greater salience of gender identity. Our results suggest that active learning in itself is not a panacea for STEM equity; rather, to maximize the benefits of active-learning pedagogy, instructors should make a concerted effort to use teaching strategies that are inclusive and encourage equitable participation by all students.

Deconstructing isolation-by-distance: The genomic consequences of limited dispersal.

Geographically limited dispersal can shape genetic population structure and result in a correlation between genetic and geographic distance, commonly called isolation-by-distance. Despite the prevalence of isolation-by-distance in nature, to date few studies have empirically demonstrated the processes that generate this pattern, largely because few populations have direct measures of individual dispersal and pedigree information. Intensive, long-term demographic studies and exhaustive genomic surveys in the Florida Scrub-Jay (Aphelocoma coerulescens) provide an excellent opportunity to investigate the influence of dispersal on genetic structure. Here, we used a panel of genome-wide SNPs and extensive pedigree information to explore the role of limited dispersal in shaping patterns of isolation-by-distance in both sexes, and at an exceedingly fine spatial scale (within ~10 km). Isolation-by-distance patterns were stronger in male-male and male-female comparisons than in female-female comparisons, consistent with observed differences in dispersal propensity between the sexes. Using the pedigree, we demonstrated how various genealogical relationships contribute to fine-scale isolation-by-distance. Simulations using field-observed distributions of male and female natal dispersal distances showed good agreement with the distribution of geographic distances between breeding individuals of different pedigree relationship classes. Furthermore, we built coalescent simulations parameterized by the observed dispersal curve, population density, and immigration rate, and showed how incorporating these extensions to Malécot's theory of isolation-by-distance allows us to accurately reconstruct observed sex-specific isolation-by-distance patterns in autosomal and Z-linked SNPs. Therefore, patterns of fine-scale isolation-by-distance in the Florida Scrub-Jay can be well understood as a result of limited dispersal over contemporary timescales.