Pronounced differentiation on the Z chromosome and parts of the autosomes in crowned sparrows contrasts with mitochondrial paraphyly: implications for speciation.

When a single species evolves into multiple descendent species, some parts of the genome can play a key role in the evolution of reproductive isolation while other parts flow between the evolving species via interbreeding. Genomic evolution during the speciation process is particularly interesting when major components of the genome-for instance, sex chromosomes vs. autosomes vs. mitochondrial DNA-show widely differing patterns of relationships between three diverging populations. The golden-crowned sparrow (Zonotrichia atricapilla) and the white-crowned sparrow (Zonotrichia leucophrys) are phenotypically differentiated sister species that are largely reproductively isolated despite possessing similar mitochondrial genomes, likely due to recent introgression. We assessed variation in more than 45,000 single nucleotide polymorphisms to determine the structure of nuclear genomic differentiation between these species and between two hybridizing subspecies of Z. leucophrys. The two Z. leucophrys subspecies show moderate levels of relative differentiation and patterns consistent with a history of recurrent selection in both ancestral and daughter populations, with much of the sex chromosome Z and a large region on the autosome 1A showing increased differentiation compared to the rest of the genome. The two species Z. leucophrys and Z. atricapilla show high relative differentiation and strong heterogeneity in the level of differentiation among various chromosomal regions, with a large portion of the sex chromosome (Z) showing highly divergent haplotypes between these species. Studies of speciation often emphasize mitochondrial DNA differentiation, but speciation between Z. atricapilla and Z. leucophrys appears primarily associated with Z chromosome divergence and more moderately associated with autosomal differentiation, whereas mitochondria are highly similar due apparently to recent introgression. These results add to the growing body of evidence for highly heterogeneous patterns of genomic differentiation during speciation, with some genomic regions showing a lack of gene flow between populations many hundreds of thousands of years before other genomic regions.

High heterogeneity in genomic differentiation between phenotypically divergent songbirds: a test of mitonuclear co-introgression.

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.

Successful Integration of Data Science in Undergraduate Biostatistics Courses Using Cognitive Load Theory.

Biostatistics courses are integral to many undergraduate biology programs. Such courses have often been taught using point-and-click software, but these programs are now seldom used by researchers or professional biologists. Instead, biology professionals typically use programming languages, such as R, which are better suited to analyzing complex data sets. However, teaching biostatistics and programming simultaneously has the potential to overload the students and hinder their learning. We sought to mitigate this overload by using cognitive load theory (CLT) to develop assignments for two biostatistics courses. We evaluated the effectiveness of these assignments by comparing student cohorts who were taught R using these assignments (n = 146) with those who were taught R through example scripts or were instructed on a point-and-click software program (control, n = 181). We surveyed all cohorts and analyzed statistical and programming ability through students' lab reports or final exams. Students who learned R through our assignments rated their programming ability higher and were more likely to put the usage of R as a skill in their curricula vitae. We also found that the treatment students were more motivated, less frustrated, and less stressed when using R. These results suggest that we can use CLT to teach challenging material.

Population genomic analyses reveal a highly differentiated and endangered genetic cluster of northern goshawks (Accipiter gentilis laingi) in Haida Gwaii.

Accurate knowledge of geographic ranges and genetic relationships among populations is important when managing a species or population of conservation concern. Along the western coast of Canada, a subspecies of the northern goshawk (Accipiter gentilis laingi) is legally designated as Threatened. The range and distinctness of this form, in comparison with the broadly distributed North American subspecies (Accipiter gentilis atricapillus), is unclear. Given this morphological uncertainty, we analyzed genomic relationships in thousands of single nucleotide polymorphisms identified using genotyping-by-sequencing of high-quality genetic samples. Results revealed a genetically distinct population of northern goshawks on the archipelago of Haida Gwaii and subtle structuring among other North American sampling regions. We then developed genotyping assays for ten loci that are highly differentiated between the two main genetic clusters, allowing inclusion of hundreds of low-quality samples and confirming that the distinct genetic cluster is restricted to Haida Gwaii. As the laingi form was originally described as being based on Haida Gwaii (where the type specimen is from), further morphological analysis may result in this name being restricted to the Haida Gwaii genetic cluster. Regardless of taxonomic treatment, the distinct Haida Gwaii genetic cluster along with the small and declining population size of the Haida Gwaii population suggests a high risk of extinction of an ecologically and genetically distinct form of northern goshawk. Outside of Haida Gwaii, sampling regions along the coast of BC and southeast Alaska (often considered regions inhabited by laingi) show some subtle differentiation from other North American regions. These results will increase the effectiveness of conservation management of northern goshawks in northwestern North America. More broadly, other conservation-related studies of genetic variation may benefit from the two-step approach we employed that first surveys genomic variation using high-quality samples and then genotypes low-quality samples at particularly informative loci.