Comparative Population Genomics of Cryptic Speciation and Adaptive Divergence in Bicknell's and Gray-Cheeked Thrushes (Aves: Catharus bicknelli and Catharus minimus).

Cryptic speciation may occur when reproductive isolation is recent or the accumulation of morphological differences between sister lineages is slowed by stabilizing selection preventing phenotypic differentiation. In North America, Bicknell's Thrush (Catharus bicknelli) and its sister species, the Gray-cheeked Thrush (Catharus minimus), are parapatrically breeding migratory songbirds, distinguishable in nature only by subtle differences in song and coloration, and were recognized as distinct species only in the 1990s. Previous molecular studies have estimated that the species diverged approximately 120,000-420,000 YBP and found very low levels of introgression despite their similarity and sympatry in the spring (prebreeding) migration. To further clarify the history, genetic divergence, genomic structure, and adaptive processes in C. bicknelli and C. minimus, we sequenced and assembled high-coverage reference genomes of both species and resequenced genomes from population samples of C. bicknelli, C. minimus, and two individuals of the Swainson's Thrush (Catharus ustulatus). The genome of C. bicknelli exhibits markedly higher abundances of transposable elements compared with other Catharus and chicken. Demographic and admixture analyses confirm moderate genome-wide differentiation (Fst ≈ 0.10) and limited gene flow between C. bicknelli and C. minimus, but suggest a more recent divergence than estimates based on mtDNA. We find evidence of rapid evolution of the Z-chromosome and elevated divergence consistent with natural selection on genomic regions near genes involved with neuronal processes in C. bicknelli. These genomes are a useful resource for future investigations of speciation, migration, and adaptation in Catharus thrushes.

Phenotypic and genomic diversification with isolation by environment along elevational gradients in a neotropical treefrog.

Understanding how geographic and environmental heterogeneity drive local patterns of genetic variation is a major goal of ecological genomics and a key question in evolutionary biology. The tropical Andes and inter-Andean valleys are shaped by markedly heterogeneous landscapes, where species experience strong selective processes. We examined genome-wide SNP data together with behavioural and ecological traits (mating calls and body size) known to contribute to genetic isolation in anurans in the banana tree-dwelling frog, Boana platanera, distributed across an environmental gradient in Central Colombia (northern South America). Here, we analysed the relationships between environmentally (temperature and precipitation) associated genetic and phenotypic differentiation and the potential drivers of isolation by environment along an elevation gradient. We identified candidate SNPs associated with temperature and body size, which follow a clinal pattern of genome-wide differentiation tightly coupled with phenotypic variation: as elevation increases, B. platanera exhibits larger body size and longer call duration with more pulses but lower pulse rate and frequency. Thus, the environmental landscape has rendered a scenario where isolation by environment and candidate loci show concordance with phenotypic divergence in this tropical frog along an elevation gradient in the Colombian Andes. Our study sets the basis for evaluating the role of temperature in the genetic structure and local adaptation in tropical treefrogs and its putative effect on life cycle (embryos, tadpoles, adults) along elevation gradients.

Prospects for sociogenomics in avian cooperative breeding and parental care.

For the last 40 years, the study of cooperative breeding (CB) in birds has proceeded primarily in the context of discovering the ecological, geographical, and behavioral drivers of helping. The advent of molecular tools in the early 1990s assisted in clarifying the relatedness of helpers to those helped, in some cases, confirming predictions of kin selection theory. Methods for genome-wide analysis of sequence variation, gene expression, and epigenetics promise to add new dimensions to our understanding of avian CB, primarily in the area of molecular and developmental correlates of delayed breeding and dispersal, as well as the ontogeny of achieving parental status in nature. Here, we outline key ways in which modern -omics approaches, in particular genome sequencing, transcriptomics, and epigenetic profiling such as ATAC-seq, can be used to add a new level of analysis of avian CB. Building on recent and ongoing studies of avian social behavior and sociogenomics, we review how high-throughput sequencing of a focal species or clade can provide a robust foundation for downstream, context-dependent destructive and non-destructive sampling of specific tissues or physiological states in the field for analysis of gene expression and epigenetics. -Omics approaches have the potential to inform not only studies of the diversification of CB over evolutionary time, but real-time analyses of behavioral interactions in the field or lab. Sociogenomics of birds represents a new branch in the network of methods used to study CB, and can help clarify ways in which the different levels of analysis of CB ultimately interact in novel and unexpected ways.

Integrating natural history collections and comparative genomics to study the genetic architecture of convergent evolution.

Evolutionary convergence has been long considered primary evidence of adaptation driven by natural selection and provides opportunities to explore evolutionary repeatability and predictability. In recent years, there has been increased interest in exploring the genetic mechanisms underlying convergent evolution, in part, owing to the advent of genomic techniques. However, the current 'genomics gold rush' in studies of convergence has overshadowed the reality that most trait classifications are quite broadly defined, resulting in incomplete or potentially biased interpretations of results. Genomic studies of convergence would be greatly improved by integrating deep 'vertical', natural history knowledge with 'horizontal' knowledge focusing on the breadth of taxonomic diversity. Natural history collections have and continue to be best positioned for increasing our comprehensive understanding of phenotypic diversity, with modern practices of digitization and databasing of morphological traits providing exciting improvements in our ability to evaluate the degree of morphological convergence. Combining more detailed phenotypic data with the well-established field of genomics will enable scientists to make progress on an important goal in biology: to understand the degree to which genetic or molecular convergence is associated with phenotypic convergence. Although the fields of comparative biology or comparative genomics alone can separately reveal important insights into convergent evolution, here we suggest that the synergistic and complementary roles of natural history collection-derived phenomic data and comparative genomics methods can be particularly powerful in together elucidating the genomic basis of convergent evolution among higher taxa. This article is part of the theme issue 'Convergent evolution in the genomics era: new insights and directions'.

Genomic footprints of adaptation in a cooperatively breeding tropical bird across a vegetation gradient.

Identifying the genetic basis of phenotypic variation and its relationship with the environment is key to understanding how local adaptations evolve. Such patterns are especially interesting among populations distributed across habitat gradients, where genetic structure can be driven by isolation by distance (IBD) and/or isolation by environment (IBE). Here, we used variation in ~1,600 high-quality SNPs derived from paired-end sequencing of double-digest restriction site-associated DNA (ddRAD-Seq) to test hypotheses related to IBD and IBE in the Yucatan jay (Cyanocorax yucatanicus), a tropical bird endemic to the Yucatán Peninsula. This peninsula is characterized by a precipitation and vegetation gradient-from dry to evergreen tropical forests-that is associated with morphological variation in this species. We found a moderate level of nucleotide diversity (π = .008) and little evidence for genetic differentiation among vegetation types. Analyses of neutral and putatively adaptive SNPs (identified by complementary genome-scan approaches) indicate that IBD is the most reliable explanation to account for frequency distribution of the former, while IBE has to be invoked to explain those of the later. These results suggest that selective factors acting along a vegetation gradient can promote local adaptation in the presence of gene flow in a vagile, nonmigratory and geographically restricted species. The putative candidate SNPs identified here are located within or linked to a variety of genes that represent ideal targets for future genomic surveys.