Evolutionary history and diversification mechanisms in the avian genus JuncoA multidisciplinary approach using phenotypic, ecological, phylogeographic and phylogenomic data

Resumen

Recently diversified systems are optimal research subjects to study the relative roles of genetic drift, gene flow and selection in shaping patterns of diversity and promoting the formation of evolutionary lineages and species. In the early stages of the speciation process, causal correlations between patterns of phenotypic divergence and adaptive genetic variability with specific selective factors are still recent and detectable. In turn, reconstructing the evolutionary relationships of closely related lineages is a challenging task because of incomplete lineage sorting at many loci and potential gene flow among incipient lineages. In this thesis, I develop an experimental design that combines phylogenetic and phylogeographic analyses with phenotypic, ecological and genomic data in order to reconstruct the evolutionary history and study mechanisms of early lineage divergence in the songbird genus Junco (Aves: Emberizidae) from Central and North America. Previous analyses based on mtDNA markers revealed a lack of genetic diversity and strong signatures of recent population expansion in the phenotypically differentiated and geographically structured boreal forms of dark-eyed junco, suggesting a process of rapid diversification during a northward recolonization of the North American continent from Mexico after the last glacial maximum (LGM) ca. 18,000 years ago. Phylogenetic molecular dating confirmed the postglacial origin of the northern juncos, and phylogenomic analyses based on genotyping-by-sequencing (GBS) single nucleotide polymorphisms (SNPs) recovered a pattern of reciprocal monophyly among the rapidly diversified young lineages, contrasting with at least four isolated lineages in the south showing relative phenotypic stasis. Whole-genome analyses also supported the recent origin of the boreal forms of Junco, and recovered signals of demographic expansions and limited gene flow during lineage diversification, suggesting a scenario of rapid divergence in allopatry. Using linear regression and multivariate analyses, I also found signs of an association between adaptive genomic variability and variation in both ecological and sexually selected traits, evidencing the roles of natural and sexual selection in jointly driving phenotypic diversification and lineage divergence in the recently diversified dark-eyed junco complex. In addition, genome surveys based on SNPs revealed genomic landscapes of divergence with no obvious regions of high differentiation, with significant outliers found to be scattered across the genome. These patterns are consistent with a diversification process driven by multiple selective factors acting on many independent genome-wide loci. Overall, the analyses and results reported in this dissertation reveal the Junco system as one of the fastest radiations known in vertebrates, driven by the combined effects of historical processes such as demographic expansions and drift in isolation, and also selective factors, including natural and sexual selection.