Genomic divergence along the continuum of speciation in a recent evolutionary radiation of montane grasshoppers

Abstract

Unraveling the proximate processes that have shaped genetic variation of populations and led to lineage diversification and speciation is fundamental to understand the origin of present-day biodiversity patterns at both local and global scales. Cyclical Pleistocene glaciations played a pivotal role in the evolution of mid-latitude montane biotas, leading to distributional shifts that generated multiple opportunities for both allopatric speciation and secondary contact. In this thesis, we integrate genomic, morphological and environmental data and combine a diverse array of analytical procedures to investigate processes of genomic and phenotypic divergence acting at different stages along the speciation continuum. Specifically, this thesis focuses on the subgenus Dreuxius (genus Omocestus), an lbero-Maghrebian complex of montane grasshoppers distributed across the main mountain ranges of the region. Phylogenomic and geometric morphometric analyses supported the recent Pleistocene origin (< 1 Ma) of the complex, two reticulation events involving lineages at different stages ·of the· diversification continuum and the phenotypic distinctiveness of most sister taxa (Chapter 1). Moreover, phylogenetic reconstructions did not recover the reciprocal monophyly of taxa from Iberia and northwestern Africa, supporting two overseas Pleistocene migration events between the two continents (Chapter 1). lntegrative species delimitation analyses focusing on the Pyrenean endemics O. navasi and O. antigai did not support their current taxonomic status, pointing to the presence of a single species with little phenotypic variation, a wide climatic niche, and a marked genetic structure explained by limited population connectivity across the abrupt landscapes of the region (Chapter 2). Analyses of interspecific gene flow in the partially sympatric O. minutissimus and O. uhagonii rejected the hypothesis of contemporary hybridization but revealed past introgression in the area where the distributions of the two species overlap (Chapters 1 and 3). This supports a scenario of historical gene flow after secondary contact followed by the evolution of reproductive isolation that currently prevents hybridization among sympatric populations (Chapter 3). Demographic inference and testing of alternative models of intraspecific gene flow within each of the narrow-endemics O. bolivari and O. femoralis supported population genetic admixture during glacial periods and postglacial colonization of sky islands, rather than long-term isolation, as the scenario best explaining the contemporary distribution of genomic variation in the two taxa. The results of this thesis emphasize the key role of range-shifts driven by Pleistocene glacial cycles in promoting not only allopatric divergence but also secondary contact and genetic admixture among previously isolated gene pools. Overall, this thesis highlights the importance of combining population and phylogenomic approaches to improve our understanding about the processes governing the diversification of montane biotas across evolutionary scales spanning the continuum of speciation, from populations to species.