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Understanding the processes of diversification along the speciation continuum in a recent evolutionary radiation of grasshoppers

Victor Noguerales. Estación Biológica de Doñana e Instituto de Investigación en Recursos Cinegéticos. Supervisors: Joaquín Ortego & Pedro J. Cordero. Julio 2017.
Summary:
Understanding the mechanisms that determine genetic and phenotypic divergence among populations, lineages and species is a paramount goal in evolutionary biology. Recent evolutionary radiations constitute a well-suited study system to address the study of such mechanisms because the genetic signatures left by divergence processes have not been erased by time and can be used to infer the evolutionary and demographic trajectories of lineages and species. This PhD thesis employs a multi-disciplinary approach in order to address the study of neutral and adaptive processes, and their links with landscape composition, throughout the whole spatiotemporal spectrum at which genetic and phenotypic divergence takes place. Specifically, the main objective of this PhD thesis is to understand the relative contribution of environment, climatic fluctuations and geography on the spatial patterns of genetic and phenotypic variation at the species, lineage and population levels, using as study model a recent evolution radiation of grasshoppers: the Chorthippus group binotatus species complex (Acrididae: Gomphocerinae). Our species delimitation analyses integrating genomic and morphological information revealed that the taxonomic status of species and subspecies is statistically equivalent and, hence, the Chorthippus group binotatus complex is composed of eight different biological entities that merit full species recognition. The study of Chorthippus binotatus binotatus at a range-wide phylogeographic scale shows that this taxon presents four main mitochondrial lineages that probably diverged in allopatry as a consequence of its isolation by geographic barriers (i.e. the Pyrenees[JO1] ) and in different climatic refugia during the Pleistocene. The existence of a lineage exclusive from western and central France indicates that the species long-term persisted in areas located at the present northern limit of its distribution range, although such populations were likely submitted to severe demographic bottlenecks and currently present very low levels of genetic diversity. At a lower spatial scale, landscape genetic analyses revealed that isolation by resistance defined by topographic complexity was the best-fitting scenario explaining population genetic differentiation of both C. binotatus binotatus in southeastern Iberia and C. saulcyi moralesi in the Pyrenees. Although environmental conditions did not explain the spatial patterns of genetic differentiation of C. saulcyi moralesi, we found that divergent selection mediated by climatic gradients had an important role on phenotypic differentiation processes in this taxon. In particular, our results indicate that the degree of development of forewings is associated to local environmental conditions. This fact suggests that variation in genomic regions involved in the expression of such trait may have resulted from an adaptive response to different climatic regimes. The populations located at the limits of the species distribution range presented proportionally longer forewings, a trait linked with dispersal capability. Such peripheral populations exhibited lower genetic diversity in comparison to those located at the core of the species distribution range, which suggests that the former are subjected to considerable demographic instability and this leads to directional selection towards more dispersive phenotypes. Overall, the results from this PhD thesis highlight the importance of combining genetic, phenotypic and environmental data in order to better understand the evolutionary mechanisms that are at play at different spatiotemporal scales and drive divergence processes along the speciation continuum.