Genetic analyses of adaptive processes in the podarcis genus

Abstract

Wall lizards from the Podarcis genus, which have diversified and evolved in the Mediterranean basin, present wide morphological, ecological, and genetic variability. This diversity plays a key role in the maintenance of the evolutionary and adaptative potential of all the Podarcis populations and, consequently, in their conservation management. The main point of this thesis was to investigate adaptive processes in the Podarcis genus, examining how evolutionary mechanisms have shaped genomic and phenotypic divergence in different Podarcis populations. Specifically, it focuses on the Podarcis species complex that inhabit the Iberian Peninsula, especially the southeast (SE) region and the Columbretes archipelago, and on one endemic species from the Balearic Islands (Podarcis lilfordi). This objective was addressed through different approaches based on specific genetic markers, ecology, morphology, and/or genome-wide analyses. Regarding the Podarcis hispanicus species complex, a multilocus methodology showed that three different clades presenting an overlapping distribution inhabit the SE region. Phylogenetic relationships and geological history enabled a new species to be defined in this region, Podarcis galerai sp. nov. and the nominal taxon (Podarcis hispanicus sensu stricto) to be renamed. The latter was identified with Albacete/ Murcia lineage since it is situated at the closest point to the restricted-type locality of Monteagudo and presents the morphological traits that are most similar to those indicated for the nominal taxon. The taxonomic status of the third group, P. hispanicus (Valencia lineage), could not be fully defined due to the lack of sampling in the global distribution. The evolutionary origin of the Podarcis form from the Columbretes archipelago was corroborated to be conspecific with the mainland form Podarcis liolepis, specifically from the region of Peñagolosa, (Castellón, Spain). The divergence time between the insular and mainland forms was dated at 1.77 Ma coinciding with a sea level fluctuation period, when the two regions could have been connected. Current results disclose low genetic diversity in insular populations, which seems to have suffered diverse events of expansion and/or decrease in diversity (bottlenecks) throughout their evolutionary history. The extraordinary intra-specific variability present in the endemic lizard from the Balearic archipelago (P. lilfordi) was explored at the genetic, morphological, ecological, and behavioural level. The discordance found between phylogenetic, morphological, and ecological results indicates that the use of Evolutionarily Significant Units (ESUs) as taxonomic classification is better to ensure the evolutionary future of these populations and their consideration in conservation policies. Genome-wide analyses using double digest restriction-site associated DNA sequencing (ddRADseq) made it possible to detect more than 70,000 genome-wide single nucleotide polymorphisms (SNPs) that corroborated the uniqueness of these insular populations and highlighted the combined role of genetic drift and natural selection in driving divergence. Tests of selection identified approximately 2% of loci putatively under selection (outlier loci). Correlation analyses with different environmental variables found predation and human pressure as the most explanatory variables in shaping this adaptive divergence. The genetic base of the phenotypical trait of melanism present in several P. lilfordi populations was not found in either genome-wide analyses or MC1R candidate gene expression analyses.