Molecular evidence for the freshwater lifestyle conquer in two Italian endemic representatives of the Gobiidae family: Padogobius nigricans and Padogobius bonelli

Abstract

Evolutionary transitions between marine and freshwater habitats are rare events that can have profound impacts on aquatic biodiversity. Marine–freshwater transitions are a particularly interesting aspect of the evolutionary biology of many fish groups. Within Mediterranean fish biodiversity, one of the most enigmatic group in terms of adaptive radiation on evolutionary time scale is represented by the Gobiidae family (Teleostei). Mediterranean representatives of Gobiidae are divided in three distinct evolutionary lineages: Pomatoschistus lineage, with marine and freshwater species; Aphia lineage, composed of exclusively marine species inhabiting the Mediterranean and North-East Atlantic; Gobius lineage, including a radiation in the inland Ponto-Caspian region (Benthophilines), as well as species inhabiting the Mediterranean, North-eastern Atlantic, and Atlantic coast of Africa. Within Gobius lineage, one intriguing open question is related to the origin of the genus Padogobius. Padogobius is represented by only two species: P. nigricans Canestrini, 1867, endemic to Central and Northern Italy, and P. bonelli (Bonaparte, 1846), known from the North-Eastern Italy and adjacent areas. Both species are pure freshwater inhabitants. Nevertheless, whether the adaptation to the freshwater habitats evolved only once or independently is still debated. In this dissertation I inferred a more comprehensive analysis of species-level relationships of the major representatives of Mediterranean gobies, linking evolutionary marine/freshwater ecological transitions to the paleohistory of the Mediterranean basin. I implemented a time calibrated species tree inference with ancestral state reconstruction encompassing the search for a sister group of Padogobius to test the monophyly of the freshwater habit. All the reconstruction proposed in this study converge in the definition of the polyphyletic origin of the genus Padogobius. The results provide strong support for a multiple independent origin of the freshwater habit in the two endemic Italian species P. bonelli and P. nigricans. Additionally, the results from species tree inference propose new insight in the relationships among members of Mediterranean Gobius lineage, previously not considered. Molecular dating of the radiation of Gobius species and Padogobius representatives are consistent with the oceanographic and tectonic history of the basin, enhancing of the role of the Messinian Salinity Crisis in shaping Mediterranean biodiversity.