Cenozoic tectonic and climatic events in southern Iberian Peninsula: Implications for the evolutionary history of freshwater fish of the genus Squalius (Actinopterygii, Cyprinidae)

• The origin of Squalius malacitanus dates from Serravalian–Tortonian period.
• Gibraltar S. opening caused S. malacitanus Atlantic-Mediterranean populations divergence.
• Pleistocene river piracy drove southern Iberian colonization by S. pyrenaicus from Guadalquivir.
• Iberian Janda lagoon acted as a reservoir for freshwater fish populations during Pleistocene.

Southern Iberian freshwater ecosystems located at the border between the European and African plates represent a tectonically complex region spanning several geological ages, from the uplifting of the Betic Mountains in the Serravalian–Tortonian periods to the present. This area has also been subjected to the influence of changing climate conditions since the Middle–Upper Pliocene when seasonal weather patterns were established. Consequently, the ichthyofauna of southern Iberia is an interesting model system for analyzing the influence of Cenozoic tectonic and climatic events on its evolutionary history. The cyprinids Squalius malacitanus and Squalius pyrenaicus are allopatrically distributed in southern Iberia and their evolutionary history may have been defined by Cenozoic tectonic and climatic events. We analyzed MT-CYB (510 specimens) and RAG1 (140 specimens) genes of both species to reconstruct phylogenetic relationships and to estimate divergence times and ancestral distribution ranges of the species and their populations. We also assessed their levels of genetic structure and diversity as well as the amount of gene flow between populations. To investigate recent paleogeographical and climatic factors in southern Iberia, we modeled changes-through-time in sea level from the LGM to the present. Phylogenetic, geographic and population structure analyses revealed two well-supported species (S. malacitanus and S. pyrenaicus) in southern Iberia and two subclades (Atlantic and Mediterranean) within S. malacitanus. The origin of S. malacitanus and the separation of its Atlantic and Mediterranean populations occurred during the Serravalian–Tortonian and Miocene–Pliocene periods, respectively. These divergence events occurred in the Middle Pliocene and Pleistocene in S. pyrenaicus. In both species, Atlantic basins possessed populations with higher genetic diversity than Mediterranean, which may be explained by the Janda Lagoon. The isolation of S. malacitanus was earlier and related to the rising of the Betic Mountains. Divergence of its Atlantic and Mediterranean populations was associated with the creation of the freshwater systems of southern Iberia close to the Gibraltar Strait. The presence of S. pyrenaicus in southern Iberia may be the result of recent colonization associated with river capture, as demonstrated our biogeographic reconstruction.

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