Promiscuous Speciation with Gene Flow in Silverside Fish Genus Odontesthes (Atheriniformes, Atherinopsidae) from South Western Atlantic Ocean Basins Graciela Garcı´a 1 *, Ne ´stor Rı´os 1 , Vero ´ nica Gutie ´ rrez 1 , Jorge Guerra Varela 2 , Carmen Bouza Ferna ´ ndez 2 , Bele ´n Go ´ mez Pardo 2 , Paulino Martı´nez Portela 2 1 Seccio ´ n Gene ´tica Evolutiva, Facultad de Ciencias, UdelaR, Montevideo, Uruguay, 2 Departamento de Gene ´tica, Facultad de Veterinaria, Campus de Lugo, Universidad de Santiago de Compostela, Lugo, Spain Abstract The present paper integrates phylogenetic and population genetics analyses based on mitochondrial and nuclear molecular markers in silversides, genus Odontesthes, from a non-sampled area in the SW Atlantic Ocean to address species discrimination and to define Managements Units for sustainable conservation. All phylogenetic analyses based on the COI mitochondrial gene were consistent to support the monophyly of the genus Odontesthes and to include O. argentinensis, O. perugiae-humensis and some O. bonariensis haplotypes in a basal polytomy conforming a major derivative clade. Microsatellites data revealed somewhat higher genetic variability values in the O. argentinensis-perugia populations than in O. bonariensis and O. perugia-humensis taxa. Contrasting population genetics structuring emerged from mitochondrial and microsatellites analyses in these taxa. Whereas mitochondrial data supported two major groups (O. argentinensis-perugia- humensis vs. O. bonariensis-perugiae-humensis populations), microsatellite data detected three major genetic entities represented by O. bonariensis, O. perugiae-humensis and an admixture of populations belonging to O. argentinensis-perugiae respectively. Therefore, the star COI polytomy in the tree topology involving these taxa could be interpreted by several hypothetic scenarios such as the existence of shared ancestral polymorphisms, incomplete lineage sorting in a radiating speciation process and/or reticulation events. Present findings support that promiscuous and recent contact between incipient species sharing asymmetric gene flow exchanges, blurs taxa boundaries yielding complicated taxonomy and Management Units delimitation in silverside genus Odontesthes from SW Atlantic Ocean basins. Citation: Garcı ´a G, Rı ´os N, Gutie ´rrez V, Varela JG, Bouza Ferna ´ndez C, et al. (2014) Promiscuous Speciation with Gene Flow in Silverside Fish Genus Odontesthes (Atheriniformes, Atherinopsidae) from South Western Atlantic Ocean Basins. PLoS ONE 9(8): e104659. doi:10.1371/journal.pone.0104659 Editor: Valerio Ketmaier, Institute of Biochemistry and Biology, Germany Received May 29, 2014; Accepted July 11, 2014; Published August 15, 2014 Copyright: ß 2014 Garcia et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files. Funding: This research received financial support from the project Fondo Marı ´a Vin ˜ as_2009_1_2793 (FMV_2009_1_2793_Project) granted by the Agencia Nacional de Investigacio ´ n e Inovacio ´ n (ANII) of Uruguay. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * Email: ggarcia@fcien.edu.uy Introduction The New World presents multiple examples of atherinid species flocks or adaptive radiations arising from habitat transitions [1,2,3]. Silverside fish from South America constitute a exciting model to understand the scenario of fish speciation driven by divergent natural selection [1,2]. The silverside genus Odontesthes includes 20 nominal species [4] distributed in marine, estuarine and freshwater environments of tropical and temperate regions in South America [5]. Most Odontesthes species co-occur in the same habitats and they are characterized by a great morphological homogeneity [6]. The low morphological divergence between species and the high meristic plasticity within species together with the tendency of local populations to form micro-geographic habitat associations had led to complicated taxonomy among silverside taxa [7]. Among freshwater representative species, two of them O. bonariensis and O. hatcheri are endemic of rivers and lakes located east of the Andes in subtropical and temperate areas [8]. The distribution of these species was originally allopatric: O. hatcheri occuring in the South (Patagonia), whereas O. bonariensis occupying Central and Northern Argentina, South Brazil and Paraguay. The occurrence of the spontaneous hybridization between both species in a communal laboratory tank has been reported [9]. On the other hand, marine silversides generally have similar life history strategies, occurring in large numbers in semi-isolated populations in estuaries and coastal lagoons [10,11,12,1]. Ten species of Odontesthes are endemic of a chain of small shallow lakes spread along the South Western Atlantic Ocean coastal plain [13,14]. Among them, in Patos Lagoon estuary and its adjacent marine coastal area occurs O. argentinensis and O. incisa, whereas PLOS ONE | www.plosone.org 1 August 2014 | Volume 9 | Issue 8 | e104659