Ancient female philopatry, asymmetric male gene flow, and synchronous population expansion support the influence of climatic oscillations on the evolution of South American sea lion (Otaria flavescens)

The South American sea lion (Otaria flavescens) is widely distributed along the southern Atlantic and Pacific coasts of South America with a history of significant commercial exploitation. We aimed to evaluate the population genetic structure and the evolutionary history of South American sea lion along its distribution by analyses of mitochondrial DNA (mtDNA) and 10 nuclear microsatellites loci. We analyzed 147 sequences of mtDNA control region and genotyped 111 individuals of South American sea lion for 10 microsatellite loci, representing six populations (Peru, Northern Chile, Southern Chile, Uruguay (Brazil), Argentina and Falkland (Malvinas) Islands) and covering the entire distribution of the species. The mtDNA phylogeny shows that haplotypes from the two oceans comprise two very divergent clades as observed in previous studies, suggesting a long period (> 1 million years) of low inter-oceanic female gene flow. Bayesian analysis of bi-parental genetic diversity supports significant (but less pronounced than mitochondrial) genetic structure between Pacific and Atlantic populations, although also suggested some inter-oceanic gene flow mediated by males. Higher male migration rates were found in the intra-oceanic population comparisons, supporting very high female philopatry in the species. Demographic analyses showed that populations from both oceans went through a large population expansion similar to 10,000 years ago, suggesting a very similar influence of historical environmental factors, such as the last glacial cycle, on both regions. Our results support the proposition that the Pacific and Atlantic populations of the South American sea lion should be considered distinct evolutionarily significant units, with at least two managements units in each ocean.Brazilian National Council for Scientific and Technological Development, CNPq 484172-2010-7, 479199-2010-8, 303813-2011-3, 148039-2011-1, 307920-2013-5, 308650-2014-0 / Mohamed bin Zayed Species Conservation Fund, 0925516 / Amneville Zoo / Argentinean Agenda Nacional de Promocion Cientifica y Tecnologica ANPCyT-PICT 33934 / Bilbao Vizcaya Argentaria Bank, BBVA-BIOCON08-194-09 / Programa de Investigacion Marina de Excelencia (PIMEX-Nueva Aldea) of the Faculty of Natural and Oceanographic Sciences of the University of Concepcion, GMS 2010/22 / Celulosa Arauco / Constitucion S.A. / Fondo Nacional de Desarrollo Cientifico y Tecnologico (Fondecyt), 11110081 / Office of Direccion de Investigacion y Desarrollo, Universidad Austral de Chile, D-2004-7, D-2005-15, S-2006-50, S-201319 Fondecyt, 3120100 / Comision Nacional de Investigacion Cientifica y Tecnologica (CONICYT)-Postdoctoral FONDECYT Program, 314051