Promiscuous Speciation with Gene Flow in Silverside Fish Genus Odontesthes (Atheriniformes, Atherinopsidae) from South Western Atlantic Ocean Basins

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.

Biogeography, habitat transitions and hybridization in a radiation of South American silverside fishes revealed by mitochondrial and genomic RAD data

“…The pattern of evolution of freshwater species from marine ancestors implied by the RAD phylogeny does not support a previously proposed ecological model of speciation involving divergence with gene flow in southwestern Atlantic populations (Beheregaray & Sunnucks, ; Beheregaray et al, ; García et al, ). According to this model, marine populations of O. argentinensis entering the coastal lagoons and brackish estuaries along the coastal plain of Uruguay (Mirim), southern Brazil (dos Patos, Tramandaí) and Argentina (Mar Chiquita) gave rise repeatedly to phenotypically variable species flocks, similar to well‐documented marine‐to‐freshwater transitions in marine stickleback fishes in Asia, Europe and North America (Bell & Foster, ).…”

“…Until now, morphological and mtDNA hypotheses have been the primary resource available to understand the evolution South American silversides. Previous studies (Campanella et al, ; García et al, ; González‐Castro et al, , ) failed to separate many nominal species, especially in the Atlantic Basin (Figure c,d), and to confidently establish phylogenetic relationships in the Odontesthes argentinensis species‐group. In contrast, genomic ddRAD data show strong support for the current taxonomy with a few exceptions and confidently establish phylogenetic relationships.…”

“…Secondary contact between the established freshwater species and their marine relatives seems to be frequent in brackish and estuarine habitats where environmental gradients are gradual and form extensive habitats, enabling the formation of hybrids exhibiting intermediate phenotypes. Lack of genetic differentiation among species in mtDNA markers may be the consequence of hybridization, as is probably the case with the O. argentinensis species‐group (García et al, ). The numerous estuaries and coastal lagoons that have formed on the southwestern Atlantic coastline from northern Argentina to southern Brazil provide ample contact zones for marine and freshwater species that could homogenize mtDNA, with many of the freshwater species in the O. argentinensis species‐group being sympatric as well.…”

“…Phylogenetic relationships proposed using morphology fail to place O. argentinensis as the sister‐group to the O. perugiae complex (Dyer, , ; Figure c), contradicting the hypothesis of a marine‐derived origin for this group. Furthermore, published mtDNA genealogies (García et al, ; González‐Castro et al, , ; Heras & Roldán, ) support a clade that includes the marine species O. argentinensis and all freshwater species endemic to the La Plata River Basin and the coastal lagoons of Uruguay and southern Brazil (e.g., the “ O. perugiae group” plus O. bonariensis , O. retropinnis and O. humensis ), but mtDNA consistently fails to establish species boundaries among these taxa or their phylogenetic relationships, potentially due to a history of gene flow among species (García et al, ) and limited information content of mitochondrial markers.…”

“…Hybridization between marine and incipient or established freshwater species has been proposed to be widespread among Odontesthes species in the southwestern Atlantic Basin (García et al, ; González‐Castro et al, , ). The coastline from northern Argentina to southern Brazil has many large estuaries and floodplains, such as the La Plata estuary, Mar Chiquita Lagoon and Dos Patos Lagoon, creating potential secondary contact zones between marine and freshwater species.…”