Abstract

Rhamdia quelen, a Neotropical fish with hybridization between highly divergent mitochondrial DNA (mtDNA) lineages, represents an interesting evolutionary model. Previous studies suggested that there might be demographic differences between coastal lagoons and riverine environments, as well as divergent populations that could be reproductively isolated. Here, we investigated the genetic diversity pattern of this taxon in the Southern Neotropical Basin system that includes the La Plata Basin, Patos-Merin lagoon basin and the coastal lagoons draining to the SW Atlantic Ocean, through a population genomics approach using 2b-RAD-sequencing-derived single nucleotide polymorphisms (SNPs). The genomic scan identified selection footprints associated with divergence and suggested local adaptation environmental drivers. Two major genomic clusters latitudinally distributed in the Northern and Southern basins were identified, along with consistent signatures of divergent selection between them. Population structure based on the whole set of loci and on the presumptive neutral vs. adaptive loci showed deep genomic divergence between the two major clusters. Annotation of the most consistent SNPs under divergent selection revealed some interesting candidate genes for further functional studies. Moreover, signals of adaptation to a coastal lagoon environment mediated by purifying selection were found. These new insights provide a better understanding of the complex evolutionary history of R. quelen in the southernmost basin of the Neotropical region.

Highlights

  • The high Neotropical diversity of freshwater fishes is mostly explained by the hydrogeological history, paleontological evolution and climatic change of that region [1]

  • Populations analyzed were selected according to previous microsatellite and mitochondrial DNA (mtDNA) genetic diversity patterns [14,17] (Figure 1; Table 1), namely, the Uruguay River basin (UR): Cuareim River (1-UR-CR), Arapey River (2-UR-AR) and Queguay River (3-UR-QR); the Negro River basin (NR): Rincón del Bonete dam (4-NR-RB); the La Plata River basin (LP): Sauce Lagoon (5-LP-SL); the SW Atlantic Ocean coastal basin (AO): Blanca Lagoon (6-AO-BL), Rocha Lagoon (7-AO-RL) and Castillos Lagoon (8-AO-CL); and the Merin Lagoon basin (ML): Quebrada de los Cuervos (9-ML-QC)

  • In order to identify the different R. quelen mtDNA lineages, a total of 22 new partial sequences of cytb were obtained in this study (GenBank Accession numbers: MK511194–MK511214 and MK511219; Supplementary Files SI and SII)

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Summary

Introduction

The high Neotropical diversity of freshwater fishes is mostly explained by the hydrogeological history, paleontological evolution and climatic change of that region [1]. Over the last 120 million years, South America has experienced wide marine transgressions and regressions as a result of Pleistocene glaciations Their influence on the hydrological pattern of the region has been extensive, given that a large portion of South America is characterized by low elevation and low topographic relief [2,3]. In the first systematic revision of the Rhamdia genus, more than 100 species were synonymized, 46 of which were synonymized with R. quelen [13] Previous studies on this species based on mitochondrial DNA (mtDNA) data suggested different mtDNA lineages [11,14,15], while other authors provided morphological evidence supporting sister species previously included in R. quelen [10,16]. Five R. quelen cytb mtDNA lineages (Rq2, Rq4, Rq5a, Rq5b and Rq6) have been identified in the basin system encompassing the La Plata Basin, Patos-Merin lagoon Basin, as well as rivers and lagoons draining to the SW Atlantic Ocean

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