Marine incursions, cryptic species and ecological diversification in Amazonia: the biogeographic history of the croaker genusPlagioscion(Sciaenidae)

Abstract

AbstractAim We propose a phylogenetic hypothesis for the marine‐derived sciaenid genusPlagioscionin the context of geomorphology and adaptation to freshwaters of South America, and assess the extent to which contemporary freshwater hydrochemical gradients influence diversification within a widely distributedPlagioscionspecies,Plagioscion squamosissimus.Location Amazon Basin and South America.Methods Using nuclear and mitochondrial DNA sequence data, phylogenetic analyses were conducted on the five nominalPlagioscionspecies, together with representatives fromPachyurusandPachypops, using character and model‐based methods. Genealogical relationships and population genetic structure of 152P. squamosissimusspecimens sampled from the five major rivers and three hydrochemical settings/‘colours’ (i.e. white, black and clear water) of the Amazon Basin were assessed.Results Phylogenetic analyses support the monophyly ofPlagioscionin South America and identify two putative cryptic species ofPlagioscion. Divergence estimates suggest that thePlagioscionancestor invaded South America via a northern route during the late Oligocene to early Miocene. WithinP. squamosissimusa strong association of haplotype and water colour was observed, together with significant population structure detected between water colours.Main conclusions Our analyses ofPlagioscionare consistent with a biogeographic scenario of early Miocene marine incursions into South America. Based on our phylogenetic results, the fossil record, geomorphological history and distributional data of extantPlagioscionspecies, we propose that marine incursions into western Venezuela between the late Oligocene and early Miocene were responsible for the adaptation to freshwaters inPlagioscionspecies. Following the termination of the marine incursions during the late Miocene and the establishment of the modern Amazon River,Plagioscionexperienced a rapid diversification.Plagioscion squamosissimusarose during that time. The formation of the Amazon River probably facilitated population and range expansions for this species. Further, the large‐scale hydrochemical gradients within the Amazon Basin appear to be acting as ecological barriers maintaining population discontinuities inP. squamosissimuseven in the face of gene flow. Our results highlight the importance of divergent natural selection through time in the generation and maintenance of sciaenid diversity in Amazonia.