Drainage rearrangements and in situ diversification of an endemic freshwater fish genus from north‐eastern Brazilian rivers

Abstract

Abstract Drainage rearrangements, either headwater captures or coastal paleodrainages formed when sea level was low, are often invoked to explain connectivity and isolation among fish populations. Unravelling these events is crucial for understanding the evolutionary processes that have shaped the genetic diversity and differentiation in freshwater fishes, which is especially relevant in regions with high endemism and species richness. Here, we analyse mitochondrial (cytochrome c oxidase subunit I) and genomic (restriction site‐associated DNA) data to test the putative effects of the current configuration of basins and historical drainage rearrangements on the genetic structuring of a characid fish (Nematocharax) endemic to a largely overlooked Neotropical freshwater ecoregion—the North‐eastern Mata Atlantica. Bathymetric and geomorphological data were also used to generate hypotheses for two potential routes of dispersal (headwater captures and coastal paleodrainages). We found that the divergence between lineages from the highlands of the Brazilian shield and the lowlands occurred during the Mio‐Pliocene (i.e., divergence between Nematocharax varii and Nematocharax venustus), followed by divergence events within N. venustus in lowland basins during the Pleistocene. The general distribution of genetic variation in N. venustus seems to reflect the current configuration of basins, suggesting long‐term isolation, but a subset of the inferred drainage rearrangements have facilitated movement among these catchments, which is supported by both mitochondrial DNA and genomic data. Our results suggest that the North‐eastern Mata Atlantica river basins have had their own independent histories, except for some past temporary connections that allowed dispersal events and multiple independent colonisation of basins, as seen in the Contas and Cachoeira river systems. Estimating when and where connections between river basins may have occurred is fundamental to understand the role of different historical processes structuring divergence in freshwater fish species.