Do multiple karyomorphs and population genetics of freshwater darter characines (Apareiodon affinis) indicate chromosomal speciation?

Abstract

The role of chromosomal rearrangements in the evolution of species is controversial, and the term chromosomal speciation results from the observation that heterokaryotypes are often infertile. Parodontidae species (a Neotropical fish family) are distinguished only by a few subtle diagnostic morphological characteristics, leading to uncertainty over the inter-relationships and monophyly of the genera. Apareiodon affinis was originally described in the scientific literature as a species isolated from the la Plata river (Buenos Aires, Argentina) and subsequently found in all tributaries of the Rio Paraná basin. In this study, we compared the karyotypic organization, the number of cusps in premaxillary teeth and, nucleotide divergence using DNA barcode for six different demes identified morphologically as A. affinis from different hydrographic subsystems in the Paraná basin (upper Paraná − three demes, Paraguay, Cuiabá, and Uruguay rivers). Cytogenetic data revealed chromosomal differences among the A. affinis demes studied. Chromosomal rearrangements (e.g., translocations, pericentric inversion, and/or, centromere repositioning), differentiation of the ZZ/ZW1W2 multiple sex chromosome system, and accumulation of DNA repeats were proposed to explain the cytogenetic divergence among A. affinis demes. In addition, despite the absence of morphological variation, the molecular analysis demonstrates gene flow restriction among Paraguay, Cuiabá, and Uruguay A. affinis demes and, genetic isolation between upper Rio Paraná basin population from those of the lower Rio Paraná basin demes. Our results demonstrated that different A. affinis karyomorphs have differentiated in subsystems in the Paraná basin and, parapatric populations accumulate chromosomal divergences, supporting the hypothesis of an emerging younger species and/or chromosomal speciation in progress.