Biogeography of the neotropical freshwater stingrays (Myliobatiformes: Potamotrygoninae) reveals effects of continent‐scale paleogeographic change and drainage evolution

Abstract

Aim: Paleogeographic changes have had profound effects on the evolution and diversity of the Neotropical biota. However, the influence of marine incursions on the origin, diversification, and distribution of fishes is still incompletely understood. We investigate the biogeographical and chronological patterns of diversification for the marine-derived Neotropical freshwater stingrays (subfamily Potamotrygoninae) at a continental scale.Location: Neotropics, South America.Taxa: Neotropical freshwater stingrays. Subfamily Potamotrygoninae (Myliobatiformes: Chondrichthyes). Methods:We generated a time-calibrated phylogeny for 35 of the 38 valid species of Neotropical freshwater stingrays, from most of the major river basins of South America, using four genes. We used BEAST2 to determine the chronology of population and species divergence events, and "BioGeoBEARS" to infer historical biogeographic patterns. Results:The Potamotrygoninae originated during the early/middle Miocene in the upper Amazon region. We recover clades associated with particular geographic areas and detect a recurrent pattern of upper Amazon clades sister to clades in adjacent basins. The timing of dispersals from the upper Amazon to adjacent areas corresponds with the end of the Pebas wetlands. Lower Amazon and Shield associated taxa are relatively young. Main conclusions:We propose that the origin of the Neotropical freshwater stingrays is related to marine incursions that occurred during the Oligocene/Miocene. Subsequent diversification of Potamotrygoninae occurred in the Pebas wetland system in the upper Amazon with colonization of adjacent basins. These movements were generally unidirectional, with few lineages returning to the upper Amazon, and we speculate that ecological factors drove this pattern. We observed a burst of | 1407Fontenelle et al.

Western Amazon was a center of Neotropical fish dispersal, as evidenced by the continental-wide time-stratified biogeographic analysis of the hyper-diverseHypostomuscatfish

“…At a wider spatial scale, detailed fish biogeographic analyses revealed that the entire Amazon basin, taken as a single BHG region, was the center of origin and dispersal into other Neotropical basins for the catfish subfamily Hypoptopomatinae (Chiachio, Oliveira, & Montoya-Burgos, 2008) and for the characiform genus Triportheus (Mariguela et al, 2016). Recently, a more refined biogeographic reconstruction also revealed the Western Amazon as the origin of marine-derived Neotropical freshwater stingrays (Fontenelle et al, 2021), yet the marine origin of this group may not be representative of other primary freshwater lineages. Therefore, our results bring new evidence in support of the hypothesis that Western Amazon was a primary center of freshwater fish origination.…”

“…The increasing knowledge about the historical modifications of Neotropical basins offers a timely opportunity to infer freshwater fish ancestral distributions and dispersal routes integrating the changes in watershed configurations through time, but this has been explicitly explored in surprisingly few biogeographic reconstructions of Neotropical fish (e.g. Fontenelle et al, 2021;Wendt, Silva, Malabarba, & Carvalho, 2019). To take advantage of the accumulated knowledge of basins connectivity through time, it is important that reconstructions use the finest possible biogeographic partitions of the hydrological systems, but this implies extensive knowledge about species distribution as well as the inclusion of a comprehensive taxonomic sampling.…”

“…As for fish, the Amazon Basin is the biogeographic core of the Neotropical system, and by far the most species-rich river network (J. S. Albert & Reis, 2011;Böhlke et al, 1978), with more than 7'000 species estimated (Lévêque, Oberdorff, Paugy, Stiassny, & Tedesco, 2008;Reis, Kullander, & Ferraris, 2003). The Amazon Basin has also been suggested to be a cradle of fish diversity, an area where species have originated and immigrated into other basins (J. S. Albert & Reis, 2011;James S. Albert et al, 2018;Fontenelle, Marques, Kolmann, & Lovejoy, 2021;Oberdorff et al, 2019), but this hypothesis still needs further testing. Whether the many and profound landscape changes that occurred in the Amazon Basin were instrumental in fostering the origination, dispersal and diversification of modern Neotropical fish lineages is an assumption that needs to be verified too.…”

Biogeography of curimatid fishes reveals multiple lowland–upland river transitions and differential diversification in the Neotropics (Teleostei, Curimatidae)

“…Armored suckermouth catfishes (Hypostominae) originated during the Eocene in the POA, dispersed to uplands of the Paraná river basin, and experienced accelerated rates of speciation and ecomorphological diversification during the Miocene (Cardoso et al, 2012 ; Silva et al, 2016 ). Species of the characiform clades Salminus (Bryconidae) and Schizodon (Anostomidae) and freshwater stingrays (Potamotrygoninae) represent other examples of dispersal from the Proto–Amazon to upland basins of the Brazilian and Guiana Shield, such as Araguaia–Tocantins, La Plata, São Francisco, Parnaíba, and Xingu, among others (Fontenelle et al, 2021 ; Machado et al, 2018 ; Ramirez et al, 2020 ). In curimatids, lowland river captures between the Amazon/Paraguay and the Amazon/Tocantins (Figure 3 , Figure S1 ) facilitated the dispersal of taxa especially into the Brazilian Shield, although evidence for biotic or abiotic factors driving the upland colonization is not yet available, nor why those ancient lineages dispersed to uplands only in the Cenozoic.…”

“…Colors of the branch outlines (blue to red) indicate the distribution of net diversification rates along the topology (<0.001-0.26 (Fontenelle et al, 2021;Machado et al, 2018;Ramirez et al, 2020). In curimatids, lowland river captures between the Amazon/Paraguay and the Amazon/Tocantins (Figure 3, Figure S1) facilitated the dispersal of taxa especially into the Brazilian Shield, although evidence for biotic or abiotic factors driving the upland colonization is not yet available, nor why those ancient lineages dispersed to uplands only in the Cenozoic.…”