Molecular Data Reveal Multiple Lineages in Piranhas of the Genus Pygocentrus (Teleostei, Characiformes)

Abstract

Carnivorous piranhas are distributed in four serrasalmid genera including Pygocentrus, which inhabit major river basins of South America. While P. cariba and P. piraya are endemics of the Orinoco and São Francisco basins, respectively, P. nattereri is widely distributed across the Amazonas, Essequibo, lower Paraná, Paraguay, and coastal rivers of northeastern Brazil, with recent records of introductions in Asia. Few studies have focused on the genetic diversity and systematics of Pygocentrus and the putative presence of additional species within P. nattereri has never been the subject of a detailed molecular study. Here we aimed to delimit species of Pygocentrus, test the phylogeographic structure of P. nattereri, and access the origin of introduced specimens of P. nattereri in Asia. Phylogenetic analyses based on a mitochondrial dataset involving maximum-likelihood tree reconstruction, genetic distances, Bayesian analysis, three delimitation approaches, and haplotype analysis corroborate the morphological hypothesis of the occurrence of three species of Pygocentrus. However, we provide here strong evidence that P. nattereri contains at least five phylogeographically-structured lineages in the Amazonas, Guaporé (type locality), Itapecuru, Paraná/Paraguay, and Tocantins/Araguaia river basins. We finally found that the introduced specimens in Asia consistently descend from the lineage of P. nattereri from the main Rio Amazonas. These results contribute to future research aimed to detect morphological variation that may occur in those genetic lineages of Pygocentrus.

Molecular characterization and genetic relationships of seven piranha species of the genera Serrasalmus and Pygocentrus (Characiformes: Serrasalmidae) from Paraná-Paraguay, São Francisco and Tocantins River basins in Brazil

“…The genetic differentiation between P. nattereri and P. piraya was evident. Although the value of p-distance detected between the species were low (2.48%), this is an expected result, since the speciation event leading to P. nattereri and P. piraya occurred recently, during the last 2.6 ± 0.2 Ma (Mateussi et al, 2019). We also detected high genetic variability within P. nattereri, as previously reported by Mateussi et al (2019) and Luz et al (2015).…”

“…Evolutionary relationships among species of piranhas have been the subject of several publications with morphological (Machado-Allison, 1983), cytological (Nakayama et al, 2002(Nakayama et al, , 2012, parasitological (Van Every and Kritsky, 1992) and molecular markers (Ortí et al, 1996(Ortí et al, , 2008Freeman et al, 2007;Hubert et al, 2007;Thompson et al, 2014;Machado et al, 2018;Mateussi et al, 2019). Morphological and molecular approaches agree with the hypothesis that the genera of piranhas Pygopristis, Pygocentrus, Pristobrycon and Serrasalmus together with Catoprion, represent a monophyletic unit of the family Serrasalmidae.…”

“…However, all species delimitation analysis recovered two mtDNA lineages among P. nattereri specimens (Figure 3). Similarly, Mateussi et al (2019) detected at least five lineages of P. nattereri in five hydrographic river basins (Amazonas, Guaporé, Itapecuru, Paraná-Paraguay and Tocantins-Araguaia). The authors also concluded that these lineages can be potentially sibling species, a special case of cryptic species, representing the P. nattereri species complex (Mateussi et al, 2019).…”

“…Similarly, Mateussi et al (2019) detected at least five lineages of P. nattereri in five hydrographic river basins (Amazonas, Guaporé, Itapecuru, Paraná-Paraguay and Tocantins-Araguaia). The authors also concluded that these lineages can be potentially sibling species, a special case of cryptic species, representing the P. nattereri species complex (Mateussi et al, 2019). Finally, the monophyletic condition of P. nattereri confirmed in the studies of Fink (1993) and Ortí et al (1996) was also observed in our analysis (Figure 2).…”

Molecular delimitation and taxonomic revision of the wimple piranha Catoprion (Characiformes: Serrasalmidae) with the description of a new species

“…Traditionally, a 2% cut‐off of interspecific distance has been used, at least initially, in species delimitation studies based on the K2P genetic distance (Carvalho et al ., 2011; Pereira et al ., 2013). This mean value is concordant with mean values found in other serrasalmids, e.g ., 1.4%–9.0% in Mylossoma (Mateussi et al ., 2016), 2.7%–6.2% in Pygocentrus (Mateussi et al ., 2019) and 1.6%–9.3% in Tometes (Andrade et al ., 2017).…”