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Signatures of positive selection in the mitochondrial genome of neotropical freshwater stingrays provide clues about the transition from saltwater to freshwater environment

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Abstract

Neotropical freshwater stingrays (subfamily Potamotrygoninae) are carnivorous bottom feeder batoids widely distributed in most river basins of South America. They represent the unique extant group of elasmobranchs that evolved to live exclusively in freshwater environments. These species are exploited either by commercial fisheries (e.g., for food or ornamental industry) or by indigenous communities allocated along with their natural range. Restrictive life history characteristics coupled with habitat degradation make Potamotrygoninae species highly vulnerable to human impacts and highlight the necessity of studies to inform basic biological aspects, from ecology to genetics, to guide their conservation and clarify the molecular basis of adaptation to the freshwater environment. We used available and newly assembled Potamotrygon spp. mitogenomes to perform a comparative investigation of their molecular evolution. A phylogenetic estimation using the mitogenome of Potamotrygon falkneri and other Elasmobranchii supports monophyly for Potamotrygonidae and indicates a close relationship to Dasyatidae. A synteny analysis comprising 3 Potamotrygon and other 51 batoids revealed a highly conserved mitogenomic context. We detected various amino acid sites under positive selection exclusively in Potamotrygon spp., within the sequences of ND4, ND5, ND6, and COXII genes. Positively selected mutational events in key genes of energetic metabolism may be related to the physiological adaptation of Potamotrygon spp. during the ancient incursion into freshwater. This broad comparative mitogenomic study provides novel insights into the evolutionary history of neotropical freshwater stingrays and their relatives and stands out as a valuable resource to aid in current and future research on elasmobranch molecular evolution.

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Data availability

The mitogenome of P. falkneri is available at NCBI GenBank database under the accession number MZ203140. The RNA-seq dataset used to assemble the mitogenome of P. falkneri is available at NCBI SRA database under the accession number SRR14546100.

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Acknowledgements

The authors thank Carlos T. Moraes for precious discussion, Helder E. da Silva for support during field work and Domingos Garrone-Neto for the P. falkneri picture used in Fig. 1.

Funding

This work received support from ProPe-UNESP (First Projects Special Program) and São Paulo Research Foundation (FAPESP) (grants 2012/02540-0 and 2013/06864-7). DP is recipient of CNPq productivity scholarship (315139/2020-0).

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Authors and Affiliations

  1. Laboratório de Toxinologia Aplicada, CeTICS, Instituto Butantan, São Paulo, SP, Brazil

    P. G. Nachtigall

  2. Laboratório de Pesquisas Paleontológicas (LPP), CCBN, Universidade Federal do Acre (UFAC), Rio Branco, AC, Brazil

    T. S. Loboda

  3. Laboratório Genômica e Evolução Molecular (LGEM), Departamento de Ciências Químicas e Biológicas, Instituto de Biociências de Botucatu, Universidade Estadual Paulista Júlio de Mesquita Filho (UNESP), Botucatu, SP, Brazil

    D. Pinhal

  4. Departamento Acadêmico de Ensino (DAENS), Universidade Tecnológica Federal do Paraná (UTFPR), Ponta Grossa, PR, Brazil

    T. S. Loboda

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PGN and DP conceived and designed the experiments. DP collected and processed samples and provided reagents and financial resources. PGN performed all bioinformatics analysis. TSL reviewed the taxonomy of Batoidea species. PGN and TSL wrote the manuscript draft. PGN, TSL, and DP critically edited the final manuscript. All authors read and approved the final manuscript.

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Correspondence to D. Pinhal.

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The specimens of P. falkneri used in the present study were handled and collected in accordance with the guidelines of the Brazilian College for Animal Experimentation (COBEA; http://www.sbcal.org.br/), the Ethics Committee in Animal Use (CEUA) of UNESP, and recorded in the Genetic Heritage Management Council system (SisGen/CGen/MMA; access number 5936E9).

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Nachtigall, P.G., Loboda, T.S. & Pinhal, D. Signatures of positive selection in the mitochondrial genome of neotropical freshwater stingrays provide clues about the transition from saltwater to freshwater environment. Mol Genet Genomics 298, 229–241 (2023). https://doi.org/10.1007/s00438-022-01977-0

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