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Breathing Air and Living Underwater: Molecular Evolution of Genes Related to Antioxidant Response in Cetaceans and Pinnipeds

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Abstract

Cetaceans and pinnipeds are lineages of mammals that have independently returned to the aquatic environment, acquiring varying degrees of dependence on it while sharing adaptations for underwater living. Here, we focused on one critical adaptation from both groups, their ability to withstand the ischemia and reperfusion experienced during apnea diving, which can lead to the production of reactive oxygen species (ROS) and subsequent oxidative damage. Previous studies have shown that cetaceans and pinnipeds possess efficient antioxidant enzymes that protect against ROS. In this study, we investigated the molecular evolution of key antioxidant enzyme genes (CAT, GPX3, GSR, PRDX1, PRDX3, and SOD1) and the ROS-producing gene XDH, in cetaceans and pinnipeds lineages. We used the ratio of non-synonymous (dN) to synonymous (dS) substitutions as a measure to identify signatures of adaptive molecular evolution in these genes within and between the two lineages. Additionally, we performed protein modeling and variant impact analyzes to assess the functional consequences of observed mutations. Our findings revealed distinct selective regimes between aquatic and terrestrial mammals in five of the examined genes, including divergences within cetacean and pinniped lineages, between ancestral and recent lineages and between crowns groups. We identified specific sites under positive selection unique to Cetacea and Pinnipedia, with one site showing evidence of convergent evolution in species known for their long and deep-diving capacities. Notably, many sites under adaptive selection exhibited radical changes in amino acid properties, with some being damaging mutations in human variations, but with no apparent detrimental impacts on aquatic mammals. In conclusion, our study provides insights into the adaptive changes that have occurred in the antioxidant systems of aquatic mammals throughout their evolutionary history. We observed both distinctive features within each group of Cetacea and Pinnipedia and instances of convergence. These findings highlight the dynamic nature of the antioxidant system in response to challenges of the aquatic environment and provide a foundation for further investigations into the molecular mechanisms underlying these adaptations.

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Acknowledgements

This study was funded by the São Paulo Research Foundation (FAPESP) (2020/03588-2). LM was funded by Nova Scotia Graduate Scholarship, NSERC Discovery Grant and Biology Graduate A- Fellowship. AP was funded by FAPESP training program (2021/03325-4), FAS was funded by Coordination for the Improvement of Higher Education Personnel - Brazil (CAPES) master’s scholarship, and ER by FAPESP doctoral scholarship (2018/01236-1). We are grateful to the scientists that made available the gene sequences used in this study.

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  1. Laboratório de Genômica Evolutiva, Departamento de Genética, Evolução, Microbiologia e Imunologia, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, Brazil

    Giovanna Selleghin-Veiga, Letícia Magpali, Agnello Picorelli, Felipe A. Silva, Elisa Ramos & Mariana F. Nery

  2. Department of Biology, Dalhousie University, Halifax, NS, Canada

    Letícia Magpali

  3. Zoological Institute, Department of Environmental Sciences, University of Basel, Basel, Switzerland

    Elisa Ramos

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  1. Giovanna Selleghin-Veiga
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  4. Felipe A. Silva
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Contributions

G.S.V. and M.F.N. conceived the research hypothesis. G.S.V., L.M., A.P., and F.A.S performed the data analysis The manuscript was written by G.S.V. and previous versions were reviewed by E.R., L.M. and M.F.N. All authors read and approved the final manuscript.

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Correspondence to Giovanna Selleghin-Veiga or Mariana F. Nery.

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Selleghin-Veiga, G., Magpali, L., Picorelli, A. et al. Breathing Air and Living Underwater: Molecular Evolution of Genes Related to Antioxidant Response in Cetaceans and Pinnipeds. J Mol Evol (2024). https://doi.org/10.1007/s00239-024-10170-3

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