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Evidence of positive selection suggests possible role of aquaporins in the water-to-land transition of mudskippers

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Abstract

Aquaporins are integral membrane proteins that exchange water and small solutes. They played an important role in the colonisation of terrestrial environments by tetrapod ancestors via the appearance of three exclusive paralogs. Like early tetrapods, mudskippers represent an independent case of amphibious lifestyle evolution that is unparalleled by other extant fish groups. Given this lifestyle parallelism and that aquaporins were relevant for tetrapod terrestrialisation, this study examines the aquaporins in mudskippers to investigate whether similar changes in aquaporins could have possibly occurred during their water-to-land transition. We have catalogued aquaporin genes in four mudskipper genomes and studied their diversity and molecular evolution (including detection of positive selection) in a broad phylogenetic context of vertebrates. Our genomic screening returned 55 aquaporin genes for mudskippers (none of them constituting novel paralogs) that can be assigned to 10 different known classes. We detected signatures of positive selection in AQP10a and AQP11b in mudskippers (both the entire clade and the clade containing the most terrestrial species, implying different evolutionary times). This suggests possible alteration of the molecular function of such paralogs caused by changes at specific protein sequence positions, some of them located in relatively close proximity to parts of the molecule involved in pore formation and substrate selectivity. Given the importance of aquaporins for osmotic regulation in fishes, it might be possible that these selective changes (perhaps allowing permeability to new solutes) could have played a role during the adaptation of mudskippers to an amphibious lifestyle.

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Acknowledgments

We thank Antonio González-Martín, Aurora García-Dorado, and two anonymous reviewers for insightful comments on an earlier version of this manuscript. Some computational analyses were performed at the Altamira HPC cluster of the Institute of Physics of Cantabria (IFCA-CSIC), which is part of the Spanish Supercomputing Network.

Funding

D.S.M was funded by grants RYC-2011-09321 and CGL2012-40082 from the Ministry of Economy and Competitiveness of Spain. M.T was sponsored by predoctoral fellowship BES-2013-062723 of the Ministry of Economy and Competitiveness of Spain.

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  1. María Torres-Sánchez

    Present address: Department of Neuroscience, Spinal Cord and Brain Injury Research Center & Ambystoma Genetic Stock Center, University of Kentucky, Lexington, KY, 40536, USA

Authors and Affiliations

  1. Department of Biodiversity, Ecology, and Evolution, Complutense University of Madrid, José Antonio Novais 12, 28040, Madrid, Spain

    Héctor Lorente-Martínez, Ainhoa Agorreta, María Torres-Sánchez & Diego San Mauro

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  1. Héctor Lorente-Martínez
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  2. Ainhoa Agorreta
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  3. María Torres-Sánchez
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  4. Diego San Mauro
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Corresponding author

Correspondence to Ainhoa Agorreta.

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Lorente-Martínez, H., Agorreta, A., Torres-Sánchez, M. et al. Evidence of positive selection suggests possible role of aquaporins in the water-to-land transition of mudskippers. Org Divers Evol 18, 499–514 (2018). https://doi.org/10.1007/s13127-018-0382-6

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