Advertisement

Organisms Diversity & Evolution

, Volume 18, Issue 4, pp 499–514 | Cite as

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

  • Héctor Lorente-Martínez
  • Ainhoa Agorreta
  • María Torres-Sánchez
  • Diego San Mauro
Original Article

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.

Keywords

Amphibious lifestyle Aquaporin Molecular evolution Mudskipper Positive selection 

Notes

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 information

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.

Supplementary material

13127_2018_382_MOESM1_ESM.pdf (6.8 mb)
ESM 1 (PDF 6.77 MB)
13127_2018_382_MOESM2_ESM.fas (154 kb)
ESM 2 (FAS 153 kb)
13127_2018_382_MOESM3_ESM.fas (46 kb)
ESM 3 (FAS 46 kb)
13127_2018_382_MOESM4_ESM.fas (17 kb)
ESM 4 (FAS 16 kb)

References

  1. Abascal, F., Zardoya, R., & Posada, D. (2005). ProtTest: selection of best-fit models of protein evolution what can I use ProtTest for ? – introduction the program: using ProtTest. Bioinformatics, 21, 1–17.Google Scholar
  2. Abascal, F., Zardoya, R., & Telford, M. J. (2010). TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Research, 38, 7–13.Google Scholar
  3. Abascal, F., Irisarri, I., & Zardoya, R. (2014). Diversity and evolution of membrane intrinsic proteins. Biochimica et Biophysica Acta - General Subjects, 1840, 1468–1481.Google Scholar
  4. Agorreta, A., San Mauro, D., Schliewen, U., van Tassell, J. L., Kovačić, M., Zardoya, R., & Rüber, L. (2013). Molecular phylogenetics of Gobioidei and phylogenetic placement of European gobies. Molecular Phylogenetics and Evolution, 69, 619–633.PubMedGoogle Scholar
  5. Agre, P., & Kozono, D. (2003). Aquaporin water channels: molecular mechanisms for human diseases. FEBS Letters, 555, 72–78.PubMedGoogle Scholar
  6. Agre, P., Preston, G. M., Smith, B. L., Jung, J. S., Raina, S., Moon, C., Guggino, W. B., & Nielsen, S. (1993). Aquaporin CHIP: the archetypal molecular water channel. The American Journal of Physiology, 265, F463–F476.PubMedGoogle Scholar
  7. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.PubMedGoogle Scholar
  8. Anderberg HI, Danielson JÅH, Johanson U (2011) Algal MIPs, high diversity and conserved motifs. BMC Evolutionary Biology 11. Google Scholar
  9. Anisimova, M., & Yang, Z. (2007). Multiple hypothesis testing to detect lineages under positive selection that affects only a few sites. Molecular Biology and Evolution, 24, 1219–1228.PubMedGoogle Scholar
  10. Apweiler, R. (2009). The universal protein resource (UniProt) in 2010. Nucleic Acids Research, 38, D142–D148.Google Scholar
  11. Benson, D. A., Cavanaugh, M., Clark, K., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J., & Sayers, E. W. (2013). GenBank. Nucleic Acids Research, 41, D36–D42.PubMedGoogle Scholar
  12. Broekhuyse, R. M., Kuhlmann, E. D., & Stols, A. L. H. (1976). Lens membranes II. Isolation and characterization of the main intrinsic polypeptide (MIP) of bovine lens fiber membranes. Experimental Eye Research, 23, 365–371.PubMedGoogle Scholar
  13. Carrol, R. L. (2001). The origin and early adaptation of terrestrial vertebrates. Journal of Paleontology, 75, 1202–1213.Google Scholar
  14. Cerdà, J., & Finn, R. N. (2010). Piscine aquaporins: an overview of recent advances. Journal of Experimental Zoology. Part A, Ecological Genetics and Physiology, 313 A, 623–650.Google Scholar
  15. Cheng, A., van Hoek, A. N., Yeager, M., et al. (1997). Three-dimensional organization of a human water channel. Nature, 387, 627–630.PubMedGoogle Scholar
  16. Chew, S. F., Sim, M. Y., Phua, Z. C., et al. (2007). Active ammonia excretion in the giant mudskipper, Periophthalmodon schlosseri (Pallas), during emersion. Journal of Experimental Zoology. Part A, Ecological Genetics and Physiology, 307, 357–369.PubMedGoogle Scholar
  17. Church, R. L., & Wang, J. (1992). Assignment of the lens intrinsic membrane protein MP19 structural gene to human chromosome 19. Current Eye Research, 11, 421–424.PubMedGoogle Scholar
  18. Connolly, D. L., Shanahan, C. M., & Weissberg, P. L. (1998). The aquaporins. A family of water channel proteins. The International Journal of Biochemistry & Cell Biology, 30, 169–172.Google Scholar
  19. Crow, K. D., Stadler, P. F., Lynch, V. J., Amemiya, C., & Wagner, G. P. (2006). The “fish-specific” Hox cluster duplication is coincident with the origin of teleosts. Molecular Biology and Evolution, 23, 121–136.PubMedGoogle Scholar
  20. Cuvier, G., Valenciennes, A. (1837). Histoire naturelle des poissons. Tome. Chez F.G. Levrault, Paris 12:508Google Scholar
  21. Dabruzzi, T. F., Wygoda, M. L., Wright, J. E., Eme, J., & Bennett, W. A. (2011). Direct evidence of cutaneous resistance to evaporative water loss in amphibious mudskipper (family Gobiidae) and rockskipper (family Blenniidae) fishes from Pulau Hoga, Southeast Sulawesi, Indonesia. Journal of Experimental Marine Biology and Ecology, 406, 125–129.Google Scholar
  22. Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2011). ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics, 27, 1164–1165.PubMedPubMedCentralGoogle Scholar
  23. Dehal, P., & Boore, J. L. (2005). Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biology, 3, e314.PubMedPubMedCentralGoogle Scholar
  24. Escriva, H., Bertrand, S., Germain, P., et al. (2006). Neofunctionalization in vertebrates: the example of retinoic acid receptors. PLoS Genetics, 2, 0955–0965.Google Scholar
  25. Felsenstein, J. (1978). Cases in which parsimony or compatibility methods will be positively misleading. Systematic Biology, 27, 401–410.Google Scholar
  26. Finn RN, Cerdà J (2011) Aquaporin evolution in fishes. Frontiers in Physiology, 44.Google Scholar
  27. Finn, R. N., & Cerdà, J. (2015). Evolution and functional diversity of aquaporins. The Biological Bulletin, 229, 6–23.PubMedGoogle Scholar
  28. Finn, R. N., & Kristoffersen, B. A. (2007). Vertebrate vitellogenin gene duplication in relation to the “3R hypothesis”: correlation to the pelagic egg and the oceanic radiation of teleosts. PLoS One, 2, e169.PubMedPubMedCentralGoogle Scholar
  29. Finn, R. N., Chauvigné, F., Hlidberg, J. B., Cutler, C. P., & Cerdà, J. (2014). The lineage-specific evolution of aquaporin gene clusters facilitated tetrapod terrestrial adaptation. PLoS One, 9, e113686.PubMedPubMedCentralGoogle Scholar
  30. Force, A., Lynch, M., Pickett, F. B., Amores, A., Yan, Y. L., & Postlethwait, J. (1999). Preservation of duplicate genes by complementary, degenerative mutations. Genetics, 151, 1531–1545.PubMedPubMedCentralGoogle Scholar
  31. Froger, A., Thomas, D., Delamarche, C., & Tallur, B. (1998). Prediction of functional residues in water channels and related proteins. Protein Science, 7, 1458–1468.PubMedPubMedCentralGoogle Scholar
  32. Fu, D. (2000). Structure of a glycerol-conducting channel and the basis for its selectivity. Science, 290, 481–486.PubMedGoogle Scholar
  33. Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., Chen, Z., Mauceli, E., Hacohen, N., Gnirke, A., Rhind, N., di Palma, F., Birren, B. W., Nusbaum, C., Lindblad-Toh, K., Friedman, N., & Regev, A. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology, 29, 644–652.PubMedPubMedCentralGoogle Scholar
  34. Graham, J. B. (1997). Air-breathing fishes: evolution, diversity and adaptation. San Diego: Academic Press.Google Scholar
  35. Graham, J. B., & Lee, H. J. (2004). Breathing air in air: in what ways might extant amphibious fish biology relate to prevailing concepts about early tetrapods, the evolution of vertebrate air breathing, and the vertebrate land transition? Physiological and Biochemical Zoology, 77, 720–731.PubMedGoogle Scholar
  36. Graham, J., Lee, H., & Wegner, N. (2007). Transition from water to land in an extant group of fishes: air breathing and the acquisition sequence of adaptations for amphibious life in oxudercine gobies. In M. Fernandes, F. Rantin, M. Glass, & B. Kapoor (Eds.), Fish respiration and environment (pp. 255–288). Enfield: Science Publishers.Google Scholar
  37. Han, M. V., Demuth, J. P., McGrath, C. L., et al. (2009). Adaptive evolution of young gene duplicates in mammals. Genome Research, 19, 859–867.PubMedPubMedCentralGoogle Scholar
  38. Heymann, J. B., & Engel, A. (1999). Aquaporins: phylogeny, structure, and physiology of water channels. News in Physiological Sciences, 14, 187–193.PubMedGoogle Scholar
  39. Heymann, J. B., & Engel, A. (2000). Structural clues in the sequences of the aquaporins. Journal of Molecular Biology, 295, 1039–1053.PubMedGoogle Scholar
  40. Huelsenbeck, J. P., Ronquist, F. R., Nielsen, R., & Bollback, J. P. (2001). Bayesian inference of phylogeny and its impact on evolutionary biology. Science, 294, 2310–2314.Google Scholar
  41. Innan, H. (2009). Population genetic models of duplicated genes. Genetica, 137, 19–37.PubMedGoogle Scholar
  42. Ishimatsu, A., & Gonzales, T. (2011). Mudskippers: Front runners in the modern invasion of land. In R. A. Patzner, J. L. Van Tassell, M. Kovačić, & B. G. Kapoor (Eds.), The biology of gobies (pp. 609–638). CRC Press and Science Publishers.Google Scholar
  43. Jaafar, Z., & Murdy, E. O. (2017). Fishes out of water: biology and ecology of mudskippers. Boca Raton: CRC Press.Google Scholar
  44. Jahn, T. P., Møller, A. L. B., Zeuthen, T., Holm, L. M., Klaerke, D. A., Mohsin, B., Kühlbrandt, W., & Schjoerring, J. K. (2004). Aquaporin homologues in plants and mammals transport ammonia. FEBS Letters, 574, 31–36.PubMedGoogle Scholar
  45. Johanson, Z. (2011). How vertebrates left the water. Acta Zoologica, 92, 10–12.Google Scholar
  46. Jones, D. T., Taylor, W. R., & Thornton, J. M. (1992). The rapid generation of mutation data matrices from protein sequences. Bioinformatics, 8, 275–282.Google Scholar
  47. Katoh, K., Rozewicki, J., Yamada, K. D. (2017). MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform bbx108.Google Scholar
  48. Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., & Drummond, A. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649.PubMedPubMedCentralGoogle Scholar
  49. Kok, W. K., Lim, C. B., Lam, T. J., & Ip, Y. K. (1998). The mudskipper Periophthalmodon schlosseri respires more efficiently on land than in water and vice versa for Boleophthalmus boddaerti. The Journal of Experimental Zoology, 280, 86–90.Google Scholar
  50. Konno, N., Hyodo, S., Yamaguchi, Y., Matsuda, K., & Uchiyama, M. (2010). Vasotocin/V2-type receptor/aquaporin axis exists in African lungfish kidney but is functional only in terrestrial condition. Endocrinology, 151, 1089–1096.PubMedGoogle Scholar
  51. Kruse, E., Uehlein, N., & Kaldenhoff, R. (2006). The aquaporins. Genome Biology, 7, 206.PubMedPubMedCentralGoogle Scholar
  52. Laforenza, U., Bottino, C., & Gastaldi, G. (2016). Mammalian aquaglyceroporin function in metabolism. Biochimica et Biophysica Acta - Biomembranes, 1858, 1–11.Google Scholar
  53. Lee, Y.-J., Choi, Y., & Ryu, B.-S. (1995). A taxonomic revision of the genus Periophthalmus (Pisces: Gobiidae) from Korea with description of a new species. Korean Journal of Ichthyology, 7, 120–127.Google Scholar
  54. Linnaeus, C. (1758). Systema Naturae, edition X, vol. 1 (Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata). Holmiae, 1, 230–338.Google Scholar
  55. Lynch, M., & Force, A. (2000). The probability of duplicate gene preservation by subfunctionalization. Genetics, 154, 459–473.PubMedPubMedCentralGoogle Scholar
  56. Madeira, A., Fernández-Veledo, S., Camps, M., Zorzano, A., Moura, T. F., Ceperuelo-Mallafré, V., Vendrell, J., & Soveral, G. (2014). Human aquaporin-11 is a water and glycerol channel and localizes in the vicinity of lipid droplets in human adipocytes. Obesity, 22, 2010–2017.PubMedGoogle Scholar
  57. Madsen, S. S., Engelund, M. B., & Cutler, C. P. (2015). Water transport and functional dynamics of aquaporins in osmoregulatory organs of fishes. The Biological Bulletin, 229, 70–92.PubMedGoogle Scholar
  58. Martinez, A., Cutler, C. P., Wilson, G. D., et al. (2005). Regulation of expression of two aquaporin homologs in the intestine of the European eel: effects of seawater acclimation and cortisol treatment. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 288, R1733–R1743.PubMedGoogle Scholar
  59. Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Gateway Computing Environments Workshop, GCE (pp 1–8).Google Scholar
  60. Morishita, Y., Matsuzaki, T., Hara-chikuma, M., Andoo, A., Shimono, M., Matsuki, A., Kobayashi, K., Ikeda, M., Yamamoto, T., Verkman, A., Kusano, E., Ookawara, S., Takata, K., Sasaki, S., & Ishibashi, K. (2005). Disruption of aquaporin-11 produces polycystic kidneys following vacuolization of the proximal tubule. Molecular and Cellular Biology, 25, 7770–7779.PubMedPubMedCentralGoogle Scholar
  61. Moriyama, Y., Ito, F., Takeda, H., Yano, T., Okabe, M., Kuraku, S., Keeley, F. W., & Koshiba-Takeuchi, K. (2016). Evolution of the fish heart by sub/neofunctionalization of an elastin gene. Nature Communications, 7, 10397.PubMedPubMedCentralGoogle Scholar
  62. Müller, C., Sendler, M., & Hildebrandt, J.-P. (2006). Downregulation of aquaporins 1 and 5 in nasal gland by osmotic stress in ducklings, Anas platyrhynchos: implications for the production of hypertonic fluid. The Journal of Experimental Biology, 209, 4067–4076.PubMedGoogle Scholar
  63. Murdy, E. O. (1989). A taxonomic revision and cladistic analysis of the oxudercine gobies (Gobiidae: Oxudercinae). Records of the Australian Museum Supplement, 11, 1–93.Google Scholar
  64. Murdy, E. O. (2011). Systematics of oxudercinae. In R. A. Patzner, J. L. Van Tassell, M. Kovačić, & B. G. Kapoor (Eds.), The biology of gobies (pp. 99–106). CRC Press and Science Publishers.Google Scholar
  65. Nielsen, R., & Yang, Z. (1998). Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics, 148, 929–936.PubMedPubMedCentralGoogle Scholar
  66. Ogino, Y., Kuraku, S., Ishibashi, H., Miyakawa, H., Sumiya, E., Miyagawa, S., Matsubara, H., Yamada, G., Baker, M. E., & Iguchi, T. (2016). Neofunctionalization of androgen receptor by gain-of-function mutations in teleost fish lineage. Molecular Biology and Evolution, 33, 228–244.PubMedGoogle Scholar
  67. Ord, T. J., & Cooke, G. M. (2016). Repeated evolution of amphibious behavior in fish and its implications for the colonization of novel environments. Evolution (N Y), 70, 1747–1759.Google Scholar
  68. Pace, C. M., & Gibb, A. C. (2009). Mudskipper pectoral fin kinematics in aquatic and terrestrial environments. The Journal of Experimental Biology, 212, 2279–2286.PubMedGoogle Scholar
  69. Pallas, P. S. (1780). Spicilegia zoologica: quibus novae imprimis et obscurae animalium species iconibus, descriptionibus atque commentariis illustrantur. Berolini,Gottl, August, Lange.Google Scholar
  70. Park, J. H., & Saier, M. H. (1996). Phylogenetic characterization of the MIP family of transmembrane channel proteins. The Journal of Membrane Biology, 153, 171–180.PubMedGoogle Scholar
  71. Polgar, G., Ghanbarifardi, M., Milli, S., Agorreta, A., Aliabadian, M., Esmaeili, H. R., & Khang, T. F. (2017). Ecomorphological adaptation in three mudskippers (Teleostei: Gobioidei: Gobiidae) from the Persian Gulf and the Gulf of Oman. Hydrobiologia, 795, 91–111.Google Scholar
  72. Preston, G. M., & Agre, P. (1991). Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family. Proceedings of the National Academy of Sciences, 88, 11110–11114.Google Scholar
  73. R Development Core Team. (2016). R: A language and environment for statistical computing. R Found. Stat. Comput. Vienna Austria 0:409.Google Scholar
  74. Randall, D. J., Ip, Y. K., Chew, S. F., & Wilson, J. M. (2015). Air breathing and ammonia excretion in the giant mudskipper, Periophthalmodon schlosseri. Physiological and Biochemical Zoology, 77, 783–788.Google Scholar
  75. Reeves, J. H. (1992). Heterogeneity in the substitution process of amino acid sites of proteins coded for by mitochondrial DNA. Journal of Molecular Evolution, 35, 17–31.PubMedGoogle Scholar
  76. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., & Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.PubMedPubMedCentralGoogle Scholar
  77. Saad, R., Cohanim, A. B., Kosloff, M., Privman, E. (2018). Neofunctionalization in ligand binding sites of ant olfactory receptors. Genome Biology and Evolution.Google Scholar
  78. Saitoh, Y., Ogushi, Y., Shibata, Y., Okada, R., Tanaka, S., & Suzuki, M. (2014). Novel vasotocin-regulated aquaporins expressed in the ventral skin of semiaquatic anuran amphibians: evolution of cutaneous water-absorbing mechanisms. Endocrinology, 155, 2166–2177.PubMedGoogle Scholar
  79. San Mauro, D., & Agorreta, A. (2010). Molecular systematics: a synthesis of the common methods and the state of knowledge. Cellular & Molecular Biology Letters, 15, 311–341.Google Scholar
  80. São Pedro, S. L., Alves, J. M. P., Barreto, A. S., & De Souza Lima, A. O. (2015). Evidence of positive selection of aquaporins genes from Pontoporia blainvillei during the evolutionary process of cetaceans. PLoS One, 10, e0134516.PubMedPubMedCentralGoogle Scholar
  81. Saparov, S. M., Liu, K., Agre, P., & Pohl, P. (2007). Fast and selective ammonia transport by aquaporin-8. The Journal of Biological Chemistry, 282, 5296–5301.PubMedGoogle Scholar
  82. Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313.PubMedPubMedCentralGoogle Scholar
  83. Sui, H., Han, B. G., Lee, J. K., Walian, P., & Jap, B. K. (2001). Structural basis of water-specific transport through the AQP1 water channel. Nature, 414, 872–878.PubMedGoogle Scholar
  84. Suzuki, M., Hasegawa, T., Ogushi, Y., & Tanaka, S. (2007). Amphibian aquaporins and adaptation to terrestrial environments: a review. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology, 148, 72–81.Google Scholar
  85. Tavaré, S. (1986). Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures on Mathematics in the Life Sciences, 17, 57–86.Google Scholar
  86. Taylor, J. S., Van de Peer, Y., Braasch, I., & Meyer, A. (2001). Comparative genomics provides evidence for an ancient genome duplication event in fish. Philosophical Transactions of the Royal Society B Biology Science, 356, 1661–1679.Google Scholar
  87. Tingaud-Sequeira, A., Calusinska, M., Finn, R. N., Chauvigné, F., Lozano, J., & Cerdà, J. (2010). The zebrafish genome encodes the largest vertebrate repertoire of functional aquaporins with dual paralogy and substrate specificities similar to mammals. BioMed Central Evolutionary Biology, 10, 38.PubMedGoogle Scholar
  88. Tipsmark, C. K., Sorensen, K. J., & Madsen, S. S. (2010). Aquaporin expression dynamics in osmoregulatory tissues of Atlantic salmon during smoltification and seawater acclimation. The Journal of Experimental Biology, 213, 368–379.PubMedGoogle Scholar
  89. Tsuhako, Y., Ishimatsu, A., Takeda, T., Huat, K. K., & Tachihara, K. (2003). The eggs and larvae of the giant mudskipper, Periophthalmodon schlosseri, collected from a mudflat in Penang, Malaysia. Ichthyological Research, 50, 178–181.Google Scholar
  90. Virkki, L. V., Franke, C., Somieski, P., & Boron, W. F. (2002). Cloning and functional characterization of a novel aquaporin from Xenopus laevis oocytes. The Journal of Biological Chemistry, 277, 40610–40616.PubMedGoogle Scholar
  91. Wright, P. A., & Turko, A. J. (2016). Amphibious fishes: evolution and phenotypic plasticity. The Journal of Experimental Biology, 219, 2245–2259.PubMedGoogle Scholar
  92. Wu, B., & Beitz, E. (2007). Aquaporins with selectivity for unconventional permeants. Cellular and Molecular Life Sciences, 64, 2413–2421.PubMedGoogle Scholar
  93. Yakata, K., Hiroaki, Y., Ishibashi, K., Sohara, E., Sasaki, S., Mitsuoka, K., & Fujiyoshi, Y. (2007). Aquaporin-11 containing a divergent NPA motif has normal water channel activity. Biochimica et Biophysica Acta - Biomembranes, 1768, 688–693.Google Scholar
  94. Yakata, K., Tani, K., & Fujiyoshi, Y. (2011). Water permeability and characterization of aquaporin-11. Journal of Structural Biology, 174, 315–320.PubMedGoogle Scholar
  95. Yang, Z. (1994). Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. Journal of Molecular Evolution, 39, 306–314.PubMedGoogle Scholar
  96. Yang, Z. (2007). PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24, 1586–1591.PubMedGoogle Scholar
  97. Yang, Z. (2008). Adaptive molecular evolution. In: Handbook of statistical genetics: third edition (pp 375–406).Google Scholar
  98. Yang, Z., & Dos Reis, M. (2011). Statistical properties of the branch-site test of positive selection. Molecular Biology and Evolution, 28, 1217–1228.PubMedGoogle Scholar
  99. Yang, Z., Wong, W. S. W., & Nielsen, R. (2005). Bayes empirical Bayes inference of amino acid sites under positive selection. Molecular Biology and Evolution, 22, 1107–1118.PubMedGoogle Scholar
  100. You, X., Bian, C., Zan, Q., Xu, X., Liu, X., Chen, J., Wang, J., Qiu, Y., Li, W., Zhang, X., Sun, Y., Chen, S., Hong, W., Li, Y., Cheng, S., Fan, G., Shi, C., Liang, J., Tom Tang, Y., Yang, C., Ruan, Z., Bai, J., Peng, C., Mu, Q., Lu, J., Fan, M., Yang, S., Huang, Z., Jiang, X., Fang, X., Zhang, G., Zhang, Y., Polgar, G., Yu, H., Li, J., Liu, Z., Zhang, G., Ravi, V., Coon, S. L., Wang, J., Yang, H., Venkatesh, B., Wang, J., & Shi, Q. (2014). Mudskipper genomes provide insights into the terrestrial adaptation of amphibious fishes. Nature Communications, 5, 5594.PubMedPubMedCentralGoogle Scholar
  101. Zander, C. D. (2011). Morphological adaptations to special environments of gobies. In R. A. Patzner, J. L. Van Tassell, M. Kovačić, B. G. Kapoor (Eds.), The biology of gobies (pp 345–366). CRC Press and Science Publishers.Google Scholar
  102. Zardoya, R. (2005). Phylogeny and evolution of the major intrinsic protein family. Biology of the Cell, 97, 397–414.PubMedGoogle Scholar
  103. Zhang, J., Taniguchi, T., Takita, T., & Ali, A. B. (2003). A study on the epidermal structure of Periophthalmodon and Periophthalmus mudskippers with reference to their terrestrial adaptation. Ichthyological Research, 50, 310–317.Google Scholar
  104. Zhang, J., Nielsen, R., & Yang, Z. (2005). Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Molecular Biology and Evolution, 22, 2472–2479.PubMedGoogle Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2018

Authors and Affiliations

  1. 1.Department of Biodiversity, Ecology, and EvolutionComplutense University of MadridMadridSpain
  2. 2.Department of Neuroscience, Spinal Cord and Brain Injury Research Center & Ambystoma Genetic Stock CenterUniversity of KentuckyLexingtonUSA

Personalised recommendations