Abstract
Medaka Oryzias latipes is a tiny euryhaline fresh water fish distributed in environments differing widely in salinity. According to past reports, Oryzias latipes spermatozoa are not active in saline conditions. We identified a brackish water–colonized population of medaka that showed a high fertilization rate in seawater and investigated whether this was genetically based. Two G1 populations were produced and placed in either fresh water or 50% seawater soon after hatching. After maturation, sperm was obtained from dissected testis, and motility of the spermatozoa was evaluated in fresh or seawater. Spermatozoa of the fresh water–reared fish were activated only in fresh water, whereas those of the 50% seawater–reared fish were motile in both fresh and seawater. After fresh water–reared fish were acclimated to 50% seawater, spermatozoa could be activated in seawater. These results indicated that spermatozoon motility with respect to salinity is a phenotypic plastic trait in medaka.
This is a preview of subscription content, log in via an institution to check access.
Data availability
The data that support these findings are available from the corresponding author upon reasonable request.
References
Awaji M, Hanyu I (1987) Annual reproductive cycle of the wild type medaka. Nippon Suisan Gakkaishi 53:959–965. https://doi.org/10.2331/suisan.53.959
Beirão J, Lewis JA, Wringe BF, Purchase CF (2018) A novel sperm adaptation to evolutionary constraints on reproduction: pre-ejaculatory sperm activation in the beach spawning capelin (Osmeridae). Ecol Evol 8:2343–2349. https://doi.org/10.1002/ece3.3783
Brown RK, Kaurova SA, Uteshev VK, Shishova NV, McGinnity D, Figiel CR, Mansour N, Agnew D, Wu M, Gakhova EN, Dzyuba B, Cosson J (2015) Sperm motility of externally fertilizing fish and amphibians. Theriogenology 83:1–13. https://doi.org/10.1016/j.theriogenology.2014.09.018
Christen R, Gatti JL, Billard R (1987) Trout sperm motility. Eur J Biochem 166:667–671. https://doi.org/10.1111/j.1432-1033.1987.tb13565.x
Elofsson H, McAlister BG, Kime DE, Mayer I, Borg B (2003) Long lasting stickleback sperm; is ovarian fluid a key to success in fresh water? J Fish Biol 63:240–253. https://doi.org/10.1046/j.1095-8649.2003.00153.x
Green L, Haveenhand JN, Kvarnemo C (2020) Evidence of rapid adaptive trait change to local salinity in the sperm of an invasive fish. Evol Appl 13:533–544. https://doi.org/10.1111/eva.12859
Hammer Ø, Harper DA, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9
Hayakawa H, Le QD, Kinoshita M, Takehana Y, Sakuma K, Takeshima H, Kojima S, Naruse K, Inoue K (2015) Genetic similarity of the Hainan medaka populations collected from hyper- and hypo-osmotic environments in northern Vietnam. Ocean Sci J 50:231–235. https://doi.org/10.1007/s12601-015-0020-6
Inoue K, Takei Y (2002) Diverse adaptability in Oryzias species to high environmental salinity. Zoolog Sci 19:727–734. https://doi.org/10.2108/zsj.19.727
Inoue K, Takei Y (2003) Asian medaka fishes offer new models for studying mechanisms of seawater adaptation. Comp Biochem Physiol B 136:635–645. https://doi.org/10.1016/S1096-4959(03)00204-5
Kawaguchi M, Yasumasu S, Hiroi J, Naruse K, Inoue M, Iuchi I (2006) Evolution of teleostean hatching enzyme genes and their paralogous genes. Dev Genes Evol 216:769. https://doi.org/10.1007/s00427-006-0104-5
Kawaguchi M, Yasumasu S, Shimizu A, Kudo N, Sano K, Iuchi I, Nishida M (2013) Adaptive evolution of fish hatching enzyme: one amino acid substitution results in differential salt dependency of the enzyme. J Exp Biol 216:1609–1615. https://doi.org/10.1242/jeb.069716
Koike Y, Koya Y (2014) Viable periods of fertilizability of eggs and sperm of Japanese medaka, Oryzias latipes. Jpn J Ichthyol 61:9–14. https://doi.org/10.11369/jji.61.9
Koya Y, Koike Y, Onchi R, Munehara H (2013) Two patterns of parasitic male mating behaviors and their reproductive success in Japanese medaka, Oryzias latipes. Zoolog Sci 30:76–82. https://doi.org/10.2108/zsj.30.76
Legendre M, Alavi SMH, Dzyuba B, Linhart O, Prokopchuk G, Cochet C, Dugué R, Cosson J (2016) Adaptations of semen characteristics and sperm motility to harsh salinity: extreme situations encountered by the euryhaline tilapia Sarotherodon melanotheron heudelotii (Dumeril, 1859). Theriogenology 86:1251–1267. https://doi.org/10.1016/j.theriogenology.2016.04.066
Levitian DR (2000) Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegatus. Proc R Soc B 267:531–534. https://doi.org/10.1098/rspb.2000.1032
Makiguchi Y, Torao M, Kojima T, Pitcher TE (2016) Reproductive investment patterns and comparison of sperm quality in the presence and absence of ovarian fluid in alternative reproductive tactics of masu salmon, Oncorhynchus masou. Theriogenology 86:2189–2193. https://doi.org/10.1016/j.theriogenology.2016.07.0999
Miyanishi H, Inokuchi M, Nobata S, Kaneko T (2016) Past seawater experience enhances seawater adaptability in medaka, Oryzias latipes. Zool Lett 2:1–10. https://doi.org/10.1186/s40851-016-0047-2
Moka W, Sawayama E, Noguchi D, Takagi M (2016) Identification of hatchery-cultured S-type rotifer escapees, Brachionus koreanus, in a wild environment: a preliminary study. Fish Genet Breed Sci 46:23–29
Morita M, Takemura A, Okuno M (2003) Requirement of Ca2+ on activation of sperm motility in euryhaline tilapia Oreochromis mossambicus. J Exp Biol 206:913–921. https://doi.org/10.1242/jeb.00153
Morita M, Takemura A, Okuno M (2004) Acclimation of sperm motility apparatus in seawater-acclimated euryhaline tilapia Oreochromis mossambicus. J Exp Biol 207:337–345. https://doi.org/10.1242/jeb.00748
Morita M, Takemura A, Nakajima A, Okuno M (2006) Microtubule sliding movement in tilapia sperm flagella axoneme is regulated by Ca2+/calmodulin-dependent protein phosphorylation. Cell Motil 63:459–470. https://doi.org/10.1002/cm.20137
Myosho T, Takahashi H, Yoshida K, Sato T, Hamaguchi S, Sakamoto T, Sakaizumi M (2018) Hyperosmotic tolerance of adult fish and early embryos are determined by discrete, single loci in the genus Oryzias. Sci Rep 8:6897. https://doi.org/10.1038/s41598-018-24621-7
Sasaki N, Ito S (1961) Studies on the medaka (Oryzias latipes) found in sea water I Field Observation. Zool Mag 70:188–191
Shima A, Mitani H (2004) Medaka as a research organism: past, present and future. Mech Dev 121:599–604. https://doi.org/10.1016/j.mod.2004.03.011
Takehana Y, Nagai N, Matsuda M, Tsuchiya K, Sakaizumi M (2003) Geographic variation and diversity of the cytochrome b gene in Japanese wild populations of medaka, Oryzias latipes. Zoolog Sci 20:1279–1291. https://doi.org/10.2108/zsj.20.1279
Takehana Y, Zahm M, Cabau C, Klopp C, Roques C, Bouchez O, Donnadieu C, Barrachina C, Journot L, Kawaguchi M et al (2020) Genome sequence of the euryhaline Javafish medaka Oryzias Javanicus: a Small Aquarium Fish Model for Studies on Adaptation to Salinity. G3 10:907–915. https://doi.org/10.1534/g3.119.400725
Taugbøl A, Mazzarella AB, Cramer ERA, Laskemoen T (2017) Salinity-induced phenotypic plasticity in threespine stickleback sperm activation. Biol Lett 13:20170516. https://doi.org/10.1098/rsbl.2017.0516
Tiersch TR, Yang H (2012) Environmental salinity-induced shifts in sperm motility activation in Fundulus grandis. Aquaculture 324–325:145–150. https://doi.org/10.1016/j.aquaculture.2011.10.023
Yamagami K (1973) Some enzymological properties of a hatching enzyme (chorionase) isolated from the fresh-water teleost, Oryzias latipes. Comp Biochem Physiol B 46:603–614. https://doi.org/10.1016/0305-0491(73)90100-4
Yamamoto T (1942) On the adaptability of the Japanese killifish, Aplocheilus latipes (TEMMINCK & SCHLEGEL) to the sea water. Bot Zool 10:805–809
Yamamoto T, Ogawa J, Miyawaki K (2007) Faunal survey of the Akahone island, Kamijima, Ehime Pref. Bulletin of Ehime Prefectural Science Museum 12:27–30.
Yanagishima S, Mori S (1957) Studies on the variation and adaptation of fishes. I. Adaptation of killifish (Oryzias latipes T. & S.). Zool Mag 66:7–14
Yang H, Tiersch TR (2009) Sperm motility initiation and duration in a euryhaline fish, medaka (Oryzias latipes). Theriogenology 72:386–392. https://doi.org/10.1016/j.theriogenology.2009.03.007
Yasumasu S, Iuchi I, Yamagami K (1989) Purification and partial characterization of high choriolytic enzyme (HCE), a component of the hatching enzyme of the teleost, Oryzias latipes. J Biochem 105:204–211. https://doi.org/10.1093/oxfordjournals.jbchem.a122640
Acknowledgements
We are grateful to NBRP Medaka (https://shigen.nig.ac.jp/medaka/) for providing the wild stock (Strain ID: WS245).
Funding
This study was supported by a grant from Kurita Water and Environment Foundation (#20B005) to E.S.
Author information
Authors and Affiliations
Contributions
Conceptualization: E.S.; methodology: E.S. and Y.M; formal analysis: E.S., M.K., N.T., and Y.M.; investigation: M.K., N.T., and Y.M.; data curation: M.K. and N.T.; resources: E.S. and M.K.; writing – review and editing: E.S. and Y.M.; funding acquisition: E.S.
Corresponding author
Ethics declarations
Ethics approval
The study protocol was approved by the Animal Care and Use Committee of Nihon University (permit AP21BRS064-1).
Competing interests
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Sawayama, E., Koyanagi, M., Tanabe, N. et al. Acclimation to seawater allows activation of spermatozoa of a euryhaline fish Oryzias latipes. Environ Biol Fish 105, 787–794 (2022). https://doi.org/10.1007/s10641-022-01285-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10641-022-01285-x