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Fine structure of micropylar regions of Cobitis hankugensis, Iksookimia longicorpa and their unisexual natural hybrids

Published online by Cambridge University Press:  30 March 2022

Seung Woon Yun Open the ORCID record for Seung Woon Yun [Opens in a new window]  and
Jong Young Park Open the ORCID record for Jong Young Park [Opens in a new window]
Seung Woon Yun
Affiliation:
Department of Biological Sciences, College of Natural Sciences and Institute for Biodiversity Research, Jeonbuk National University, Jeonju, South Korea
Jong Young Park*
Affiliation:
Department of Biological Sciences, College of Natural Sciences and Institute for Biodiversity Research, Jeonbuk National University, Jeonju, South Korea
*
Author for correspondence: Jong Young Park. Department of Biological Sciences, College of Natural Sciences and Institute for Biodiversity Research, Chonbuk National University, Jeonju54896, South Korea. Tel: +82 63 270 3344. Fax: +82 63 270 3362. E-mail: [email protected]
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Summary

Iksookimia longicorpa and Cobitis hankugensis are two species of fish distributed only on the Korean Peninsula. They have a unique reproductive ecology that naturally hybridizes into three widely known unisexual types, maintaining populations of almost all females. In this study, the fine structure of the micropyles of I. longicorpa, C. hankugensis and their hybrids was analyzed to find out how egg–sperm interaction, a common interspecies isolation mechanism, is possible between heterogeneous species. Analysis of 30 eggs from five females of each species revealed that all had one funnel-shaped micropylar region and a manhole-shaped micropyle canal. With the exception of C. hankugensis, which had no spiral grooves or ridges, the rest had counterclockwise spiral grooves and ridges on the micropylar region. All five species, however, showed identical groove patterns for the micropyle canal. The egg size was the largest in HL (one from the C. hankugensis locus with one from the I. longicorpa locus) and the smallest in C. hankugensis. In the hybrids, the HL type had the largest egg and HHL (two from the C. hankugensis locus with one from the I. longicorpa locus) type the smallest. For the diameter of the micropylar region and micropyle canal, the diploid I. longicorpa, C. hankugensis and HL were smaller than those of the triploid. In addition, as the ratio of the canal diameter to the eggs was lower in I. longicorpa than in C. hankugensis, it was confirmed that I. longicorpa has a relatively small micropyle canal compared with C. hankugensis.

Keywords

CobitidaeCobitis hankugensis–Iksookimia longicorpa hybridEggFine structureMicropyle
Type
Research Article
Information
Zygote , Volume 30 , Issue 4 , August 2022 , pp. 516 - 521
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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References

Abbott, R., Albach, D., Ansell, S., Arntzen, J. W., Baird, S. J. E., Bierne, N., Boughman, J. W., Brelsford, A., Buerkle, C. A., Buggs, R., Butlin, R. K., Dieckmann, U., Eroukhmanoff, F., Grill, A., Cahan, S. H., Hermansen, J. S., Hewitt, G., Hudson, A. G., Jiggins, C., Jones, J., Keller, B., Marczewski, T., Mallet, J., Martinez-Rodriguez, P., Möst, M., Mullen, S., Nichols, R., Nolte, A. W., Parisod, C., Pfennig, K., Rice, A. M., Ritchie, M. G., Seifert, B., Smadja, C. M., Stelkens, R., Szymura, J. M., Väinölä, R., Wolf, J. B., Zinner, D. (2013). Hybridization and speciation. Journal of Evolutionary Biology, 26(2), 229–246. doi: 10.1111/j.1420-9101.2012.02599.x CrossRefGoogle ScholarPubMed
Amanze, D. and Iyengar, A. (1990). The micropyle—A sperm guidance-system in teleost fertilization. Development, 109(2), 495–500. doi: 10.1242/dev.109.2.495 CrossRefGoogle ScholarPubMed
Barton, N. H. and Hewitt, G. M. (1985). Analysis of hybrid zones. Annual Review of Ecology and Systematics, 16(1), 113–148. doi: 10.1146/annurev.es.16.110185.000553 CrossRefGoogle Scholar
Britz, R. and Toledo-Piza, M. (2012). Egg surface structure of the freshwater toadfish Thalassophryne amazonica (Teleostei: Batrachoididae) with information on its distribution and natural habitat. Neotropical Ichthyology, 10(3), 593–599. doi: 10.1590/S1679-62252012000300013 CrossRefGoogle Scholar
Britz, R., Kokoscha, M. and Riehl, R. (1995). The Anabantoid genera Ctenops, Luciocephalus, Parasphaerichthys, and Sphaerichthys (Teleostei, Perciformes) as a monophyletic group—evidence from egg surface-structure and reproductive-behavior. Japanese Journal of Ichthyology, 42, 71–79.Google Scholar
Chen, K. C., Shao, K. T. and Yang, J. S. (1999). Using micropylar ultrastructure for species identification and phylogenetic inference among four species of Sparidae. Journal of Fish Biology, 55(2), 288–300. doi: 10.1111/j.1095-8649.1999.tb00679.x CrossRefGoogle Scholar
Chevassus, B. (1983). Hybridization in fish. Aquaculture, 33, 245–262.CrossRefGoogle Scholar
Coward, K., Bromage, N. R., Hibbitt, O. and Parrington, J. (2002). Gamete physiology, fertilization and egg activation in teleost fish. Reviews in Fish Biology and Fisheries, 12(1), 33–58. doi: 10.1023/A:1022613404123 CrossRefGoogle Scholar
Debus, L., Winkler, M. and Billard, R. (2008). Ultrastructure of the oocyte envelopes of some Eurasian acipenserids. Journal of Applied Ichthyology, 24(s1), 57–64. doi: 10.1111/j.1439-0426.2008.01093.x CrossRefGoogle Scholar
Ginsburg, A. S. (1968). Fertilization in Fishes and the Problem of Polyspermy, p. 354. Izdatelnaya Nauka.Google Scholar
Hardie, D. C. and Hebert, P. D. N. (2004). Genome-size evolution in fishes. Canadian Journal of Fisheries and Aquatic Sciences, 61(9), 1636–1646. doi: 10.1139/f04-106 CrossRefGoogle Scholar
Hart, N. H. (1990). Fertilization in teleost fishes: Mechanisms of sperm–egg interactions. International Review of Cytology, 121, 1–66. doi: 10.1016/s0074-7696(08)60658-0 CrossRefGoogle ScholarPubMed
Hart, N. H., Pietri, R. and Donovan, M. (1984). The structure of the chorion and associated surface filaments in Oryzias–evidence for the presence of extracellular tubules. Journal of Experimental Zoology, 230(2), 273–296. doi: 10.1002/jez.1402300213 CrossRefGoogle ScholarPubMed
Hirai, A. and Yamamoto, T. S. (1986). Micropyle in the developing eggs of the anchovy, Engraulis japonica . Japanese Journal of Ichthyology, 33(1), 62–66. doi: 10.1007/BF02905561 CrossRefGoogle Scholar
Iwamatsu, T., Onitake, K., Matsuyama, K., Satoh, M. and Yukawa, S. (1997). Effect of micropylar morphology and size on rapid sperm entry into the eggs of the medaka. Zoological Science, 14(4), 623–628. doi: 10.2108/zsj.14.623 CrossRefGoogle Scholar
Kim, H. T. and Park, J. Y. (2021). Comparative morphology and morphometry of the micropyle of two Korean rice-fishes, Oryzias latipes and Oryzias sinensis (Pisces, Adrianichthyidae). Journal of Vertebrate Biology, 70(1), 20130.1–8. doi: 10.25225/jvb.20130 CrossRefGoogle Scholar
Kim, C. H., Kim, J. G. and Park, J. Y. (2011). Structure of egg envelope and oogenesis of Kichulchoia multifasciata . Korean Journal of Microscopy, 41, 189–196.Google Scholar
Kim, I. S., Choi, K. C. and Nalbant, T. (1976). Cobitis longicorpus, a new cobitid fish form Korea. Korean Journal of Zoology, 19, 171–178.Google Scholar
Ko, M. H. (2009). Reproductive mechanisms of the unisexual diploid-tripoid hybrid complex of between the spined loach Cobitis hankugensis and Iksookimia longicorpa (Teleostei, Cobitidae) in Korea [Chonbuk National University Dotoral Thesis], 160 pp.Google Scholar
Kobayashi, W. and Yamamoto, T. S. (1981). Fine-structure of the micropylar apparatus of the chum salmon egg, with a discussion of the mechanism for blocking polyspermy. Journal of Experimental Zoology, 217(2), 265–275. doi: 10.1002/jez.1402170213 CrossRefGoogle Scholar
Lee, E. H. (1995). A study of reproductive mode of the unisexual Cobitid fishes, Cobitis sinensis-longicorpus complex (Cobididae) by hybridization with its parental species [Chonbuk National University Dotoral Thesis], 92 pp.Google Scholar
Lee, J. H. (1992). A systematic study of the unisexual Cobitid fish, Cobitis sinensis-longicorpus complex in the Naktong River, Korea [Chonbuk National University Doctoral Thesis], 103 pp.Google Scholar
Matsunaga, S., Katagiri, Y., Nagashima, Y., Sugiyama, T., Hasegawa, J., Hayashi, K. and Sakamoto, T. (2013). New insights into the dynamics of plant cell nuclei and chromosomes. International Review of Cell and Molecular Biology, 305, 253–301. doi: 10.1016/B978-0-12-407695-2.00006-8 CrossRefGoogle ScholarPubMed
Mazzini, M., Callaini, G. and Mencarelli, C. (1984). A comparative analysis of the evolution of the egg envelopes and the origin of the yolk. Bolletino di Zoologia, 51(1–2), 35–101. doi: 10.1080/11250008409439457 CrossRefGoogle Scholar
Mendell, J. E., Clements, K. D., Choat, J. H. and Angert, E. R. (2008). Extreme polyploidy in a large bacterium. Proceedings of the National Academy of Sciences of the United States of America, 105(18), 6730–6734. doi: 10.1073/pnas.0707522105 CrossRefGoogle Scholar
Mito, S. (1979). Fish eggs. Gekkan Kaiyo-Kagaku, 11, 126–130.Google Scholar
Morisawa, S. (1999). Fine structure of micropylar region during late oogenesis in eggs of the hagfish Eptatretus burgeri (Agnatha). Development, Growth and Differentiation, 41(5), 611–618. doi: 10.1046/j.1440-169x.1999.00458.x CrossRefGoogle Scholar
Nelson, J. S. (2006). Fishes of the world (4th edn) John Wiley and Sons, Inc., 601 pp.Google Scholar
Park, J. Y. (1996). A morphological study on the gonad of the species in the family Cobitidae (Pisces: Cypriniformes) from Korea [Dissertation]. Chonbuk National University (pp. 6–158).Google Scholar
Park, J. Y. and Kim, I. S. (1997). Egg membrane in five cobitid species of Cobitis (Pisces: Cobitidae). Korean Journal of Ichthyology, 9, 121–129.Google Scholar
Park, J. Y., Kim, I. S. and Ko, M. H. (2011). Characteristics of rare males in the cobitid unisexual complex, Cobitis hankugensis–Iksookimia longicorpa . Folia Zoologica, 60(4), 290–294. doi: 10.25225/fozo.v60.i4.a4.2011 CrossRefGoogle Scholar
Psenicka, M., Rodina, M. and Linhart, O. (2010). Ultrastructural study on the fertilisation process in sturgeon (Acipenser), function of acrosome and prevention of polyspermy. Animal Reproduction Science, 117(1–2), 147–154. doi: 10.1016/j.anireprosci.2009.03.013 CrossRefGoogle Scholar
Riehl, R. (1980). Micropyle of some Salmonins and Coregonins. Environmental Biology of Fishes, 5(1), 59–66. doi: 10.1007/BF00000950 CrossRefGoogle Scholar
Riehl, R. and Kock, K.-H. (1989). The surface-structure of Antarctic fish eggs and its use in identifying fish eggs from the Southern Ocean. Polar Biology, 9(3), 197–203. doi: 10.1007/BF00297176 CrossRefGoogle Scholar
Riehl, R. and Kokoscha, M. (1993). A unique surface pattern and micropylar apparatus in the eggs of Luciocephalus sp. (Perciformes, Luciocephalidae). Journal of Fish Biology, 43(4), 617–620. doi: 10.1111/j.1095-8649.1993.tb00444.x CrossRefGoogle Scholar
Riehl, R. and Schulte, E. (1977). Scanning electron microscopical investigations of micropyles of selected freshwater teleost fishes. Archiv für Fischereiwissenschaft, 28, 95–107.Google Scholar
Scopece, G., Widmer, A. and Cozzolino, S. (2008). Evolution of postzygotic reproductive isolation in a guild of deceptive orchids. American Naturalist, 171(3), 315–326. doi: 10.1086/527501 CrossRefGoogle Scholar
Slechtová, V., Bohlen, J. and Perdices, A. (2008). Molecular phylogeny of the freshwater fish family Cobitidae (Cypriniformes: Teleostei): Delimitation of genera, mitochondrial introgression and evolution of sexual dimorphism. Molecular Phylogenetics and Evolution, 47(2), 812–831. doi: 10.1016/j.ympev.2007.12.018 CrossRefGoogle ScholarPubMed
Solis Murgas, L. D., Paulino, M. S., Palhares, P. C., Miliorini, A. B., Alves, E. and Oliveira Felizardo, Vd. (2017). Ultrastructural and morphometric analysis of gametes in Neotropical teleost fishes. Journal of FisheriesSciences.com, 11(1), 56–61. doi: 10.21767/1307-234X.1000109 CrossRefGoogle Scholar
Yamamoto, K. (1952). Studies on the fertilization of the egg of the flounder. 2. The morphological structure of the micropyle and its behavior in response to sperm-entry. Cytologia, 16(4), 302–306. doi: 10.1508/cytologia.16.302 CrossRefGoogle Scholar
Yanagimachi, R., Cherr, G., Matsubara, T., Andoh, T., Harumi, T., Vines, C., Pillai, M., Griffin, F., Matsubara, H., Weatherby, T. and Kaneshiro, K. (2013). Sperm attractant in the micropyle region of fish and insect eggs. Biology of Reproduction, 88(2), 47. doi: 10.1095/biolreprod.112.105072 CrossRefGoogle ScholarPubMed
Yanagimachi, R., Harumi, T., Matsubara, H., Yan, W., Yuan, S., Hirohashi, N., Iida, T., Yamaha, E., Arai, K., Matsubara, T., Andoh, T., Vines, C. and Cherr, G. (2017). Chemical and physical guidance of fish spermatozoa into the egg through the micropyle. Biology of Reproduction, 96(4), 780–799. doi: 10.1093/biolre/iox015 CrossRefGoogle Scholar
Yun, S. W. (2017). Molecular biological study of ploidy level determination and mode of hybridization in the loach Cobitis hankugensis—Iksookimia longicorpa complex [Chonbuk National University Doctoral Thesis], 115 pp.Google Scholar