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Abortive meiosis in the oogenesis of parthenogenetic Daphnia pulex

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Abstract

Most daphnid species adopt parthenogenesis and sexual reproduction differentially in response to varied environmental cues, resulting in the production of diploid progenies in both cases. Previous studies have reportedly suggested that daphnids produce their parthenogenetic eggs via apomixis; the nuclear division of mature oocytes should be an equational division similar to somatic mitosis. However, it seems premature to conclude that this has been unequivocally established in any daphnids. Therefore, the objective of our research was to precisely reveal the process and mechanism of parthenogenetic oogenesis and maintenance of diploidy in Daphnia pulex through histology, karyology, and immunohistochemistry. We found that, when a parthenogenetic egg entered the first meiosis, division was arrested in the early first anaphase. Then, two half-bivalents, which were dismembered from each bivalent, moved back to the equatorial plate and assembled to form a diploid equatorial plate. Finally, the sister chromatids were separated and moved to opposite poles in the same manner as the second meiotic division followed by the extrusion of one extremely small daughter cell (resembling a polar body). These results suggest that parthenogenetic D. pulex do not adopt typical apomixis. We hypothesize that D. pulex switches reproductive mode depending on whether the egg is fertilized or not.

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References

  • Bacci G, Cogneiti G, Vaccari AM (1961) Endomeiosis and sex determination in Daphnia pulex. Experientia 11:505–506

    Article  Google Scholar 

  • Beaton MJ, Hebert PDN (1994) Variation in chromosome numbers of Daphnia (Crustacea, Cladocera). Hereditas 120:275–279

    Article  Google Scholar 

  • Hebert PDN (1978) The population biology of Daphnia (Cruatacea, Daphnidae). Biol Rev 53:387–426

    Article  Google Scholar 

  • Hendzel MJ, Wei Y, Mancini MA, Hooser AV, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:348–360

    Article  CAS  PubMed  Google Scholar 

  • Itono M, Morishima K, Fujimoto T, Bando E, Yamaha E, Arai K (2006) Premeiotic endomitosis produces diploid eggs in the natural clone loach, Misgurnus anguilicautadus (Teleostei: Cobitidae). J Exp Zool 305A:513–523

    Article  CAS  Google Scholar 

  • Kühn A (1908) Die Entwicklung der Keimzellen in den parthenogenetischen Generationen der Cladoceren Daphnia pulex de Geer und Polyphemus pediculus de Geer. Arch Zellforsch 1:538–586

    Google Scholar 

  • Lachowska D, Rożek M, Holecová M (2008) New data on the cytology of parthenogenetic weevils (Coleoptera, Curculionidae). Genetica 134:235–242

    Article  PubMed  Google Scholar 

  • Lumer H (1937) Growth and maturation in the parthenogenetic eggs of Daphnia magna Strauss. Cytologia 8:1–14

    Google Scholar 

  • Narbel M (1946) La cytologie de la parthénogenèse chez Apterona helix Sieb. (Lepid, Psychides). Rev Suisse Zool 53:625–681

    Google Scholar 

  • Narbel-Hofstetter M (1950) La cytologie de la parthénogenèse chez Solinobia sp. (lichenella L.?) (Lépidoptères, Psychides). Chromosoma 4:56–90

    Article  CAS  PubMed  Google Scholar 

  • Narbel-Hofstetter M (1963) Cytologie de la pseudogamie chez Luffia lapidella Goeze (Lepidoptera, Psychidae). Chromosoma 13:623–645

    Article  Google Scholar 

  • Narbel-Hofstetter M (1965) La variabilité cytologique dans la descendance des femelles de Luffia ferchaultella Steph. (Lepidoptera, Psychidae). Chromosoma 16:345–350

    Article  CAS  PubMed  Google Scholar 

  • Ojima Y (1954) Some cytological observations on parthenogenesis in Daphnia pulex (de Geer). J Fac Sci Hokkaido Univ Ser VI, Zool 12:230–241

    Google Scholar 

  • Ojima Y (1958) A cytological study on the development and maturation of the parthenogenetic and sexual eggs of Daphnia pulex (Crustacea, Cladocera). Kwansei Gakuin Univ Annu Stud 6:123–176

    Google Scholar 

  • Otto SP, Barton NH (2001) Selection for recombination in small populations. Evolution 55:1921–1931

    CAS  PubMed  Google Scholar 

  • Peck JR (1994) A ruby in the rubbish: beneficial mutations, deleterious mutations and the evolution of sex. Genetics 137:597–606

    CAS  PubMed  Google Scholar 

  • Rożek M, Lachowska D, Milada H, Kajtoch Ł (2009) Karyology of parthenogenetic weevils (Coleoptera, Curculionidae): do meiotic prophase stages occur? Micron 40:881–885

    Article  PubMed  Google Scholar 

  • Sakai C, Konno F, Nakano O, Iwai T, Yokota T, Lee J, Nishida-Umehara C, Kuroiwa A, Matsuda Y, Yamashita M (2007) Chromosome elimination in the interspecific hybrid medaka between Oryzias latipes and O. hubbsi. Chromosome Res 15:697–709

    Article  CAS  PubMed  Google Scholar 

  • Sanderson AR (1952) Maturation and probable gynogenesis in the liver fluke, Fasciola hepatica L. Nature 172:110–112

    Article  Google Scholar 

  • Schurko AM, Logsdon JM Jr, Eads BD (2009) Meiosis genes in Daphnia pulex and the role of parthenogenesis in genome evolution. BMC Evol Biol 9:78

    Article  PubMed  Google Scholar 

  • Stefani R (1960) L’Artemia salina parthenogenetica a Cagliari. Riv Biol 52:463–490

    Google Scholar 

  • Sueoka N (1960) Mitotic replication of deoxyribonucleic acid in Chlamydomonas reinhardi. Proc Natl Acad Sci USA 46:83–91

    Article  CAS  PubMed  Google Scholar 

  • Suomalainen E, Saura A, Lokki J (1987) Cytology and evolution in parthenogenesis. CRC Press, Boca Raton

    Google Scholar 

  • Wei Y, Mizzen CA, Cook RG, Gorovsky MA, Allis CD (1998) Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena. Proc Natl Acad Sci USA 95:7480–7484

    Article  CAS  PubMed  Google Scholar 

  • Welch DM, Meselson M (2000) Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288:1211–1215

    Article  CAS  Google Scholar 

  • Zaffagnini F, Sabelli B (1972) Karyologic observations on the maturation of the summer and winter eggs of Daphnia pulex and Daphnia middendorffiana. Chromosoma 36(2):193–203

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We are grateful to Dr. Masakane Yamashita and his team, Faculty of Advanced Life Science, Hokkaido University, and Dr. Toru Miura and his team, Graduate School of Environmental Sciences, Hokkaido University, for helpful comments and suggestions on the study. We also thank the members of the Tochinai laboratory for their helpful advice and discussions. Chizue Hiruta was supported by a JSPS Research Fellowship for Young Scientists. This work was supported by a Grant-in-Aid for Exploratory Research, financed by the Ministry of Education, Culture, Sports, Science and Technology, Japan, to Shin Tochinai.

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Authors and Affiliations

  1. Department of Natural History Sciences, Graduate School of Science, Hokkaido University, Kita 10 Nishi 8, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan

    Chizue Hiruta, Chizuko Nishida & Shin Tochinai

  2. Department of Biological Sciences, Faculty of Science, Hokkaido University, Kita 10 Nishi 8, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan

    Chizuko Nishida

  3. Department of Natural History Sciences, Faculty of Science, Hokkaido University, Kita 10 Nishi 8, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan

    Shin Tochinai

  4. Department of Natural History Sciences, Graduate School of Science, Hokkaido University, Kita 10 Nishi 8, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan

    Chizue Hiruta

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  1. Chizue Hiruta
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  2. Chizuko Nishida
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  3. Shin Tochinai
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Correspondence to Chizue Hiruta.

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Responsible Editor: Yoichi Matsuda.

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Hiruta, C., Nishida, C. & Tochinai, S. Abortive meiosis in the oogenesis of parthenogenetic Daphnia pulex . Chromosome Res 18, 833–840 (2010). https://doi.org/10.1007/s10577-010-9159-2

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  • DOI: https://doi.org/10.1007/s10577-010-9159-2

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