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Chromosome Research

, Volume 26, Issue 4, pp 243–253 | Cite as

Clonal reproduction assured by sister chromosome pairing in dojo loach, a teleost fish

  • Masamichi KurodaEmail author
  • Takafumi Fujimoto
  • Masaru Murakami
  • Etsuro Yamaha
  • Katsutoshi Arai
Original Article

Abstract

Wild-type dojo loach (Misgurnus anguillicaudatus) commonly reproduces bisexually as a gonochoristic diploid (2n = 50), but gynogenetically reproducing clonal diploid lines (2n = 50) exist in certain districts in Japan. Clones have been considered to develop from past hybridization event(s) between two genetically diverse groups, A and B, within the species. Fluorescence in situ hybridization analyses using the repetitive sequence “ManDra” as a probe clearly distinguished 25 chromosomes derived from group B out of a total of 50 diploid chromosomes of the clone, providing strong molecular cytogenetic evidence of its hybrid origin. In meiosis, diploid wild-type showed 25 bivalents, while diploid clones revealed 50 bivalents, indicating the presence of 100 chromosomes. In meiotic chromosome spreads in sex-reversed clonal males, ManDra signals were detected in 25 out of 50 bivalents, and only one out of two bivalents possessing major ribosomal RNA coding regions exhibited two positive ManDra signals. In clonal females, ManDra signals were detected in approximately 25 out of 50 bivalents. Thus, unreduced gametes should be generated by the pairing between sister chromosomes doubled from each ancestral chromosome from the different groups by premeiotic endomitosis. Sister chromosome pairing should assure production of unreduced isogenic clonal gametes due to the absence of the influence of recombination or crossing over.

Keywords

Clone FISH Hybrid Premeiotic endomitosis Sister chromosome Unreduced gametes 

Abbreviations

DAPI

4′, 6-Diamidino-2-phenylindole, dihydrochloride

FISH

Fluorescence in situ hybridization

GISH

Genomic in situ hybridization

GV

Germinal vesicle

IRBP2

Interphotoreceptor retinoid binding protein 2

mtDNA-CR

Mitochondrial DNA control region

NORs

Nucleolar organizing regions

RAG1

Recombination activating gene 1

rDNA

Ribosomal DNA

SSC

Saline sodium citrate buffer

tRNA

Transfer RNA

Notes

Acknowledgments

We thank Dr. Atsushi Fujiwara (National Research Institute of Fisheries Science, Japan Fisheries Research and Education Agency) for technical advice. This study was supported by Grants-in-Aid from JSPS (Japan Society for the Promotion of Science) KAKENHI Grant Number 15H02457 and JSPS Research Fellow Number 17J01971.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Ethical approval

This study was performed according to the Guide for the Care and Use of Laboratory Animals at Hokkaido University. All animal experiments were approved by the animal study ethical committee of Hokkaido University (approval number 19-2).

Supplementary material

10577_2018_9581_MOESM1_ESM.pdf (123 kb)
Table S1 (PDF 122 kb)
10577_2018_9581_MOESM2_ESM.pdf (111 kb)
Table S2 (PDF 110 kb)
10577_2018_9581_MOESM3_ESM.pdf (110 kb)
Table S3 (PDF 109 kb)
10577_2018_9581_MOESM4_ESM.pdf (114 kb)
Table S4 (PDF 113 kb)
10577_2018_9581_MOESM5_ESM.pdf (281 kb)
Fig. S1 (PDF 281 kb)

References

  1. Arai K, Fujimoto T (2013) Genomic constitution and atypical reproduction in polyploid and unisexual lineages of the Misgurnus loach, a teleost fish. Cytogenet Genome Res 140(2–4):226–240.  https://doi.org/10.1159/000353301 CrossRefPubMedGoogle Scholar
  2. Arai K, Mukaino M (1997) Clonal nature of gynogenetically induced progeny of triploid (diploid × tetraploid) loach, Misgurnus anguillicaudatus (Pisces: Cobitididae). J Exp Zool 278(6):412–421.  https://doi.org/10.1002/(SICI)1097-010X(19970815)278:6<412::AID-JEZ9>3.0.CO;2-R CrossRefGoogle Scholar
  3. Arias-Rodriguez L, Morishima K, Arai K (2007) Genetically diversified populations in the loach Misgurnus anguillicaudatus inferred from newly developed microsatellite markers. Mol Ecol Notes 7(1):82–85.  https://doi.org/10.1111/j.1471-8286.2006.01536.x CrossRefGoogle Scholar
  4. Arias-Rodriguez L, Yasui GS, Arai K (2009) Disruption of normal meiosis in artificial inter-populational hybrid females of Misgurnus loach. Genetica 136(1):49–56.  https://doi.org/10.1007/s10709-008-9299-x CrossRefPubMedGoogle Scholar
  5. Beukeboom LW, Vrijenhoek RC (1998) Evolutionary genetics and ecology of sperm-dependent parthenogenesis. J Evol Biol 11(6):755–782CrossRefGoogle Scholar
  6. Bi K, Bogart JP (2006) Identification of intergenomic recombinations in unisexual salamanders of the genus Ambystoma by genomic in situ hybridization (GISH). Cytogenet Genome Res 112(3–4):307–312.  https://doi.org/10.1159/000089885 CrossRefPubMedGoogle Scholar
  7. Cherfas NB (1966) Natural triploidy in females of the unisexual form of silver crucian carp (Carassius auratus gibelio Bloch). Genetika 5:16–24Google Scholar
  8. Cherfas NB, Gomelsky BI, Emelyanova OV, Recoubratsky AV (1994) Induced diploid gynogenesis and polyploidy in crucian carp, Carassius auratus gibelio (Bloch), × common carp, Cyprinus carpio L., hybrids. Aquac Res 25(9):943–954.  https://doi.org/10.1111/j.1365-2109.1994.tb01356.x CrossRefGoogle Scholar
  9. Chevassus B (1983) Hybridization in fish. Aquaculture 33(1):245–262.  https://doi.org/10.1016/0044-8486(83)90405-2 CrossRefGoogle Scholar
  10. Choleva L, Janko K, Gelas KD et al (2012) Synthesis of clonality and polyploidy in vertebrate animals by hybridization between two sexual species. Evolution 66(7):2191–2203.  https://doi.org/10.1111/j.1558-5646.2012.01589.x CrossRefPubMedGoogle Scholar
  11. Collares-Pereira MJ, Matos I, Morgado-Santos M, Coelho MM (2013) Natural pathways towards polyploidy in animals: the Squalius alburnoides fish complex as a model system to study genome size and genome reorganization in polyploids. Cytogenet Genome Res 140(2–4):97–116.  https://doi.org/10.1159/000351729 CrossRefPubMedGoogle Scholar
  12. Dawley RM (1987) Hybridization and polyploidy in a community of three sunfish species (Pisces: Centrarchidae). Copeia 1987(2):326–335.  https://doi.org/10.2307/1445768 CrossRefGoogle Scholar
  13. Dawley RM (1989) An introduction to unisexual vertebrates. In: Dawley RM, Bogart JP (eds) Evolution and ecology of unisexual vertebrates. New York State Museum, Albany, New York, pp 1–18Google Scholar
  14. Fujimoto T, Yamada A, Kodo Y, Nakaya K, Okubo-Murata M, Saito T, Ninomiya K, Inaba M, Kuroda M, Arai K, Murakami M (2017) Development of nuclear DNA markers to characterize genetically diverse groups of Misgurnus anguillicaudatus and its closely related species. Fish Sci 83(5):743–756.  https://doi.org/10.1007/s12562-017-1108-y CrossRefGoogle Scholar
  15. Fujiwara A, Abe S, Yamaha E, Yamazaki F, Yoshida CM (1998) Chromosomal localization and heterochromatin association of ribosomal RNA gene loci and silver-stained nucleolar organizer regions in salmonid fishes. Chromosom Res 6(6):463–471.  https://doi.org/10.1023/A:1009200428369 CrossRefGoogle Scholar
  16. Goddard KA, Dawley RM (1990) Clonal inheritance of a diploid nuclear genome by a hybrid freshwater minnow (Phoxinus eos-neogaeus, Pisces:Cyprinidae). Evolution 44(4):1052–1065.  https://doi.org/10.1111/j.1558-5646.1990.tb03825.x CrossRefPubMedGoogle Scholar
  17. Goddard KA, Megwinoff O, Wessner LL, Giaimo F (1998) Confirmation of gynogenesis in Phoxinus eos-neogaeus (Pisces:Cyprinidae). J Hered 89(2):151–157.  https://doi.org/10.1093/jhered/89.2.151 CrossRefGoogle Scholar
  18. Islam FB, Ishishita S, Uno Y, Mollah MBR, Srikulnath K, Matsuda Y (2013) Male hybrid sterility in the mule duck is associated with meiotic arrest in primary spermatocytes. Journal of Poultry Science 50(4):311–320.  https://doi.org/10.2141/jpsa.0130011 CrossRefGoogle Scholar
  19. Itono M, Morishima K, Fujimoto T, Bando E, Yamaha E, Arai K (2006) Premeiotic endomitosis produces diploid eggs in the natural clone loach, Misgurnus anguillicaudatus (Teleostei: Cobitidae). J Exp Zool A Comp Exp Biol 305(6):513–523.  https://doi.org/10.1002/jez.a.283 CrossRefPubMedGoogle Scholar
  20. Itono M, Okabayashi N, Morishima K, Fujimoto T, Yoshikawa H, Yamaha E, Arai K (2007) Cytological mechanisms of gynogenesis and sperm incorporation in unreduced diploid eggs of the clonal loach, Misgurnus anguillicaudatus (Teleostei: Cobitidae). J Exp Zool A Comp Exp Biol 307(1):35–50.  https://doi.org/10.1002/jez.a.344 CrossRefGoogle Scholar
  21. Janko K, Bohlen J, Lamatsch D, Flajšhans M, Epplen JT, Ráb P, Kotlík P, Šlechtová V (2007) The gynogenetic reproduction of diploid and triploid hybrid spined loaches (Cobitis:Teleostei), and their ability to establish successful clonal lineages—on the evolution of polyploidy in asexual vertebrates. Genetica 131(2):185–194.  https://doi.org/10.1007/s10709-006-9130-5 CrossRefPubMedGoogle Scholar
  22. Johnson KR, Wright JE (1986) Female brown trout × Atlantic salmon hybrids produce gynogens and triploids when backcrossed to male Atlantic salmon. Aquaculture 57(1):345–358.  https://doi.org/10.1016/0044-8486(86)90213-9 CrossRefGoogle Scholar
  23. Khan MR, Arai K (2000) Allozyme variation and genetic differentiation in the loach Misgurnus anguillicaudatus. Fish Sci 66(2):211–222.  https://doi.org/10.1046/j.1444-2906.2000.00037.x CrossRefGoogle Scholar
  24. Knytl M, Kalous L, Symonová R, Rylková K, Ráb P (2013) Chromosome studies of European cyprinid fishes: cross-species painting reveals natural allotetraploid origin of a Carassius female with 206 chromosomes. Cytogenet Genome Res 139(4):276–283.  https://doi.org/10.1159/000350689 CrossRefPubMedGoogle Scholar
  25. Kobel HR, Du Pasquier L (1975) Production of large clones of histocompatible, fully identical clawed toads (Xenopus). Immunogenetics 2:87–91.  https://doi.org/10.1007/BF01572278 CrossRefGoogle Scholar
  26. Kobel HR, Du Pasquier L (1979) Hyperdiploid species hybrids for gene mapping in Xenopus. Nature 279:157–158.  https://doi.org/10.1038/279157a0 CrossRefPubMedGoogle Scholar
  27. Lamatsch DK, Stöck M (2009) Sperm-dependent parthenogenesis and hybridogenesis in teleost fishes. In: Schön I, Martens K, Dijk P (eds) Lost sex: the evolutionary biology of parthenogenesis. Springer, Dordrecht, pp 399–432CrossRefGoogle Scholar
  28. Li YJ, Tian Y, Zhang MZ, Tian PP, Yu Z, Abe S, Arai K (2010) Chromosome banding and FISH with rDNA probe in the diploid and tetraploid loach Misgurnus anguillicaudatus. Ichthyol Res 57(4):358–366.  https://doi.org/10.1007/s10228-010-0168-0 CrossRefGoogle Scholar
  29. Li YJ, Yu Z, Zhang MZ, Qian C, Abe S, Arai K (2011) The origin of natural tetraploid loach Misgurnus anguillicaudatus (Teleostei: Cobitidae) inferred from meiotic chromosome configurations. Genetica 139(6):805–811.  https://doi.org/10.1007/s10709-011-9585-x CrossRefPubMedGoogle Scholar
  30. Li YJ, Yu Z, Zhang MZ, Qian C, Abe S, Arai K (2012) Induction of viable gynogenetic progeny using eggs and UV-irradiated sperm from the Chinese tetraploid loach, Misgurnus anguillicaudatus. Aquac Int 21(4):759–768.  https://doi.org/10.1007/s10499-012-9551-3 CrossRefGoogle Scholar
  31. Li YJ, Gao YC, Zhou H, Ma HY, Li JQ, Arai K (2015) Meiotic chromosome configurations in triploid progeny from reciprocal crosses between wild-type diploid and natural tetraploid loach Misgurnus anguillicaudatus in China. Genetica 143(5):555–562.  https://doi.org/10.1007/s10709-015-9853-2 CrossRefPubMedGoogle Scholar
  32. Li YJ, Gao YC, Zhou H, Ma HY, Lin ZQ, Ma TY, Sui Y, Arai K (2016) Aneuploid progenies of triploid hybrids between diploid and tetraploid loach Misgurnus anguillicaudatus in China. Genetica 144(5):601–609.  https://doi.org/10.1007/s10709-016-9928-8 CrossRefPubMedGoogle Scholar
  33. Liu S, Liu Y, Zhou G, Zhang X, Luo C, Feng H, He X, Zhu G, Yang H (2001) The formation of tetraploid stocks of red crucian carp × common carp hybrids as an effect of interspecific hybridization. Aquaculture 192(2):171–186.  https://doi.org/10.1016/S0044-8486(00)00451-8 CrossRefGoogle Scholar
  34. Lutes AA, Neaves WB, Baumann DP, Wiegraebe W, Baumann P (2010) Sister chromosome pairing maintains heterozygosity in parthenogenetic lizards. Nature 464:283–286.  https://doi.org/10.1038/nature08818 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Majtanova Z, Choleva L, Symonová R et al (2016) Asexual reproduction does dot apparently increase the rate of chromosomal evolution: karyotype stability in diploid and triploid clonal hybrid fish (Cobitis, Cypriniformes, Teleostei). PLoS One 11(1):e0146872.  https://doi.org/10.1371/journal.pone.0146872 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Morishima K, Horie S, Yamaha E, Arai K (2002) A cryptic clonal line of the loach Misgurnus anguillicaudatus (Teleostei: Cobitidae) evidenced by induced gynogenesis, interspecific hybridization, microsatellite genotyping and multilocus DNA fingerprinting. Zool Sci 19(5):565–575.  https://doi.org/10.2108/zsj.19.565 CrossRefPubMedGoogle Scholar
  37. Morishima K, Nakamura-Shiokawa Y, Bando E, Li YJ, Boroń A, Khan MMR, Arai K (2008) Cryptic clonal lineages and genetic diversity in the loach Misgurnus anguillicaudatus (Teleostei: Cobitidae) inferred from nuclear and mitochondrial DNA analyses. Genetica 132(2):159–171.  https://doi.org/10.1007/s10709-007-9158-1 CrossRefPubMedGoogle Scholar
  38. Morishima K, Yoshikawa H, Arai K (2012) Diploid clone produces unreduced diploid gametes but tetraploid clone generates reduced diploid gametes in the Misgurnus loach. Biol Reprod 86(2):1–8.  https://doi.org/10.1095/biolreprod.111.093302 CrossRefGoogle Scholar
  39. Moritz C, Brown WM, Densmore LD et al (1989) Genetic diversity and the dynamics of hybrid parthenogenesis in Cnemidophorus (Teiidae) and Heteronotia (Gekkonidae). In: Dawley RM, Bogart JP (eds) Evolution and ecology of unisexual vertebrates. New York State Museum, Albany, New York, pp 87–112Google Scholar
  40. Ogielska M (2009) Development and reproduction of amphibian species, hybrids, and polyploids. In: Ogielska M (ed) Reproduction of amphibians. Science Publishers, New Hampshire, pp 343–410CrossRefGoogle Scholar
  41. Rampin M, Bi K, Bogart JP, Collares-Pereira MJ (2012) Identifying parental chromosomes and genomic rearrangements in animal hybrid complexes of species with small genome size using genomic in situ hybridization (GISH). Comp Cytogenet 6(3):287–300.  https://doi.org/10.3897/CompCytogen.v6i3.3543 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Schultz RJ (1967) Gynogenesis and triploidy in the viviparous fish Poeciliopsis. Science 157(3796):1564–1567.  https://doi.org/10.1126/science.157.3796.1564 CrossRefPubMedGoogle Scholar
  43. Schultz RJ (1969) Hybridization, unisexuality, and polyploidy in the teleost Poeciliopsis (Poeciliidae) and other vertebrates. Am Nat 103(934):605–619.  https://doi.org/10.1086/282629 CrossRefGoogle Scholar
  44. Shimizu Y, Shibata N, Sakaizumi M, Yamashita M (2000) Production of diploid eggs through premeiotic endomitosis in the hybrid medaka between Oryzias latipes and O. curvinotus. Zool Sci 17(7):951–958.  https://doi.org/10.2108/zsj.17.951 CrossRefGoogle Scholar
  45. Vrijenhoek RC (1994) Unisexual fish: model systems for studying ecology and evolution. Annu Rev Ecol Syst 25(1):71–96CrossRefGoogle Scholar
  46. Yamada A, Kodo Y, Murakami M, Kuroda M, Aoki T, Fujimoto T, Arai K (2015) Hybrid origin of gynogenetic clones and the introgression of their mitochondrial genome into sexual diploids through meiotic hybridogenesis in the loach, Misgurnus anguillicuadatus. J Exp Zool A Ecol Genet Physiol 323(9):593–606.  https://doi.org/10.1002/jez.1950 CrossRefPubMedGoogle Scholar
  47. Yamashita M, Jiang J, Onozato H, Nakanishi T, Nagahama Y (1993) A tripolar spindle formed at meiosis I assures the retention of the original ploidy in the gynogenetic triploid crucian carp, ginbuna Carassius auratus langsdorfii. Develop Growth Differ 35(6):631–636.  https://doi.org/10.1111/j.1440-169X.1993.00631.x CrossRefGoogle Scholar
  48. Yoshikawa H, Morishima K, Kusuda S, Yamaha E, Arai K (2007) Diploid sperm produced by artificially sex-reversed clone loaches. J Exp Zool A Ecol Genet Physiol 307(2):75–83.  https://doi.org/10.1002/jez.a.337 CrossRefPubMedGoogle Scholar
  49. Yoshikawa H, Morishima K, Fujimoto T, Saito T, Kobayashi T, Yamaha E, Arai K (2009) Chromosome doubling in early spermatogonia produces diploid spermatozoa in a natural clonal fish. Biol Reprod 80(5):973–979.  https://doi.org/10.1095/biolreprod.108.075150 CrossRefPubMedGoogle Scholar
  50. Zalesna A, Choleva L, Ogielska M, Rábová M, Marec F, Ráb P (2011) Evidence for integrity of parental genomes in the diploid hybridogenetic water frog Pelophylax esculentus by genomic in situ hybridization. Cytogenet Genome Res 134(3):206–212.  https://doi.org/10.1159/000327716 CrossRefPubMedGoogle Scholar
  51. Zhang Q, Arai K, Yamashita M (1998) Cytogenetic mechanisms for triploid and haploid egg formation in the triploid loach Misgurnus anguillicaudatus. J Exp Zool 281(6):608–619.  https://doi.org/10.1002/(SICI)1097-010X(19980815)281:6<608::AID-JEZ9>3.0.CO;2-R CrossRefGoogle Scholar

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© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Faculty and Graduate School of Fisheries SciencesHokkaido UniversityHakodateJapan
  2. 2.Japan Society for the Promotion of ScienceTokyoJapan
  3. 3.School of Veterinary MedicineAzabu UniversitySagamiharaJapan
  4. 4.Nanae Fresh-Water Laboratory, Field Science Center for Northern BiosphereHokkaido UniversityNanaeJapan

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