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The cryptic Y-autosome translocation in the small Indian mongoose, Herpestes auropunctatus, revealed by molecular cytogenetic approaches

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Abstract

In initial studies of the eutherian small Indian mongoose (Herpestes auropunctatus), the Y chromosome could not be identified in somatic cells. The male chromosome number is uniquely odd, 2n = 35, whereas that of females is 2n = 36. Previous reports indicated that this unique karyotype resulted from a translocation of the ancestral Y chromosome to an autosome. However, it has been difficult to identify the chromosomes that harbor the translocated Y chromosomal segment because it is an extremely small euchromatic region. Using a Southern blot analysis, we detected four conserved Y-linked genes, SRY, EIF2S3Y, KDM5D, and ZFY, in the male genome. We cloned homologues of these genes and determined their sequences, which showed high homology to genes in two carnivore species, cat and dog. To unambiguously identify the Y-bearing autosome, we performed immunostaining of pachytene spermatocytes using antibodies against SYCP3, γH2AX, and the centromere. We observed trivalent chromosomes, and the associations between the distal ends of the chromosomes were consistent with those of Y and X1 chromosomes. The centromere of the Y chromosome was located on the ancestral Y chromosomal segment. We mapped the complementary DNA (cDNA) clones of these genes to the male chromosomes using fluorescence in situ hybridization (FISH), and the linear localization of all genes was confirmed by two-colored FISH. These Y-linked genes were localized to the proximal region of the long arm of a single telomeric chromosome, and we successfully identified the chromosome harboring the ancestral Y chromosomal segment.

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References

  • Barun A, Hanson CC, Campbell KJ, Simberloff D (2011) A review of small Indian mongoose management and eradications on islands. In: Veitch CR, Clout MN, Towns DR (eds) Island invasives: eradication and management. IUCN, Gland, pp 17–25

    Google Scholar 

  • Cohen MM, Chandra HS (1970) The somatic chromosomes of the small Indian mongoose: autoradiographic analysis of an unbalanced translocation heterozygote. Cytogenet 9:173–185

    Article  CAS  Google Scholar 

  • Davis BW, Raudsepp T, Pearks Wilkerson AJ, Agarwala R, Schäffer AA, Houck M, Chowdhary BP, Murphy WJ (2009) A high-resolution cat radiation hybrid and integrated FISH mapping resource for phylogenomic studies across Felidae. Genomics 93:299–304

    Article  CAS  PubMed  Google Scholar 

  • Fredga K (1965) A new sex determining mechanism in a mammal. Chromosomes of Indian mongoose (Herpestes auropunctatus). Hereditas 52:411–420

    Article  CAS  PubMed  Google Scholar 

  • Fredga K (1967) Chromosome studies in six different tissues of a male small Indian mongoose (Herpestes auropunctatus). Hereditas 57:421–431

    Article  CAS  PubMed  Google Scholar 

  • Fredga K (1970) Unusual sex chromosome inheritance in mammals. Philos Trans R Soc Lond B Biol Sci 259:15–36

    Article  CAS  PubMed  Google Scholar 

  • Fredga K (1972) Comparative chromosome studies in mongooses (Carnivora, Viverridae). I. Idiograms of 12 species and karyotype evolution in Herpestinae. Hereditas 71:1–74

    Article  CAS  PubMed  Google Scholar 

  • Gilchrist JS, Jennings AP, Veron G, Cavallini P (2009) Family Herpestidae (mongoose). In: Wilson DE, Mittermeier RA (eds) Handbook of the mammals of the world, vol 1, Carnivores. Lynx Editions, Barcelona, pp 262–328

    Google Scholar 

  • Ishishita S, Tsuboi K, Ohishi N, Tsuchiya K, Matsuda Y (2015) Abnormal pairing of X and Y sex chromosomes during meiosis I in interspecific hybrids of Phodopus campbelli and P. sungorus. Sci Rep 5:9435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kishida K (1931) Professor Watase and mongoose import. Zool Mag 43:70–78, in Japanese

    Google Scholar 

  • Kuroiwa, Ishiguchi Y, Yamada F, Shintaro A, Matsuda Y (2010) The process of a Y-loss event in an XO/XO mammal, the Ryukyu spiny rat. 119:519–526

  • Li G, Davis BW, Raudsepp T, Pearks Wilkerson AJ, Mason VC, Ferguson-Smith M, O’Brien PC, Waters PD, Murphy WJ (2013) Comparative analysis of mammalian Y chromosomes illuminates ancestral structure and lineage-specific evolution. 23:1486–1495

  • Matsuda Y, Chapman VM (1995) Application of fluorescence in situ hybridization in genome analysis of the mouse. Electrophoresis 16:261–272

    Article  CAS  PubMed  Google Scholar 

  • Matsuda Y, Harada YN, Natsuume-Sakai S, Lee K, Shiomi T, Chapman VM (1992) Location of the mouse compliment factor H gene (cfh) by FISH analysis and replication R-banding. Cytogenet Cell Genet 61:282–285

    Article  CAS  PubMed  Google Scholar 

  • Murata C, Yamada F, Kawauchi N, Matsuda Y, Kuroiwa A (2010) Multiple copies of SRY on the large Y chromosome of the Okinawa spiny rat, Tokudaia muenninki. Chromosome Res 18:623–634

    Article  CAS  PubMed  Google Scholar 

  • Murata C, Ogura G, Kuroiwa A (2011) A primer set to determine sex in the small Indian mongoose, Herpestes auropunctatus. Mol Ecol Resour 11:386–388

    Article  CAS  PubMed  Google Scholar 

  • Patou ML, Mclenachan PA, Morley CG, Couloux A, Jennings AP, Veron G (2009) Molecular phylogeny of the Herpestidae (Mammalia, Carnivora) with a special emphasis on the Asian Herpestes. Mol Phylogenet Evol 53:69–80

    Article  CAS  PubMed  Google Scholar 

  • Perez M, Li B, Tillier A, Cruaud A, Veron G (2006) Systematic relationships of the bushy-tailed and black-footed mongooses (genus Bdeogale, Herpestidae, Carnivora) based on molecular, chromosomal and morphological evidence. JZS 44:251–259

    Google Scholar 

  • Peters AH, Plug AW, van Vugt MJ, de Boer P (1997) A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res 5:66–68

    Article  CAS  PubMed  Google Scholar 

  • Raman R, Nanda I (1982) Identification and patterns of synapsis of the autosomally translocated Y-chromosome of the Indian mongoose, Herpestes auropunctatus (Hodgson). Chromosoma 87:477–489

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sekiguchi K, Inoue F, Ueda T, Ogura G, Kawashima Y (2001) Genealogical relationship between introduced mongooses in Okinawa and Amamiohsima Islands, Ryukyu Archipelago, inferred from sequences of mtDNA cytochrome b gene. Mammal Sci 41:65–70, in Japanese with English summary

    Google Scholar 

  • Sen S, Sharma T (1979) Sparse distribution of constitutive heterochromatin and its variation in two species of mongooses (Carnivora) with exact G-band homology. Genetica 50:221–226

    Article  Google Scholar 

  • Simberloff DT, Dayan C, Jones C, Ogura G (2000) Character displacement and release in the small Indian mongoose, Herpestes javanicus. Ecology 81:2086–2099

    Article  Google Scholar 

  • Thulin CG, Simberloff D, Barun A, Mccracken G, Pascal M, Islam MA (2006) Genetic divergence in the small Indian mongoose (Herpestes auropunctatus), a widely distributed invasive species. Mol Ecol 15:3947–3956

    Article  CAS  PubMed  Google Scholar 

  • Veron G, Patou ML, Pothet G, Simberloff D, Jennings AP (2007) Systematic status and biogeography of the Javan and small Indian mongooses (Herpestidae, Carnivora). Zool Scr 36:1–10

    Article  Google Scholar 

  • Waters PD, Wallis MC, Marshall Graves JA (2007) Mammalian sex—Origin and evolution of the Y chromosome and SRY. Semin Cell Dev Biol 18:389–400

    Article  CAS  PubMed  Google Scholar 

  • Yamada F, Sugimura K (2004) Negative impact of an invasive small Indian mongoose Herpestes javanicus on native wildlife species and evaluation of a control project in Amami-Oshima and Okinawa Islands, Japan. Global Environ Res 8:117–124

    Google Scholar 

  • Yamada F, Ogura G, Abe S (2015) Herpestes auropunctatus (Hodgson, 1836). In: Ohdachi SD, Ishibashi Y, Iwasa MA, Saitoh T (eds) The wild mammals of Japan, 2nd edn. Shoukadoh Book Sellers, Kyoto, pp 272–274

    Google Scholar 

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Acknowledgments

The authors thank S. Ishishita, K. Matsubara, and Yoichi Matsuda for their advice on the drying-down technique and cell culture. We also thank C. Nishida-Umehara and T. Kudo for preparing chromosomes and collecting data and S. Abe for the kind help with sampling.

Authors’ contribution

CM conducted molecular experiments and immunostaining. FS contributed to the majority of the cytogenetic experiments and Southern blot analysis. FY and KN captured animals and performed sampling. II commented on the final version of the paper. AK designed the study and analyzed the data, and wrote the manuscript. All authors discussed the results and approved the final version of the manuscript.

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Authors and Affiliations

  1. Department of Human Genetics, Institute of Biomedical Sciences, Tokushima University Graduate School, 3-18-15 Kuramoto-cho, Tokushima, 770-8503, Japan

    Chie Murata & Issei Imoto

  2. Graduate School of Life Science, Hokkaido University, North 10, West 8, Kita-ku, Sapporo, 060-0810, Japan

    Hirohito Sawaya

  3. Yambaru Wildlife Conservation Center, Ministry of the Environment, 263-1 Hiji, Kunigami-son, Kunigami-gun, Okinawa, 905-1413, Japan

    Katsushi Nakata

  4. Forestry and Forest Products Research Institute, Matsunosato 1, Tsukuba, Ibaraki, 305-8687, Japan

    Fumio Yamada

  5. Laboratory of Animal Cytogenetics, Faculty of Science, Hokkaido University, Kita 10 Nishi 8, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan

    Asato Kuroiwa

Authors
  1. Chie Murata
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  2. Hirohito Sawaya
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  3. Katsushi Nakata
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  4. Fumio Yamada
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  5. Issei Imoto
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  6. Asato Kuroiwa
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Corresponding author

Correspondence to Asato Kuroiwa.

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Ethical approval

All the animal experiments in this study were approved by Institutional Animal Care and Use Committee of National University Corporation Hokkaido University and were performed in accordance with the Guidelines for the Care and Use of Laboratory Animals, Hokkaido University. This article does not contain any studies on human participants by any of the authors.

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The authors declare that they have no competing interests.

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Murata, C., Sawaya, H., Nakata, K. et al. The cryptic Y-autosome translocation in the small Indian mongoose, Herpestes auropunctatus, revealed by molecular cytogenetic approaches. Chromosoma 125, 807–815 (2016). https://doi.org/10.1007/s00412-015-0572-3

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  • DOI: https://doi.org/10.1007/s00412-015-0572-3

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