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Co-segregation of sex chromosomes in the male black widow spider Latrodectus mactans (Araneae, Theridiidae)

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Abstract

During meiosis I, homologous chromosomes join together to form bivalents. Through trial and error, bivalents achieve stable bipolar orientations (attachments) on the spindle that eventually allow the segregation of homologous chromosomes to opposite poles. Bipolar orientations are stable through tension generated by poleward forces to opposite poles. Unipolar orientations lack tension and are stereotypically not stable. The behavior of sex chromosomes during meiosis I in the male black widow spider Latrodectus mactans (Araneae, Theridiidae) challenges the principles governing such a scenario. We found that male L. mactans has two distinct X chromosomes, X1 and X2. The X chromosomes join together to form a connection that is present in prometaphase I but is lost during metaphase I, before the autosomes disjoin at anaphase I. We found that both X chromosomes form stable unipolar orientations to the same pole that assure their co-segregation at anaphase I. Using micromanipulation, immunofluorescence microscopy, and electron microscopy, we studied this unusual chromosome behavior to explain how it may fit the current dogma of chromosome distribution during cell division.

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References

  • Araujo D, Maia UM, Brescovit AD (2010) The first cytogenetic characterization of the poisonous black widow spider Latrodectus gr. curacaviensis from Brazil, with chromosomal review of the family Theridiidae (Arachnida, Araneae). Micron 41:165–168

    Article  CAS  PubMed  Google Scholar 

  • Araujo D, Schneider MC, Paula-Neto E, Cella DM (2016) The spider cytogenetic database. Available: www.arthropodacytogenetics.bio.br/spiderdatabase

  • Ault JG (1984) Unipolar orientation stability of the sex univalent in the grasshopper (Melanoplus sanguinipes). Chromosoma 89:201–205

    Article  Google Scholar 

  • Ault JG (1986) Stable versus unstable orientations of sex chromosomes in two grasshopper species. Chromosoma 93:298–304

    Article  CAS  PubMed  Google Scholar 

  • Ault JG, Nicklas RB (1989) Tension, microtubule rearrangements, and proper distribution of chromosomes in mitosis. Chromosoma 98:33–39

    Article  CAS  PubMed  Google Scholar 

  • Ault JG, Rieder CL (1994) Meiosis in Drosophila males. I. The question of separate conjunctive mechanisms for the XY and autosomal bivalents. Chromosoma 103:352–356

    Article  CAS  PubMed  Google Scholar 

  • Benavente R, Wettstein R (1977) An ultrastructural cytogenetic study on the evolution of sex chromosomes during the spermatogenesis of Lycosa malitosa (Arachnida). Chromosoma 64:255–277

    Article  Google Scholar 

  • Fabig G, Müller-Reichert T, Paliulis LV (2016) Back to the roots: segregation of univalent sex chromosomes in meiosis. Chromosoma 125:277–286

    Article  PubMed  Google Scholar 

  • Hackman W (1948) Chromosomenstudien an Araneen mit besonderer Berucksichtigung der Geschlechtschromosomen. Acta Zool Fenn 54:1–101

    Google Scholar 

  • Hard WL (1939) The spermatogenesis of the lycosid spider Schizocosa crassipes (Walckenaer). J Morph 65:121–150

    Article  Google Scholar 

  • King JM, Nicklas RB (2000) Tension on chromosomes increases the number of kinetochore microtubules but only within limits. J Cell Sci 113(Pt 21):3815–3823

    CAS  PubMed  Google Scholar 

  • Král J, Korinkova T, Forman M, Krkavcova L (2011) Insights into the meiotic behavior and evolution of multiple sex chromosome systems in spiders. Cytogen Gen Res 133:43–66

    Article  Google Scholar 

  • Magidson V, He J, Ault JG, O’Connell CB, Yang N, McEwen BF, Sui H, Khodjakov A (2016) Unattached kinetochores rather than intrakinetochore tension arrest mitosis in taxol-treated cells. J Cell Biol 212:307–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martindale C (1980) Studies on Latrodectus. Proceedings of the Entomological Congress of the Entomological Society of Southern Africa 3:45–46

    Google Scholar 

  • McKee BD, Karpen GH (1990) Drosophila ribosomal RNA genes function as an X-Y meiotic pairing site during male meiosis. Cell 61:61–72

    Article  CAS  PubMed  Google Scholar 

  • Moens PB (1970) Serial sectioning in electron microscopy. Proc Can Fed Biol Soc 13:160

    Google Scholar 

  • Moore DP, Orr-Weaver TL (1998) Chromosome segregation during meiosis: building an unambivalent bivalent. Curr Top Dev Biol 37:263–299

    Article  CAS  PubMed  Google Scholar 

  • Nicklas RB (1961) Recurrent pole-to-pole movements of the sex chromosome during prometaphase I in Melanoplus differentialis spermatocytes. Chromosoma 12:97–115

    Article  CAS  PubMed  Google Scholar 

  • Nicklas RB (1963) A quantitative study of chromosomal elasticity and its influence on chromosome movement. Chromosoma 14:276–295

    Article  CAS  PubMed  Google Scholar 

  • Nicklas RB, Koch CA (1969) Chromosome micromanipulation. III. Spindle fiber tension and the reorientation of mal-oriented chromosomes. J Cell Biol 43:40–50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nicklas RB, Kubai DF (1985) Microtubules, chromosome movement, and reorientation after chromosomes are detached from the spindle by micromanipulation. Chromosoma 92:313–324

    Article  CAS  PubMed  Google Scholar 

  • Nicklas RB, Staehly CA (1967) Chromosome micromanipulation. I. The mechanics of chromosome attachment to the spindle. Chromosoma 21:1–16

    Article  CAS  PubMed  Google Scholar 

  • Nicklas RB, Ward SC (1994) Elements of error correction in mitosis: microtubule capture, release, and tension. J Cell Biol 126:1241–1253

    Article  CAS  PubMed  Google Scholar 

  • Nicklas EB, Brinkley BR, Pepper DA, Kubai DF, Richards GK (1979) Electron microscopy of spermatocytes previously studied in life: methods and some observation on micromanipulated chromosomes. J Cell Sci 35:87–104

    CAS  PubMed  Google Scholar 

  • Nicklas RB, Waters JC, Salmon ED, Ward SC (2001) Checkpoint signals in grasshopper meiosis are sensitive to microtubule attachment, but tension is still essential. J Cell Sci 114:4173–4183

    CAS  PubMed  Google Scholar 

  • Painter TS (1914) Spermatogenesis in spiders. Zool Jb 38:509–576

    Google Scholar 

  • Paliulis LV, Nicklas RB (2004) Micromanipulation of chromosomes reveals that cohesion release during cell division is gradual and does not require tension. Curr Biol 14:2124–2129

    Article  CAS  PubMed  Google Scholar 

  • Patau K (1948) X-segregation and heterochromasy in the spider Aranea reaumuri. Heredity 2:77–100

    Article  CAS  PubMed  Google Scholar 

  • Revell SH (1947) Controlled X-segregation at meiosis in Tegenaria. Heredity 1:337–347

    Article  Google Scholar 

  • Suzuki S (1954) Cytological studies in spiders. III. Studies on the chromosomes of fifty-seven species of spiders belonging to seventeen families with general consideration of chromosomal evolution. J Sci Hiroshima Univ Ser B, Div 15:23–136

    Google Scholar 

  • White MJD (1973) Animal cytology and evolution, 3rd edn. Cambridge University Press, London, p 960

    Google Scholar 

  • Wise D (1983) An electron microscope study of the karyotypes of two wolf spiders. Can J Gen Cyt 25:161–168

    Article  Google Scholar 

  • Zhao Y, Ayoub NA, Hayashi CY (2010) Chromosome mapping of dragline silk genes in the genomes of widow spiders (Araneae, Theridiidae). PLoS One 5:e12804

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank E. Stowe for valuable discussion of the manuscript and three anonymous reviewers for their constructive suggestions. We thank C. Kristensen at Spider Pharm for all of his assistance with spiders. The electron microscopy reported in this paper was performed at the Wadsworth Center’s Electron Microscopy Core Facility.

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Authors and Affiliations

  1. New York State Department of Health, Wadsworth Center, Albany, NY, 12201-0509, USA

    Jeffrey G. Ault

  2. Biology Department, Bucknell University, Lewisburg, PA, 17837, USA

    Kristen D. Felt, Ryan N. Doan, Alexander O. Nedo, Cassondra A. Ellison & Leocadia V. Paliulis

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  1. Jeffrey G. Ault
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  2. Kristen D. Felt
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  3. Ryan N. Doan
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  4. Alexander O. Nedo
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  5. Cassondra A. Ellison
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  6. Leocadia V. Paliulis
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Correspondence to Leocadia V. Paliulis.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

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Ault, J.G., Felt, K.D., Doan, R.N. et al. Co-segregation of sex chromosomes in the male black widow spider Latrodectus mactans (Araneae, Theridiidae). Chromosoma 126, 645–654 (2017). https://doi.org/10.1007/s00412-017-0628-7

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  • DOI: https://doi.org/10.1007/s00412-017-0628-7

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