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Complex meiotic configuration of the holocentric chromosomes: the intriguing case of the scorpion Tityus bahiensis

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Abstract

Mitotic and meiotic chromosomes of Tityus bahiensis were investigated using light (LM) and transmission electron microscopy (TEM) to determine the chromosomal characteristics and disclose the mechanisms responsible for intraspecific variability in chromosome number and for the presence of complex chromosome association during meiosis. This species is endemic to Brazilian fauna and belongs to the family Buthidae, which is considered phylogenetically basal within the order Scorpiones. In the sample examined, four sympatric and distinct diploid numbers were observed: 2n = 5, 2n = 6, 2n = 9, and 2 = 10. The origin of this remarkable chromosome variability was attributed to chromosome fissions and/or fusions, considering that the decrease in chromosome number was concomitant with the increase in chromosome size and vice versa. The LM and TEM analyses showed the presence of chromosomes without localised centromere, the lack of chiasmata and recombination nodules in male meiosis, and two nucleolar organiser regions carrier chromosomes. Furthermore, male prophase I cells revealed multivalent chromosome associations and/or unsynapsed or distinctly associated chromosome regions (gaps, less-condensed chromatin, or loop-like structure) that were continuous with synapsed chromosome segments. All these data permitted us to suggest that the chromosomal rearrangements of T. bahiensis occurred in a heterozygous state. A combination of various factors, such as correct disjunction and balanced segregation of the chromosomes involved in complex meiotic pairing, system of achiasmate meiosis, holocentric nature of the chromosomes, population structure, and species dispersion patterns, could have contributed to the high level of chromosome rearrangements present in T. bahiensis.

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Abbreviations

CV:

Coefficient of variation

DSL:

Diploid set length

LM:

Light microscopy

NOR:

Nucleolar organiser region

PTA:

Phosphotungstic acid

SC:

Synaptonemal complex

TEM:

Transmission electron microscopy

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Acknowledgements

We are indebted to two anonymous reviewers for critical reading and valuable suggestions for the manuscript. The authors are also grateful to the Centro de Controle de Zoonoses, from Piracicaba, SP, Brazil, for collecting T. bahiensis. Furthermore, we would like to thank Dr. Flávio H. Caetano and Antonio T. Yabuki, both from the Centro de Microscopia Eletrônica, Departamento de Biologia, Instituto de Biociências, UNESP, Rio Claro, SP, Brazil, for providing access to the infrastructure required for ultrastructural analysis and for technical assistance, respectively. This research was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo, FAPESP (06/53275-3).

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Authors and Affiliations

  1. Departamento de Ciências Biológicas, Universidade Federal de São Paulo, UNIFESP, Av. Prof. Artur Riedel, 275, 09972-270, Diadema, São Paulo, Brazil

    Marielle Cristina Schneider

  2. Departamento de Biologia, Universidade Estadual Paulista, UNESP, Avenida 24-A, 1515, Caixa Postal 199, 13506-900, Rio Claro, São Paulo, Brazil

    Doralice Maria Cella

  3. Departamento de Biologia Geral, Universidade Federal de Viçosa, UFV, Viçosa, Minas Gerais, Brazil

    Adilson Ariza Zacaro

  4. Departamento de Zoologia, Universidade de São Paulo, USP, São Paulo, São Paulo, Brazil

    Ricardo Pinto-da-Rocha

  5. Instituto Butantan, Laboratório de Artrópodes, São Paulo, São Paulo, Brazil

    Denise Maria Candido

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  1. Marielle Cristina Schneider
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  2. Adilson Ariza Zacaro
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  3. Ricardo Pinto-da-Rocha
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Correspondence to Marielle Cristina Schneider.

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Schneider, M.C., Zacaro, A.A., Pinto-da-Rocha, R. et al. Complex meiotic configuration of the holocentric chromosomes: the intriguing case of the scorpion Tityus bahiensis . Chromosome Res 17, 883–898 (2009). https://doi.org/10.1007/s10577-009-9076-4

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