More sex chromosomes than autosomes in the Amazonian frog Leptodactylus pentadactylus

Abstract

Heteromorphic sex chromosomes are common in eukaryotes and largely ubiquitous in birds and mammals. The largest number of multiple sex chromosomes in vertebrates known today is found in the monotreme platypus (Ornithorhynchus anatinus, 2n = 52) which exhibits precisely 10 sex chromosomes. Interestingly, fish, amphibians, and reptiles have sex determination mechanisms that do or do not involve morphologically differentiated sex chromosomes. Relatively few amphibian species carry heteromorphic sex chromosomes, and when present, they are frequently represented by only one pair, either XX:XY or ZZ:ZW types. Here, in contrast, with several evidences, from classical and molecular cytogenetic analyses, we found 12 sex chromosomes in a Brazilian population of the smoky jungle frog, designated as Leptodactylus pentadactylus Laurenti, 1768 (Leptodactylinae), which has a karyotype with 2n = 22 chromosomes. Males exhibited an astonishing stable ring-shaped meiotic chain composed of six X and six Y chromosomes. The number of sex chromosomes is larger than the number of autosomes found, and these data represent the largest number of multiple sex chromosomes ever found among vertebrate species. Additionally, sequence and karyotype variation data suggest that this species may represent a complex of species, in which the chromosomal rearrangements may possibly have played an important role in the evolution process.

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Acknowledgements

We thank Natalia Maria Espíndola Salles, Juliano Mafra Neves, and Karll Cavalcante Pinto for help in field work, and to João Rodrigo Cabeza as well as Companhia Hidrelétrica Teles Pires for allowing collecting activities in their study areas. We are grateful to Heidi Horn, for a revision in the final version of this manuscript. TG thanks Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio – SISBIO) for providing a collection permit (no. 30202-2). The authors are also grateful to the Centro de Estudos de Insetos Sociais, UNESP – Univ. Estadual Paulista, Rio Claro, Brazil, for allowing the utilization of facilities for molecular analyses.

Funding

This work was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES, which provided a PhD fellowship to TG, by Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq for research funding (no. 473264/212-9) to PPPM, and by São Paulo Research Foundation (FAPESP) for a research grant (no. 2013/50741–7) to CFBH. CNPq provided a research fellowship to CFBH.

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T. G., P. P. P. M., and C. F. B. H. designed the study. T. G. performed the cytogenetic analyses. D. C. C. M. assisted on microsatellite and CGH experiments. M. L. L. performed DNA sequencing and similarity analyses. T. G. and H. N. collected the specimens. T. G. and P. P. P. M. wrote the main manuscript, and all authors contributed to improve it. All authors approved the final version of the manuscript.

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Correspondence to P. P. Parise-Maltempi.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

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Gazoni, T., Haddad, C.F.B., Narimatsu, H. et al. More sex chromosomes than autosomes in the Amazonian frog Leptodactylus pentadactylus. Chromosoma 127, 269–278 (2018). https://doi.org/10.1007/s00412-018-0663-z

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Keywords

  • Meiotic multivalents
  • Multiple sex chromosomes
  • Translocations
  • Amphibia
  • Leptodactylidae