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New insights into sex chromosome evolution in anole lizards (Reptilia, Dactyloidae)

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Abstract

Anoles are a clade of iguanian lizards that underwent an extensive radiation between 125 and 65 million years ago. Their karyotypes show wide variation in diploid number spanning from 26 (Anolis evermanni) to 44 (A. insolitus). This chromosomal variation involves their sex chromosomes, ranging from simple systems (XX/XY), with heterochromosomes represented by either micro- or macrochromosomes, to multiple systems (X1X1X2X2/X1X2Y). Here, for the first time, the homology relationships of sex chromosomes have been investigated in nine anole lizards at the whole chromosome level. Cross-species chromosome painting using sex chromosome paints from A. carolinensis, Ctenonotus pogus and Norops sagrei and gene mapping of X-linked genes demonstrated that the anole ancestral sex chromosome system constituted by microchromosomes is retained in all the species with the ancestral karyotype (2n = 36, 12 macro- and 24 microchromosomes). On the contrary, species with a derived karyotype, namely those belonging to genera Ctenonotus and Norops, show a series of rearrangements (fusions/fissions) involving autosomes/microchromosomes that led to the formation of their current sex chromosome systems. These results demonstrate that different autosomes were involved in translocations with sex chromosomes in closely related lineages of anole lizards and that several sequential microautosome/sex chromosome fusions lead to a remarkable increase in size of Norops sagrei sex chromosomes.

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Acknowledgments

This research was supported by: funds provided by the Ministry of Education, University and Research (Italy) (“Ricerche di citogenetica molecolare sui sistemi di determinazione del sesso nei rettili squamati, sottordine Sauria”, grant number: PRIN2009/20093HYH97) to Vincenzo Caputo Barucchi, by Budget Projects 0310-2014-0003, 0310-2014-0008, 0310-2014-0009 provided to Vladimir A. Trifonov.

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Authors and Affiliations

  1. Dipartimento di Scienze della Vita e dell’Ambiente, Università Politecnica delle Marche, via Brecce Bianche, 60131, Ancona, Italy

    M. Giovannotti, A. Paoletti, G. Giovagnoli, P. Ruggeri, P. Nisi Cerioni, A. Splendiani, E. Olmo & V. Caputo Barucchi

  2. Cambridge Resource Centre for Comparative Genomics, Department of Veterinary Medicine, University of Cambridge, Madingley Road, Cambridge, CB3 0ES, UK

    M. Giovannotti, P. C. M. O’Brien, F. Kasai, J. C. Pereira, W. Rens & M. A. Ferguson-Smith

  3. Institute of Molecular and Cellular Biology, SB RAS, Novosibirsk, 630090, Russia

    V. A. Trifonov & I. G. Kichigin

  4. Novosibirsk State University, Novosibirsk, Russia

    V. A. Trifonov

  5. Cytometry Core Facility, Wellcome Trust Sanger Institute, Cambridge, CB10 1SA, UK

    B. L. Ng

  6. Cytocell Ltd, Cambridge Technopark, Newmarket Road, Cambridge, CB5 8PB, UK

    J. C. Pereira

  7. Consiglio Nazionale delle Ricerche, Istituto di Scienze Marine Sezione Pesca Marittima, Largo Fiera della Pesca, 60125, Ancona, Italy

    V. Caputo Barucchi

Authors
  1. M. Giovannotti
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  2. V. A. Trifonov
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  3. A. Paoletti
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  4. I. G. Kichigin
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  5. P. C. M. O’Brien
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  6. F. Kasai
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  7. G. Giovagnoli
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  8. B. L. Ng
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  9. P. Ruggeri
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  10. P. Nisi Cerioni
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  11. A. Splendiani
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  12. J. C. Pereira
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  13. E. Olmo
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  14. W. Rens
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  15. V. Caputo Barucchi
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  16. M. A. Ferguson-Smith
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Corresponding author

Correspondence to M. Giovannotti.

Ethics declarations

It was not necessary to get an approval of the institutional animal care and use committee (IACUC) or any relevant ethics body since this study on animal tissues complies with article 2e of D.L. 26/2014 of the Italian Government derived from Directive 2010/63/EU of the European Parliament and of the Council (article 1, paragraph 5e) on the protection of animals used for scientific purposes.

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The authors declare that they have no conflict of interest.

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Giovannotti, M., Trifonov, V.A., Paoletti, A. et al. New insights into sex chromosome evolution in anole lizards (Reptilia, Dactyloidae). Chromosoma 126, 245–260 (2017). https://doi.org/10.1007/s00412-016-0585-6

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  • DOI: https://doi.org/10.1007/s00412-016-0585-6

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