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Sex determination in Madagascar geckos of the genus Paroedura (Squamata: Gekkonidae): are differentiated sex chromosomes indeed so evolutionary stable?

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Abstract

Among amniote vertebrates, geckos represent a clade with exceptional variability in sex determination; however, only a minority of species of this highly diverse group has been studied in this respect. Here, we describe for the first time a female heterogamety in the genus Paroedura, the group radiated in Madagascar and adjacent islands. We identified homomorphic ZZ/ZW sex chromosomes with a highly heterochromatic W chromosome in Paroedura masobe, Paroedura oviceps, Paroedura karstophila, Paroedura stumpffi, and Paroedura lohatsara. Comparative genomic hybridization (CGH) revealed that female-specific sequences are greatly amplified in the W chromosome of P. lohatsara and that P. gracilis seems to possess a derived system of multiple sex chromosomes. Contrastingly, neither CGH nor heterochromatin visualization revealed differentiated sex chromosomes in the members of the Paroedura picta—Paroedura bastardi—Paroedura ibityensis clade, which is phylogenetically nested within lineages with a heterochromatic W chromosome. As a sex ratio consistent with genotypic sex determination has been reported in P. picta, it appears that the members of the P. picta—P. bastardi—P. ibityensis clade possess homomorphic, poorly differentiated sex chromosomes and may represent a rare example of evolutionary loss of highly differentiated sex chromosomes. Fluorescent in situ hybridization (FISH) with a telomeric probe revealed a telomere-typical pattern in all species and an accumulation of telomeric sequences in the centromeric region of autosomes in P. stumpffi and P. bastardi. Our study adds important information for the greater understanding of the variability and evolution of sex determination in geckos and demonstrates how the geckos of the genus Paroedura provide an interesting model for studying the evolution of the sex chromosomes.

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Abbreviations

CGH :

Comparative genomic hybridization

DAPI :

4′,6-Diamidino-2-phenylindole

DUTP:

Deoxy-uridine-5′-triphosphate

ESD:

Environmental sex determination

FISH:

Fluorescence in situ hybridization

FITC:

Fluorescein isothiocyanate

GSD:

Genotypic sex determination

ITSs:

Interstitial telomeric sequences

PCR:

Polymerase chain reaction

SSC:

Saline sodium citrate

SDS:

Sodium dodecyl sulfate

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Acknowledgment

The authors would like to express their gratitude to Jan Červenka for his valuable assistance with animal handling, to Zuzana Majtánová for her assistance with CGH methodology, to Petr Ráb and Marie Rábová for their support and advice regarding the experimental component, to Christopher Johnson for his linguistic improvements to the draft manuscript, and to two anonymous reviewers for their insightful comments. This project was supported by the Czech Science Foundation (GAČR 506/10/0718) and the Grant Agency of Charles University (GAUK 527112). This paper represents part 10 of our series “Evolution of sex-determining systems in lizards.”

Ethical standards

All institutional and national guidelines for the care and use of laboratory animals were followed.

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Ecology, Faculty of Science, Charles University in Prague, Viničná 7, Praha 2, Prague, Czech Republic

    Martina Koubová, Martina Johnson Pokorná, Michail Rovatsos, Klára Farkačová, Marie Altmanová & Lukáš Kratochvíl

  2. Institute of Animal Physiology and Genetics, Academy of the Sciences of the Czech Republic, Rumburská 89, Liběchov, Czech Republic

    Martina Johnson Pokorná

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  1. Martina Koubová
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  2. Martina Johnson Pokorná
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Correspondence to Lukáš Kratochvíl.

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Responsible Editor: Fengtang Yang.

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Koubová, M., Pokorná, M.J., Rovatsos, M. et al. Sex determination in Madagascar geckos of the genus Paroedura (Squamata: Gekkonidae): are differentiated sex chromosomes indeed so evolutionary stable?. Chromosome Res 22, 441–452 (2014). https://doi.org/10.1007/s10577-014-9430-z

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