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Do sex chromosomes of snakes, monitor lizards, and iguanian lizards result from multiple fission of an “ancestral amniote super-sex chromosome”?

Chromosome Research volume 28, pages 209–228 (2020)Cite this article

Abstract

Sex chromosomes in some amniotes share linkage homologies with distantly related taxa in regions orthologous to squamate reptile chromosome 2 (SR2) and the snake W sex chromosome. Thus, the SR2 and W chromosomes may formerly have been part of a larger ancestral amniote super-sex chromosome. Comparison of various sex chromosomal linkage homologies in Toxicofera with those in other amniotes offers an excellent model to assess key cytological differences, to understand the mechanisms of amniote sex chromosome evolution in each lineage and the existence of an ancestral amniote super-sex chromosome. Chromosome maps of four species of Toxicofera were constructed using bacterial artificial chromosomes (BACs) derived from chicken and zebra finch libraries containing amniote sex chromosomal linkages. Different macrochromosome linkage homologies were highly conserved among Toxicofera, and at least two BACs (CH261-125F1 and CH261-40D6) showed partial homology with sex chromosomes of amniotes associated with SR2, which supports the hypothesis of an ancestral super-sex chromosome with overlaps of partial linkage homologies. The present data also suggest a possible multiple fission mechanism of an ancestral super-sex chromosome, which resulted in further development of various sex chromosomal linkages of Toxicofera based on particular properties that favored the role of sex chromosomes.

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Abbreviations

ACA:

Anolis carolinensis

ASP:

Apalone spinifera

BACs:

Bacterial artificial chromosomes

CVE:

Calotes versicolor

DAPI:

4′,6-Diamidino-2-phenylindole

EDTA:

Ethylenediaminetetraacetic acid

EQU:

Elaphe quadrivirgata

FBS:

Fetal bovine serum

FISH:

Fluorescent in situ hybridization

FITC:

Fluorescein isothiocyanate

GGA:

Gallus gallus

GHO:

Gekko hokouensis

GIN:

Glyptemys insculpta

GSD:

Genotypic sex determination

HSA:

Homo sapiens

LAG:

Lacerta agilis

LRE:

Leiolepis reevesii rubritaeniata

MEU:

Macropus eugenii

NKA:

Naja kaouthia

OAN:

Ornithorhynchus anatinus

PSI:

Pelodiscus sinensis

PVI:

Pogona vitticeps

QSMI:

Queen Saovabha Memorial Institute

SCR:

Siebenrockiella crassicollis

SSA:

Staurotypus salvinii

STR:

Staurotypus triporcatus

TGU:

Taeniopygia guttata

TSD:

Temperature sex determination

TSE:

Takydromus sexlineatus

VKO:

Varanus komodoensis

VSA:

Varanus salvator macromaculatus

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Acknowledgments

We extend grateful thanks to Lawan Chanhome, Tanapong Tawan, Taksa Vasaruchapong, and Panithi Laoungbua (Snake Farm, Queen Saovabha Memorial Institute, Thai Red Cross Society, Thailand) and the Conservation Research and Education Division, Zoological Park Organization, Dusit, Bangkok, Thailand, for help with sample collection and advice on sample preparation.

Availability of data and material

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Funding

This study was financially supported by grants from the Center for Advanced Studies in Tropical Natural Resources, National Research University-Kasetsart University (CASTNAR, NRU-KU, Thailand) (nos. 6/2558 and 9/2559) awarded to KS, Thailand Research Fund (TRF) (nos. RSA6180075 and PHD60I0014) awarded to KS and WS, Thailand Research Fund-Newton Fund Ph.D. Placement (no. GA/PhD/scholar/Year5/007) awarded to WS, and the Thailand Research Fund-Newton Fund Placement, Travel Grant for PhD Supervisors (GA/PhD/Sup/Year4/003) awarded to KS. This work was also funded in part by the Biotechnology and Biological Sciences Research Council (BB/K008161/1) to the University of Kent (DKG).

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Authors and Affiliations

  1. Laboratory of Animal Cytogenetics and Comparative Genomics (ACCG), Department of Genetics, Faculty of Science, Kasetsart University, 50 Ngamwongwan, Chatuchak, Bangkok, 10900, Thailand

    Worapong Singchat, Siwapech Sillapaprayoon, Chantra Indananda, Surin Peyachoknagul & Kornsorn Srikulnath

  2. Special Research Unit for Wildlife Genomics (SRUWG), Department of Forest Biology, Faculty of Forestry, Kasetsart University, 50 Ngamwongwan, Chatuchak, Bangkok, 10900, Thailand

    Worapong Singchat, Siwapech Sillapaprayoon, Chantra Indananda, Prateep Duengkae & Kornsorn Srikulnath

  3. Department of Fishery Biology, Faculty of Fisheries, Kasetsart University, 50 Ngamwongwan, Chatuchak, Bangkok, 10900, Thailand

    Narongrit Muangmai

  4. Bureau of Conservation and Research, Zoological Park Organization under the Royal Patronage of His Majesty the King, Bangkok, Thailand

    Sudarath Baicharoen

  5. School of Biosciences, University of Kent, Canterbury, CT2 7NY, UK

    Rebecca E. O’Connor & Darren K. Griffin

  6. Omics Center for Agriculture, Bioresources, Food and Health, Kasetsart University (OmiKU), Bangkok, 10900, Thailand

    Kornsorn Srikulnath

  7. Center for Advanced Studies in Tropical Natural Resources, National Research University-Kasetsart University (CASTNAR, NRU-KU), Kasetsart University, Bangkok, 10900, Thailand

    Kornsorn Srikulnath

  8. Center of Excellence on Agricultural Biotechnology (AG-BIO/PERDO-CHE), Bangkok, 10900, Thailand

    Kornsorn Srikulnath

  9. Amphibian Research Center, Hiroshima University, 1-3-1, Kagamiyama, Higashihiroshima, 739-8526, Japan

    Kornsorn Srikulnath

Authors
  1. Worapong Singchat
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  2. Siwapech Sillapaprayoon
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  3. Narongrit Muangmai
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  4. Sudarath Baicharoen
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  6. Prateep Duengkae
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  7. Surin Peyachoknagul
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  8. Rebecca E. O’Connor
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  9. Darren K. Griffin
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  10. Kornsorn Srikulnath
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Contributions

W.S. and K.S. drafted the manuscript; W.S., B.E.O., D.K.G., and K.S. conceived the ideas and designed methodology; W.S. and K.S. carried out the lab work; W.S. and K.S. participated in data analysis; W.S., S.S., N.M., S.B., C.I., P.D., S.P., B.E.O., D.K.G., and K.S. reviewed the data and the manuscript. All authors gave final approval for publication.

Corresponding author

Correspondence to Kornsorn Srikulnath.

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Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

Animal care and all experimental procedures were approved by the Animal Experiment Committee, Kasetsart University, Thailand (approval nos. ACKU61-SCI-021, ACKU61-SCI-023, and ACKU61-SCI-024) and conducted in accordance with the Regulations on Animal Experiments at Kasetsart University.

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Rebecca E O’Connor, Darren K Griffin, and Kornsorn Srikulnath are joint last authors.

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Singchat, W., Sillapaprayoon, S., Muangmai, N. et al. Do sex chromosomes of snakes, monitor lizards, and iguanian lizards result from multiple fission of an “ancestral amniote super-sex chromosome”?. Chromosome Res 28, 209–228 (2020). https://doi.org/10.1007/s10577-020-09631-4

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