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Structural and Molecular Diversification of the Anguimorpha Lizard Mandibular Venom Gland System in the Arboreal Species Abronia graminea

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Abstract

In the past, toxinological research on reptiles has focused principally on clinically important species. As a result, our understanding of the evolution of the reptile venom system is limited. Here, for the first time, we describe the structural and molecular evolutionary features of the mandibular toxin-secreting gland of Abronia graminea, a representative of one of the poorly known and entirely arboreal lineages of anguimorph lizards. We show that the mandibular gland is robust and serous, characters consistent with those expected of a toxin-secreting gland in active use. A wide array of transcripts were recovered that were homologous to those encoded by the indisputably venomous helodermatid lizards. We show that some of these toxin transcripts are evolving under active selection and show evidence of rapid diversification. Helokinestatin peptides in particular are revealed to have accumulated residues that have undergone episodic diversifying selections. Conversely, the natriuretic peptides have evolved under tremendous evolutionary constraints despite being encoded in tandem with helokinestatins by the same gene precursor. Of particular note is the sequencing for the first time of kunitz peptides from a lizard toxin-secreting gland. Not only are kunitz peptides shown to be an ancestral toxicoferan toxin, the ancestral state of this peptide is revealed to be a dual domain encoding precursor. This research provides insight into the evolutionary history of the ancient toxicoferan reptile venom system. In addition, it shows that even ‘clinically irrelevant’ species can be a rich source of novel venom components, worthy of investigation for drug design and biomedical research.

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Acknowledgments

BGF was funded by the Australian Research Council and the University of Queensland. EABU would like to acknowledge funding from the University of Queensland (International Postgraduate Research Scholarship, UQ Centennial Scholarship, and UQ Advantage Top-Up Scholarship) and the Norwegian State Education Loans Fund. This research was supported in part by the Portuguese Foundation for Science and Technology (FCT) through the Ph.D. grant conferred to KS (SFRH/BD/61959/2009) and the project PTDC/AAC-AMB/121301/2010 (FCOMP-01-0124-FEDER-019490) to AA.

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Authors and Affiliations

  1. Venom Evolution Laboratory, School of Biological Sciences, University of Queensland, St. Lucia, QLD, 4072, Australia

    Ivan Koludarov, Eivind A. B. Undheim, Timothy N. W. Jackson, Tim Ruder & Bryan G. Fry

  2. Institute for Molecular Biosciences, University of Queensland, St. Lucia, QLD, 4072, Australia

    Eivind A. B. Undheim & Glenn King

  3. CIMAR/CIIMAR, Centro Interdisciplinar de Investigação Marinha e Ambiental, Universidade do Porto, Rua dos Bragas, 177, 4050-123, Porto, Portugal

    Kartik Sunagar & Agostinho Antunes

  4. Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre, 4169-007, Porto, Portugal

    Kartik Sunagar & Agostinho Antunes

  5. School of Biomedical Sciences, University of Queensland, St. Lucia, QLD, 4072, Australia

    Darryl Whitehead

  6. Departamento de Medicina Molecular y Bioprocesos, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Av. Universidad 2001, 62210, Cuernavaca, Morelos, Mexico

    Alejandro C. Saucedo, G. Roberto Mora & Alejandro C. Alagon

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  1. Ivan Koludarov
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  2. Kartik Sunagar
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  3. Eivind A. B. Undheim
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  4. Timothy N. W. Jackson
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  5. Tim Ruder
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  6. Darryl Whitehead
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  7. Alejandro C. Saucedo
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  8. G. Roberto Mora
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  9. Alejandro C. Alagon
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  10. Glenn King
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  11. Agostinho Antunes
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  12. Bryan G. Fry
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Correspondence to Bryan G. Fry.

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Ivan Koludarov, Kartik Sunagar and Eivind A. B. Undheim are Co-first authors.

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Koludarov, I., Sunagar, K., Undheim, E.A.B. et al. Structural and Molecular Diversification of the Anguimorpha Lizard Mandibular Venom Gland System in the Arboreal Species Abronia graminea . J Mol Evol 75, 168–183 (2012). https://doi.org/10.1007/s00239-012-9529-9

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