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Phylogenomics of scorpions reveal a co-diversification of scorpion mammalian predators and mammal-specific sodium channel toxins

View ORCID ProfileCarlos E. Santibáñez-López, Shlomi Aharon, Jesús A. Ballesteros, Guilherme Gainett, Caitlin M. Baker, Edmundo González-Santillán, Mark S. Harvey, Mohamed K. Hassan, Ali Hussin Abu-Almaaty, Shorouk Mohamed Aldeyarbi, Lionel Monod, Andrés Ojanguren-Affilastro, Robert J. Raven, Ricardo Pinto-Da-Rocha, Yoram Zvik, Efrat Gavish-Regev, Prashant P. Sharma
doi: https://doi.org/10.1101/2020.11.06.372045
Carlos E. Santibáñez-López
1Department of Integrative Biology, University of Wisconsin–Madison, Madison, WI 53706
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  • ORCID record for Carlos E. Santibáñez-López
  • For correspondence: santibanezlopezc@easternct.edu
Shlomi Aharon
2National Natural History Collections, The Hebrew University of Jerusalem, Jerusalem, Israel
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Jesús A. Ballesteros
1Department of Integrative Biology, University of Wisconsin–Madison, Madison, WI 53706
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Guilherme Gainett
1Department of Integrative Biology, University of Wisconsin–Madison, Madison, WI 53706
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Caitlin M. Baker
1Department of Integrative Biology, University of Wisconsin–Madison, Madison, WI 53706
3Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138
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Edmundo González-Santillán
4Laboratorio de Aracnología, Facultad de Ciencias, Departamento de Biología Comparada, Universidad Nacional Autónoma de México, C.P. 04510 Mexico City, Mexico
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Mark S. Harvey
5Department of Terrestrial Zoology, Western Australian Museum, Locked Bag 49, Welshpool DC 6986, Western Australia, Australia
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Mohamed K. Hassan
6Zoology Department, Faculty of Science, Port Said University, Egypt
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Ali Hussin Abu-Almaaty
6Zoology Department, Faculty of Science, Port Said University, Egypt
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Shorouk Mohamed Aldeyarbi
6Zoology Department, Faculty of Science, Port Said University, Egypt
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Lionel Monod
7Département des arthropodes et d’entomologie I, Muséum d’histoire naturelle, Route de Malagnou 1, 1208 Geneve, Switzerland
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Andrés Ojanguren-Affilastro
8División Aracnología, Museo Argentino de Ciencias Naturales, Av. ángel Gallardo 470, Buenos Aires, Argentina
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Robert J. Raven
9Department of Terrestrial Biodiversity, Queensland Museum, Grey Street, South Bank, Brisbane, Queensland, Australia
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Ricardo Pinto-Da-Rocha
10Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, travessa 14, 321, São Paulo, Cep: 05508-900, Brasil
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Yoram Zvik
11Hoopoe Ornithology & Ecology Center, Yeroham, Israel & Ben-Gurion University of the Negev, Be’er-Sheva, Israel
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Efrat Gavish-Regev
2National Natural History Collections, The Hebrew University of Jerusalem, Jerusalem, Israel
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Prashant P. Sharma
1Department of Integrative Biology, University of Wisconsin–Madison, Madison, WI 53706
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Abstract

Scorpions constitute a charismatic lineage of arthropods and comprise more than 2,500 described species. Found throughout various tropical and temperate habitats, these predatory arachnids have a long evolutionary history, with a fossil record that began in the Silurian. While all scorpions are venomous, the asymmetrically diverse family Buthidae harbors nearly half the diversity of extant scorpions, and all but one of the 58 species that are medically significant to humans. Many aspects of scorpion evolutionary history are unclear, such as the relationships of the most toxic genera and their constituent venom peptides. Furthermore, the diversification age of toxins that act specifically on mammalian ion channels have never been inferred. To redress these gaps, we assembled a large-scale phylogenomic dataset of 100 scorpion venom transcriptomes and/or genomes, emphasizing the sampling of highly toxic buthid genera. To infer divergence times of venom gene families, we applied a phylogenomic node dating approach for the species tree in tandem with phylostratigraphic bracketing to estimate minimum ages of mammal-specific toxins. Our analyses establish a robustly supported phylogeny of scorpions, particularly with regard to relationships between medically significant taxa. Analysis of venom gene families shows that mammal-specific sodium channel toxins have independently evolved in five lineages within Buthidae. The temporal windows of mammal-specific toxin origins are contiguous with the basal diversification of major scorpion mammal predators such as carnivores, shrews, bats and rodents. These results suggest an evolutionary arms race model comprised of co-diversification of mammalian predators and NaTx homologs in buthid venom.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵# Co-senior authors.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Phylogenomics of scorpions reveal a co-diversification of scorpion mammalian predators and mammal-specific sodium channel toxins
Carlos E. Santibáñez-López, Shlomi Aharon, Jesús A. Ballesteros, Guilherme Gainett, Caitlin M. Baker, Edmundo González-Santillán, Mark S. Harvey, Mohamed K. Hassan, Ali Hussin Abu-Almaaty, Shorouk Mohamed Aldeyarbi, Lionel Monod, Andrés Ojanguren-Affilastro, Robert J. Raven, Ricardo Pinto-Da-Rocha, Yoram Zvik, Efrat Gavish-Regev, Prashant P. Sharma
bioRxiv 2020.11.06.372045; doi: https://doi.org/10.1101/2020.11.06.372045
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Phylogenomics of scorpions reveal a co-diversification of scorpion mammalian predators and mammal-specific sodium channel toxins
Carlos E. Santibáñez-López, Shlomi Aharon, Jesús A. Ballesteros, Guilherme Gainett, Caitlin M. Baker, Edmundo González-Santillán, Mark S. Harvey, Mohamed K. Hassan, Ali Hussin Abu-Almaaty, Shorouk Mohamed Aldeyarbi, Lionel Monod, Andrés Ojanguren-Affilastro, Robert J. Raven, Ricardo Pinto-Da-Rocha, Yoram Zvik, Efrat Gavish-Regev, Prashant P. Sharma
bioRxiv 2020.11.06.372045; doi: https://doi.org/10.1101/2020.11.06.372045

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