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Concerted evolution reveals co-adapted amino acid substitutions in Na+K+-ATPase of frogs that prey on toxic toads

View ORCID ProfileShabnam Mohammadi, View ORCID ProfileLu Yang, View ORCID ProfileArbel Harpak, View ORCID ProfileSantiago Herrera-Álvarez, María del Pilar Rodríguez-Ordoñez, Julie Peng, View ORCID ProfileKaren Zhang, View ORCID ProfileJay F. Storz, View ORCID ProfileSusanne Dobler, View ORCID ProfileAndrew J. Crawford, View ORCID ProfilePeter Andolfatto
doi: https://doi.org/10.1101/2020.08.04.234435
Shabnam Mohammadi
1School of Biological Sciences, University of Nebraska, Lincoln, NE, USA
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Lu Yang
2Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USA
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Arbel Harpak
3Department of Biological Sciences, Columbia University, New York, NY, USA
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Santiago Herrera-Álvarez
4Department of Biological Sciences, Universidad de los Andes, Bogotá, 111711, Colombia
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  • ORCID record for Santiago Herrera-Álvarez
María del Pilar Rodríguez-Ordoñez
4Department of Biological Sciences, Universidad de los Andes, Bogotá, 111711, Colombia
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Julie Peng
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Karen Zhang
2Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USA
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Jay F. Storz
1School of Biological Sciences, University of Nebraska, Lincoln, NE, USA
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Susanne Dobler
6Molecular Evolutionary Biology, Zoological Institute, Universität Hamburg, Hamburg, Germany
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Andrew J. Crawford
4Department of Biological Sciences, Universidad de los Andes, Bogotá, 111711, Colombia
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  • For correspondence: andrew@dna.ac pa2543@columbia.edu
Peter Andolfatto
3Department of Biological Sciences, Columbia University, New York, NY, USA
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  • For correspondence: andrew@dna.ac pa2543@columbia.edu
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ABSTRACT

Gene duplication is an important source of evolutionary innovation, but the adaptive division-of-labor between duplicates can be opposed by ongoing gene conversion between them. Here we document a tandem duplication of Na+,K+-ATPase subunit α1 (ATP1A1) shared by frogs in the genus Leptodactylus, a group of species that feeds on toxic toads. One ATP1A1 paralog evolved resistance to toad toxins while the other paralog retained ancestral susceptibility. We show that the two Leptodactylus paralogs are distinguished by 12 amino acid substitutions that were maintained by strong selection that counteracted the homogenizing effect of gene conversion. Protein-engineering experiments show that two major-effect substitutions confer toxin resistance, whereas the 10 additional substitutions mitigate deleterious pleiotropic effects on enzyme function. Our results highlight how trans-specific, neofunctionalized gene duplicates can provide unique insights into interactions between adaptive substitutions and the genetic backgrounds on which they arise.

One Sentence Summary Selection counteracts gene conversion to maintain an adaptive division-of-labor between tandemly duplicated genes.

Competing Interest Statement

The authors have declared no competing interest.

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Posted September 12, 2020.
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Concerted evolution reveals co-adapted amino acid substitutions in Na+K+-ATPase of frogs that prey on toxic toads
Shabnam Mohammadi, Lu Yang, Arbel Harpak, Santiago Herrera-Álvarez, María del Pilar Rodríguez-Ordoñez, Julie Peng, Karen Zhang, Jay F. Storz, Susanne Dobler, Andrew J. Crawford, Peter Andolfatto
bioRxiv 2020.08.04.234435; doi: https://doi.org/10.1101/2020.08.04.234435
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Concerted evolution reveals co-adapted amino acid substitutions in Na+K+-ATPase of frogs that prey on toxic toads
Shabnam Mohammadi, Lu Yang, Arbel Harpak, Santiago Herrera-Álvarez, María del Pilar Rodríguez-Ordoñez, Julie Peng, Karen Zhang, Jay F. Storz, Susanne Dobler, Andrew J. Crawford, Peter Andolfatto
bioRxiv 2020.08.04.234435; doi: https://doi.org/10.1101/2020.08.04.234435

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