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When one phenotype is not enough – divergent evolutionary trajectories govern venom variation in a widespread rattlesnake species

View ORCID ProfileGiulia Zancolli, Juan J. Calvete, Michael D. Cardwell, Harry W. Greene, William K. Hayes, Matthew J. Hegarty, Hans-Werner Herrmann, Andrew T. Holycross, Dominic I. Lannutti, John F. Mulley, Libia Sanz, Zachary D. Travis, Joshua R. Whorley, Catharine E. Wüster, Wolfgang Wüster
doi: https://doi.org/10.1101/413831
Giulia Zancolli
1Molecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, Bangor University, Bangor LL57 2UW, UK.
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  • ORCID record for Giulia Zancolli
  • For correspondence: giulia.zancolli@gmail.com
Juan J. Calvete
2Evolutionary and Translational Venomics Laboratory, CSIC, Jaume Roig 11, Valencia 46010, Spain.
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Michael D. Cardwell
3Department of Biology, San Diego State University, San Diego 92182, California, USA.
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Harry W. Greene
4Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca 14853, New York, USA.
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William K. Hayes
5Department of Earth and Biological Sciences, School of Medicine, Loma Linda University, Loma Linda 92350, California, USA.
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Matthew J. Hegarty
6Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth SY23 3EE, UK.
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Hans-Werner Herrmann
7Wildlife Conservation and Management, School of Natural Resources and the Environment, University of Arizona, 1064 East Lowell Street (ENR2), Tucson 85721, Arizona, USA.
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Andrew T. Holycross
8Natural History Collections, Arizona State University, 734 W. Alameda Drive, Tempe 85282, Arizona, USA.
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Dominic I. Lannutti
9Department of Biological Sciences, University of Texas at El Paso, 500 W. University, El Paso 79968, Texas, USA.
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John F. Mulley
10School of Biological Sciences, Bangor University, Bangor LL57 2UW, UK.
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Libia Sanz
2Evolutionary and Translational Venomics Laboratory, CSIC, Jaume Roig 11, Valencia 46010, Spain.
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Zachary D. Travis
5Department of Earth and Biological Sciences, School of Medicine, Loma Linda University, Loma Linda 92350, California, USA.
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Joshua R. Whorley
11Seattle Central College, Science, Technology, Engineering & Mathematics Division, 1701 Broadway Ave. E., Seattle 98122, Washington, USA.
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Catharine E. Wüster
1Molecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, Bangor University, Bangor LL57 2UW, UK.
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Wolfgang Wüster
1Molecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, Bangor University, Bangor LL57 2UW, UK.
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SUMMARY

Understanding the relationship between genome, phenotypic variation, and the ecological pressures that act to maintain that variation, represents a fundamental challenge in evolutionary biology. Functional polymorphisms typically segregate in spatially isolated populations [1, 2] and/or discrete ecological conditions [3-5], whereas dissecting the evolutionary processes involved in adaptive geographic variation across a continuous spatial distribution is much more challenging [6]. Additionally, pleiotropic interactions between genes and phenotype often complicate the identification of specific genotype-phenotype links [7-8], and thus of the selective pressures acting on them. Animal venoms are ideal systems to overcome these constraints: they are complex and variable, yet easily quantifiable molecular phenotypes with a clear function and a direct link to both genome and fitness [9]. Here, we use dense and widespread population-level sampling of the Mohave rattlesnake, Crotalus scutulatus, and show that genomic structural variation at multiple loci underlies extreme geographic variation in venom composition, which is maintained despite extensive gene flow. Unexpectedly, selection for diet does not explain venom variation, contrary to the dominant paradigm of venom evolution, and neither does neutral population structure caused by past vicariance. Instead, different toxin genes correlate with distinct environmental factors, suggesting that divergent selective pressures can act on individual loci independently of their genomic proximity or co-expression patterns. Local-scale spatial heterogeneity thus appears to maintain a remarkably ancient complex of molecular phenotypes, which have been retained in populations that diverged more than 1.5-2 MYA, representing an exceptional case of long-term structural polymorphism. These results emphasize how the interplay between genomic architecture and spatial heterogeneity in selective pressures may facilitate the retention of functional polymorphisms of an adaptive phenotype.

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Posted September 12, 2018.
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When one phenotype is not enough – divergent evolutionary trajectories govern venom variation in a widespread rattlesnake species
Giulia Zancolli, Juan J. Calvete, Michael D. Cardwell, Harry W. Greene, William K. Hayes, Matthew J. Hegarty, Hans-Werner Herrmann, Andrew T. Holycross, Dominic I. Lannutti, John F. Mulley, Libia Sanz, Zachary D. Travis, Joshua R. Whorley, Catharine E. Wüster, Wolfgang Wüster
bioRxiv 413831; doi: https://doi.org/10.1101/413831
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When one phenotype is not enough – divergent evolutionary trajectories govern venom variation in a widespread rattlesnake species
Giulia Zancolli, Juan J. Calvete, Michael D. Cardwell, Harry W. Greene, William K. Hayes, Matthew J. Hegarty, Hans-Werner Herrmann, Andrew T. Holycross, Dominic I. Lannutti, John F. Mulley, Libia Sanz, Zachary D. Travis, Joshua R. Whorley, Catharine E. Wüster, Wolfgang Wüster
bioRxiv 413831; doi: https://doi.org/10.1101/413831

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