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A framework to quantify phenotypic and genotypic parallel evolution

View ORCID ProfileMaddie E. James, Melanie J. Wilkinson, Henry L. North, View ORCID ProfileJan Engelstädter, View ORCID ProfileDaniel Ortiz-Barrientos
doi: https://doi.org/10.1101/2020.02.05.936450
Maddie E. James
1The University of Queensland, School of Biological Sciences, St. Lucia QLD 4072, Australia
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  • For correspondence: maddie.james@uqconnect.edu.au
Melanie J. Wilkinson
1The University of Queensland, School of Biological Sciences, St. Lucia QLD 4072, Australia
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Henry L. North
1The University of Queensland, School of Biological Sciences, St. Lucia QLD 4072, Australia
2University of Cambridge, Department of Zoology, Downing St., Cambridge CB2 14 3EJ, UK
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Jan Engelstädter
1The University of Queensland, School of Biological Sciences, St. Lucia QLD 4072, Australia
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Daniel Ortiz-Barrientos
1The University of Queensland, School of Biological Sciences, St. Lucia QLD 4072, Australia
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Abstract

The independent and repeated adaptation of populations to similar environments often results in the evolution of similar forms. This phenomenon creates a strong correlation between phenotype and environment and is referred to as parallel evolution. However, there is ongoing debate as to when we should call a system either phenotypically or genotypically ‘parallel.’ Here, we suggest a novel and simple framework to quantify parallel evolution at the genotypic and phenotypic levels. Our framework combines both traditional and new approaches to measure parallel evolution, and categorizes them into broad- and narrow-sense scales. We then apply this framework to coastal ecotypes of an Australian wildflower, Senecio lautus, that have evolved in parallel. Our findings show that S. lautus populations inhabiting similar environments have evolved strikingly similar phenotypes. These phenotypes have arisen via mutational changes occurring in different genes, although many share the same biological functions. Our work paves the way towards a common framework to study the repeated evolution of forms in nature.

Author summary When organisms face similar ecological conditions, they often evolve similar phenotypic solutions. When this occurs in closely related taxa, it is referred to as parallel evolution. Systems of parallel evolution provide some of the most compelling evidence for the role of natural selection in evolution, as they can be used as natural replicates of the adaptation process. However, there is debate as to when we should call a system ‘parallel’. This debate stems back to the mid 1900s, and although there have been multiple attempts within the literature to clarify terminology, controversy still remains. In this study, we propose a novel framework to quantify phenotypic and genotypic parallel evolution within empirical systems, partitioning parallelism into broad- and narrow-sense components. Our framework is applicable to non-model organisms and provides a common set of analyses to measure parallel evolution, enabling researchers to compare the extent of parallel evolution across different study systems. In turn, this helps to reduce confusion surrounding the term ‘parallel evolution’ at both the phenotypic and genotypic levels. We then apply our framework to two coastal ecotypes of an Australian plant, Senecio lautus. We show that similar phenotypes within each ecotype have evolved via mutational changes in different genes, though some are involved in similar biological functions. Our research not only helps to consolidate the field of parallel evolution, but paves the way to understanding the role of natural selection in the repeated evolution of similar phenotypes within nature.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
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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Posted July 12, 2020.
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A framework to quantify phenotypic and genotypic parallel evolution
Maddie E. James, Melanie J. Wilkinson, Henry L. North, Jan Engelstädter, Daniel Ortiz-Barrientos
bioRxiv 2020.02.05.936450; doi: https://doi.org/10.1101/2020.02.05.936450
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A framework to quantify phenotypic and genotypic parallel evolution
Maddie E. James, Melanie J. Wilkinson, Henry L. North, Jan Engelstädter, Daniel Ortiz-Barrientos
bioRxiv 2020.02.05.936450; doi: https://doi.org/10.1101/2020.02.05.936450

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