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Adaptive divergence in shoot gravitropism creates hybrid sterility in an Australian wildflower

View ORCID ProfileMelanie J. Wilkinson, Federico Roda, View ORCID ProfileGreg M. Walter, Maddie E. James, Rick Nipper, Jessica Walsh, Scott L. Allen, Henry L. North, Christine A. Beveridge, View ORCID ProfileDaniel Ortiz-Barrientos
doi: https://doi.org/10.1101/845354
Melanie J. Wilkinson
1The University of Queensland, School of Biological Sciences, St Lucia QLD 4072, Australia
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  • For correspondence: m.wilkinson2@uq.edu.au
Federico Roda
1The University of Queensland, School of Biological Sciences, St Lucia QLD 4072, Australia
2Universidad Nacional de Colombia, Departamento de Biología, Bogotá, Colombia
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Greg M. Walter
1The University of Queensland, School of Biological Sciences, St Lucia QLD 4072, Australia
3Monash University, School of Biological Sciences, Clayton Vic 3800
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Maddie E. James
1The University of Queensland, School of Biological Sciences, St Lucia QLD 4072, Australia
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Rick Nipper
4Floragenex, Inc., 4640 SW Macadam Avenue, Suite 200F, Portland, OR 97239, USA
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Jessica Walsh
4Floragenex, Inc., 4640 SW Macadam Avenue, Suite 200F, Portland, OR 97239, USA
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Scott L. Allen
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
5University of Cambridge, Department of Zoology, Downing St., Cambridge CB2 3EJ, UK
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Christine A. Beveridge
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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  • ORCID record for Daniel Ortiz-Barrientos
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Abstract

Natural selection is a significant driver of speciation. Yet it remains largely unknown whether local adaptation can drive speciation through the evolution of hybrid sterility between populations. Here, we show that adaptive divergence in shoot gravitropism, the ability of a plant’s shoot to bend upwards in response to the downward pull of gravity, contributes to the evolution of hybrid sterility in an Australian wildflower, Senecio lautus. We find that shoot gravitropism has evolved multiple times in association with plant height between adjacent populations inhabiting contrasting environments, suggesting that these traits have evolved by natural selection. We directly tested this prediction using a hybrid population subjected to eight rounds of recombination and three rounds of selection in the field. It revealed that shoot gravitropism responds to natural selection in the expected direction of the locally adapted population. This provided an ideal platform to test whether genetic differences in gravitropism contribute to hybrid sterility in S. lautus. Using this advanced hybrid population, we discovered that crossing individuals with extreme differences in gravitropism reduce their ability to produce seed by 21%, providing strong evidence that this adaptive trait is genetically correlated with hybrid sterility. Our results suggest that natural selection can drive the evolution of locally adaptive traits that also create hybrid sterility, thus indicating an evolutionary connection between local adaptation and the origin of new species.

Significance statement New species originate as populations become reproductively isolated from one another. Despite recent progress in uncovering the genetic basis of reproductive isolation, it remains unclear whether intrinsic reproductive barriers, such as hybrid sterility, evolve as a by-product of local adaptation to contrasting environments or evolve through non-ecological processes, such as meiotic drive. Here, we show that differences in a plant’s response to the pull of gravity have repeatedly evolved amongst coastal populations of an Australian wildflower, thus implicating a role of natural selection in their evolution. We found a strong genetic correlation between variation in this adaptive trait and hybrid sterility, suggesting that intrinsic reproductive barriers contribute to the origin of new species as populations adapt to heterogeneous environments.

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 March 21, 2021.
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Adaptive divergence in shoot gravitropism creates hybrid sterility in an Australian wildflower
Melanie J. Wilkinson, Federico Roda, Greg M. Walter, Maddie E. James, Rick Nipper, Jessica Walsh, Scott L. Allen, Henry L. North, Christine A. Beveridge, Daniel Ortiz-Barrientos
bioRxiv 845354; doi: https://doi.org/10.1101/845354
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Adaptive divergence in shoot gravitropism creates hybrid sterility in an Australian wildflower
Melanie J. Wilkinson, Federico Roda, Greg M. Walter, Maddie E. James, Rick Nipper, Jessica Walsh, Scott L. Allen, Henry L. North, Christine A. Beveridge, Daniel Ortiz-Barrientos
bioRxiv 845354; doi: https://doi.org/10.1101/845354

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