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Testing the predictability of morphological evolution in contrasting thermal environments

View ORCID ProfileNatalie Pilakouta, Joseph L. Humble, Iain D.C. Hill, Jessica Arthur, Ana P.B. Costa, Bethany A. Smith, View ORCID ProfileBjarni K. Kristjánsson, Skúli Skúlason, View ORCID ProfileShaun S. Killen, Jan Lindström, View ORCID ProfileNeil B. Metcalfe, Kevin J. Parsons
doi: https://doi.org/10.1101/609933
Natalie Pilakouta
1Institute of Biodiversity, Animal Health, and Comparative Medicine, University of Glasgow, Glasgow, UK
2School of Biological Sciences, University of Aberdeen, Aberdeen, UK
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  • For correspondence: natalie.pilakouta@abdn.ac.uk kevin.parsons@glasgow.ac.uk
Joseph L. Humble
1Institute of Biodiversity, Animal Health, and Comparative Medicine, University of Glasgow, Glasgow, UK
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Iain D.C. Hill
1Institute of Biodiversity, Animal Health, and Comparative Medicine, University of Glasgow, Glasgow, UK
3School of Life Sciences, University of Nottingham, Nottingham, UK
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Jessica Arthur
1Institute of Biodiversity, Animal Health, and Comparative Medicine, University of Glasgow, Glasgow, UK
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Ana P.B. Costa
1Institute of Biodiversity, Animal Health, and Comparative Medicine, University of Glasgow, Glasgow, UK
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Bethany A. Smith
1Institute of Biodiversity, Animal Health, and Comparative Medicine, University of Glasgow, Glasgow, UK
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Bjarni K. Kristjánsson
4Department of Aquaculture and Fish Biology, Hólar University, Sauðárkrókur, Iceland
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  • ORCID record for Bjarni K. Kristjánsson
Skúli Skúlason
4Department of Aquaculture and Fish Biology, Hólar University, Sauðárkrókur, Iceland
5Icelandic Museum of Natural History, Reykjavík, Iceland
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Shaun S. Killen
1Institute of Biodiversity, Animal Health, and Comparative Medicine, University of Glasgow, Glasgow, UK
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Jan Lindström
1Institute of Biodiversity, Animal Health, and Comparative Medicine, University of Glasgow, Glasgow, UK
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Neil B. Metcalfe
1Institute of Biodiversity, Animal Health, and Comparative Medicine, University of Glasgow, Glasgow, UK
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Kevin J. Parsons
1Institute of Biodiversity, Animal Health, and Comparative Medicine, University of Glasgow, Glasgow, UK
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  • For correspondence: natalie.pilakouta@abdn.ac.uk kevin.parsons@glasgow.ac.uk
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ABSTRACT

In light of climate change, the ability to predict evolutionary responses to temperature changes is of central importance for conservation efforts. Prior work has focused on exposing model organisms to different temperatures for just one or a few generations under laboratory conditions. Using a ‘natural experiment’, we show that studying parallel evolution in wild populations from contrasting thermal environments presents a more powerful approach for understanding and predicting responses to climate change. More specifically, we used a unique study system in Iceland, where freshwater populations of threespine sticklebacks (Gasterosteus aculeatus) are found in waters warmed by geothermal activity, adjacent to populations in ambient-temperature water. We used three sympatric and three allopatric warm-cold population pairs to test for repeated patterns of morphological divergence in relation to thermal habitat. We found that thermal habitat explained over 50% of body shape variation: fish from warm habitats had a deeper mid-body, a shorter jaw, and smaller eyes. Our common garden experiment showed that most of these morphological differences between thermal habitats were heritable. Lastly, absence of gene flow seems to facilitate parallel divergence across thermal habitats: all three allopatric population pairs were on a common evolutionary trajectory, whereas sympatric pairs followed different trajectories. Our findings therefore suggest that morphological responses to rising temperatures can be predictable when there is limited gene flow. On the other hand, migration of individuals between different thermal habitats or microhabitats can exaggerate nonparallel evolution and reduce our ability to predict evolutionary responses.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • We have added data from a common garden experiment showing evidence for heritability of morphological differences in lab-reared F1 fish.

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 August 14, 2020.
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Testing the predictability of morphological evolution in contrasting thermal environments
Natalie Pilakouta, Joseph L. Humble, Iain D.C. Hill, Jessica Arthur, Ana P.B. Costa, Bethany A. Smith, Bjarni K. Kristjánsson, Skúli Skúlason, Shaun S. Killen, Jan Lindström, Neil B. Metcalfe, Kevin J. Parsons
bioRxiv 609933; doi: https://doi.org/10.1101/609933
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Testing the predictability of morphological evolution in contrasting thermal environments
Natalie Pilakouta, Joseph L. Humble, Iain D.C. Hill, Jessica Arthur, Ana P.B. Costa, Bethany A. Smith, Bjarni K. Kristjánsson, Skúli Skúlason, Shaun S. Killen, Jan Lindström, Neil B. Metcalfe, Kevin J. Parsons
bioRxiv 609933; doi: https://doi.org/10.1101/609933

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