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Genetic population structure constrains local adaptation in sticklebacks

Petri Kemppainen, Zitong Li, Pasi Rastas, Ari Löytynoja, Bohao Fang, Jing Yang, Baocheng Guo, Takahito Shikano, View ORCID ProfileJuha Merilä
doi: https://doi.org/10.1101/2020.01.17.908970
Petri Kemppainen
1Ecological Genetics Research Unit, Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, FI-00014 University of Helsinki, Finland
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  • For correspondence: petrikemppainen2@gmail.com
Zitong Li
1Ecological Genetics Research Unit, Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, FI-00014 University of Helsinki, Finland
2CSIRO Agriculture & Food, GPO Box 1600, Canberra, ACT 2601, Australia
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Pasi Rastas
1Ecological Genetics Research Unit, Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, FI-00014 University of Helsinki, Finland
3Institute of Biotechnology, FI-00014 University of Helsinki, Finland
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Ari Löytynoja
3Institute of Biotechnology, FI-00014 University of Helsinki, Finland
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Bohao Fang
1Ecological Genetics Research Unit, Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, FI-00014 University of Helsinki, Finland
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Jing Yang
1Ecological Genetics Research Unit, Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, FI-00014 University of Helsinki, Finland
4Chinese Sturgeon Research Institute, Three Gorges Corporation, Yichang, 443100, China
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Baocheng Guo
5The Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
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Takahito Shikano
1Ecological Genetics Research Unit, Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, FI-00014 University of Helsinki, Finland
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Juha Merilä
1Ecological Genetics Research Unit, Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, FI-00014 University of Helsinki, Finland
6Division of Ecology and Biodiversity, Kadoorie Building, The University of Hong Kong, Pokfulam Road, Hong Kong, SAR
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  • ORCID record for Juha Merilä
  • For correspondence: petrikemppainen2@gmail.com
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Abstract

Repeated and independent adaptation to specific environmental conditions from standing genetic variation is common. However, if genetic variation is limited, the evolution of similar locally adapted traits may be restricted to genetically different and potentially less optimal solutions or prevented from happening altogether. Using a quantitative trait locus (QTL) mapping approach, we identified the genomic regions responsible for the repeated pelvic reduction (PR) in three crosses between nine-spined stickleback populations expressing full and reduced pelvic structures. In one cross, PR mapped to linkage group 7 (LG7) containing the gene Pitx1, known to control pelvic reduction also in the three-spined stickleback. In the two other crosses, PR was polygenic and attributed to ten novel QTL, of which 90% were unique to specific crosses. When screening the genomes from 27 different populations for deletions in the Pitx1 regulatory element, these were only found in the population in which PR mapped to LG7, even though the morphological data indicated large effect QTL for PR in several other populations as well. Consistent with the available theory and simulations parameterised on empirical data, we hypothesise that the observed variability in genetic architecture of PR is due to heterogeneity in the spatial distribution of standing genetic variation caused by >2x stronger population structuring among freshwater populations and >10x stronger genetic isolation by distance in the sea in nine-spined sticklebacks as compared to three-spined sticklebacks.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • This a version Accepted for Publication in Molecular Ecology.

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 January 20, 2021.
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Genetic population structure constrains local adaptation in sticklebacks
Petri Kemppainen, Zitong Li, Pasi Rastas, Ari Löytynoja, Bohao Fang, Jing Yang, Baocheng Guo, Takahito Shikano, Juha Merilä
bioRxiv 2020.01.17.908970; doi: https://doi.org/10.1101/2020.01.17.908970
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Genetic population structure constrains local adaptation in sticklebacks
Petri Kemppainen, Zitong Li, Pasi Rastas, Ari Löytynoja, Bohao Fang, Jing Yang, Baocheng Guo, Takahito Shikano, Juha Merilä
bioRxiv 2020.01.17.908970; doi: https://doi.org/10.1101/2020.01.17.908970

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