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The rise of the three-spined stickleback – eco-evolutionary consequences of a mesopredator release

View ORCID ProfileBritas Klemens Eriksson, Casey Yanos, View ORCID ProfileSarah Bourlat, View ORCID ProfileSerena Donadi, View ORCID ProfileMichael C. Fontaine, View ORCID ProfileJoakim P. Hansen, View ORCID ProfileEglė Jakubavičiūtė, View ORCID ProfileKarine Kiragosyan, View ORCID ProfileMartine E. Maan, View ORCID ProfileJuha Merilä, Åsa N. Austin, View ORCID ProfileJens Olsson, View ORCID ProfileKatrin Reiss, View ORCID ProfileGöran Sundblad, View ORCID ProfileUlf Bergström, View ORCID ProfileJohan S. Eklöf
doi: https://doi.org/10.1101/2020.05.08.083873
Britas Klemens Eriksson
1Groningen Institute for Evolutionary Life-Sciences, GELIFES, Nijenborgh 7, 9747 AG Groningen, University of Groningen, The Netherlands
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  • For correspondence: b.d.h.k.eriksson@rug.nl
Casey Yanos
1Groningen Institute for Evolutionary Life-Sciences, GELIFES, Nijenborgh 7, 9747 AG Groningen, University of Groningen, The Netherlands
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Sarah Bourlat
2Zoological Research Museum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany
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Serena Donadi
3Department of Aquatic Resources, Swedish University of Agricultural Science, Sweden
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Michael C. Fontaine
1Groningen Institute for Evolutionary Life-Sciences, GELIFES, Nijenborgh 7, 9747 AG Groningen, University of Groningen, The Netherlands
4Laboratoire MIVEGEC (Université de Montpellier, UMR CNRS 5290, IRD 229), Centre IRD de Montpellier, Montpellier, France
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Joakim P. Hansen
5Stockholm University Baltic Sea Centre, SE-106 91 Stockholm, Sweden
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Eglė Jakubavičiūtė
6Nature Research Centre, Akademijos 2, 08412 Vilnius, Lithuania
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Karine Kiragosyan
1Groningen Institute for Evolutionary Life-Sciences, GELIFES, Nijenborgh 7, 9747 AG Groningen, University of Groningen, The Netherlands
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Martine E. Maan
1Groningen Institute for Evolutionary Life-Sciences, GELIFES, Nijenborgh 7, 9747 AG Groningen, University of Groningen, The Netherlands
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Juha Merilä
7Ecological Genetics Research Unit, Organismal and Evolutionary Biology Research Programme, Faculty Biological & Environmental Sciences, PO Box 65, FI-00014 University of Helsinki, Finland
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Åsa N. Austin
8Department of Ecology, Environment and Plant Sciences, Stockholm University, Sweden
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Jens Olsson
3Department of Aquatic Resources, Swedish University of Agricultural Science, Sweden
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Katrin Reiss
9Faculty for Biosciences and Aquaculture, Nord University, 8049 Bodø, Norway
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Göran Sundblad
3Department of Aquatic Resources, Swedish University of Agricultural Science, Sweden
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Ulf Bergström
3Department of Aquatic Resources, Swedish University of Agricultural Science, Sweden
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Johan S. Eklöf
8Department of Ecology, Environment and Plant Sciences, Stockholm University, Sweden
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Abstract

Declines of large predatory fish due to overexploitation are restructuring food webs across the globe. It is now becoming evident that restoring these altered food webs requires addressing not only ecological processes, but evolutionary ones as well, because human-induced rapid evolution may in turn affect ecological dynamics. In the central Baltic Sea, abundances of the mesopredatory fish, the three-spined stickleback (Gasterosteus aculeatus), have increased dramatically during the past decades. Time-series data covering 22 years show that this increase coincides with a decline in the number of juvenile perch (Perca fluviatilis), the most abundant predator of stickleback along the coast. We studied the interaction between evolutionary and ecological effects of this mesopredator take-over, by surveying the armour plate morphology of stickleback and the structure of the associated food web. First, we investigated the distribution of different stickleback phenotypes depending on predator abundances and benthic production; and described the stomach content of the stickleback phenotypes using metabarcoding. Second, we explored differences in the relation between different trophic levels and benthic production, between bays where the relative abundance of fish was dominated by stickleback or not; and compared this to previous cage-experiments to support causality of detected correlations. We found two distinct lateral armour plate phenotypes of stickleback, incompletely and completely plated. The proportion of incompletely plated individuals increased with increasing benthic production and decreasing abundances of adult perch. Stomach content analyses showed that the completely plated individuals had a stronger preference for invertebrate herbivores (amphipods) than the incompletely plated ones. In addition, predator dominance interacted with ecosystem production to determine food web structure and the propagation of a trophic cascade: with increasing production, biomass accumulated on the first (macroalgae) and third (stickleback) trophic levels in stickleback-dominated bays, but on the second trophic level (invertebrate herbivores) in perch-dominated bays. Since armour plates are defence structures favoured by natural selection in the presence of fish predators, the phenotype distribution suggest that a novel low-predation regime favours sticklebacks with less armour. Our results indicate that an interaction between evolutionary and ecological effects of the stickleback take-over has the potential to affect food web dynamics.

Competing Interest Statement

The authors have declared no competing interest.

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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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The rise of the three-spined stickleback – eco-evolutionary consequences of a mesopredator release
Britas Klemens Eriksson, Casey Yanos, Sarah Bourlat, Serena Donadi, Michael C. Fontaine, Joakim P. Hansen, Eglė Jakubavičiūtė, Karine Kiragosyan, Martine E. Maan, Juha Merilä, Åsa N. Austin, Jens Olsson, Katrin Reiss, Göran Sundblad, Ulf Bergström, Johan S. Eklöf
bioRxiv 2020.05.08.083873; doi: https://doi.org/10.1101/2020.05.08.083873
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The rise of the three-spined stickleback – eco-evolutionary consequences of a mesopredator release
Britas Klemens Eriksson, Casey Yanos, Sarah Bourlat, Serena Donadi, Michael C. Fontaine, Joakim P. Hansen, Eglė Jakubavičiūtė, Karine Kiragosyan, Martine E. Maan, Juha Merilä, Åsa N. Austin, Jens Olsson, Katrin Reiss, Göran Sundblad, Ulf Bergström, Johan S. Eklöf
bioRxiv 2020.05.08.083873; doi: https://doi.org/10.1101/2020.05.08.083873

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