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How do invasion syndromes evolve? An experimental evolution approach using the ladybird Harmonia axyridis

View ORCID ProfileJulien Foucaud, View ORCID ProfileRuth A. Hufbauer, View ORCID ProfileVirginie Ravigné, View ORCID ProfileLaure Olazcuaga, Anne Loiseau, Aurélien Ausset, View ORCID ProfileSu Wang, View ORCID ProfileLian-Sheng Zang, Nicolas Leménager, View ORCID ProfileAshraf Tayeh, Arthur Weyna, Pauline Gneux, Elise Bonnet, Vincent Dreuilhe, Bastien Poutout, View ORCID ProfileArnaud Estoup, Benoît Facon
doi: https://doi.org/10.1101/849968
Julien Foucaud
1UMR CBGP (INRA-IRD-CIRAD, Montpellier SupAgro), Campus International de Baillarguet, CS 30 016, 34988 Montferrier / Lez cedex, France
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  • For correspondence: benoit.facon@inrae.fr julien.foucaud@inrae.fr
Ruth A. Hufbauer
1UMR CBGP (INRA-IRD-CIRAD, Montpellier SupAgro), Campus International de Baillarguet, CS 30 016, 34988 Montferrier / Lez cedex, France
2Colorado State Univ, Dept Bioagr Sci & Pest Management, Graduate Degree Program in Ecology, Ft Collins, CO 80523 USA
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  • ORCID record for Ruth A. Hufbauer
Virginie Ravigné
3CIRAD, UMR PVBMT, F-97410 Saint-Pierre, Réunion, France
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  • ORCID record for Virginie Ravigné
Laure Olazcuaga
1UMR CBGP (INRA-IRD-CIRAD, Montpellier SupAgro), Campus International de Baillarguet, CS 30 016, 34988 Montferrier / Lez cedex, France
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Anne Loiseau
1UMR CBGP (INRA-IRD-CIRAD, Montpellier SupAgro), Campus International de Baillarguet, CS 30 016, 34988 Montferrier / Lez cedex, France
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Aurélien Ausset
1UMR CBGP (INRA-IRD-CIRAD, Montpellier SupAgro), Campus International de Baillarguet, CS 30 016, 34988 Montferrier / Lez cedex, France
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Su Wang
4Beijing Academy of Agriculture and Forestry Sciences, China
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Lian-Sheng Zang
5Institute of Biological Control, Jilin Agricultural University, Changchun, China
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  • ORCID record for Lian-Sheng Zang
Nicolas Leménager
1UMR CBGP (INRA-IRD-CIRAD, Montpellier SupAgro), Campus International de Baillarguet, CS 30 016, 34988 Montferrier / Lez cedex, France
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Ashraf Tayeh
1UMR CBGP (INRA-IRD-CIRAD, Montpellier SupAgro), Campus International de Baillarguet, CS 30 016, 34988 Montferrier / Lez cedex, France
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Arthur Weyna
1UMR CBGP (INRA-IRD-CIRAD, Montpellier SupAgro), Campus International de Baillarguet, CS 30 016, 34988 Montferrier / Lez cedex, France
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Pauline Gneux
1UMR CBGP (INRA-IRD-CIRAD, Montpellier SupAgro), Campus International de Baillarguet, CS 30 016, 34988 Montferrier / Lez cedex, France
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Elise Bonnet
1UMR CBGP (INRA-IRD-CIRAD, Montpellier SupAgro), Campus International de Baillarguet, CS 30 016, 34988 Montferrier / Lez cedex, France
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Vincent Dreuilhe
1UMR CBGP (INRA-IRD-CIRAD, Montpellier SupAgro), Campus International de Baillarguet, CS 30 016, 34988 Montferrier / Lez cedex, France
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Bastien Poutout
1UMR CBGP (INRA-IRD-CIRAD, Montpellier SupAgro), Campus International de Baillarguet, CS 30 016, 34988 Montferrier / Lez cedex, France
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Arnaud Estoup
1UMR CBGP (INRA-IRD-CIRAD, Montpellier SupAgro), Campus International de Baillarguet, CS 30 016, 34988 Montferrier / Lez cedex, France
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Benoît Facon
6INRA, UMR PVBMT, F-97410 Saint-Pierre, Réunion, France
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  • For correspondence: benoit.facon@inrae.fr julien.foucaud@inrae.fr
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ABSTRACT

Experiments comparing native to introduced populations or distinct introduced populations to each other show that phenotypic evolution is common and often involves a suit of interacting phenotypic traits. We define such sets of traits that evolve in concert and contribute to the success of invasive populations as an ‘invasion syndrome’. The invasive Harlequin ladybird Harmonia axyridis displays such an invasion syndrome with, for instance, females from invasive populations being larger and heavier than individuals from native populations, allocating more resources to reproduction, and spreading reproduction over a longer lifespan. Invasion syndromes could emerge due to selection acting jointly and directly on a multitude of traits, or due to selection on one or a few key traits that drive correlated indirect responses in other traits. Here, we investigated the degree to which the H. axyridis invasion syndrome would emerge in response to artificial selection on either female body mass or on age at first reproduction, two traits involved in their invasion syndrome. To further explore the interaction between environmental context and evolutionary change in molding the phenotypic response, we phenotyped the individuals from the selection experiments in two environments, one with abundant food resources and one with limited resources. The two artificial selection experiments show that the number of traits showing a correlated response depends upon the trait undergoing direct selection. Artificial selection on female body mass resulted in few correlated responses and hence poorly reproduced the invasion syndrome. In contrast, artificial selection on age at first reproduction resulted in more widespread phenotypic changes, which nevertheless corresponded only partly to the invasion syndrome. The artificial selection experiments also revealed a large impact of diet on the traits, with effects dependent on the trait considered and the selection regime. Overall, our results indicate that direct selection on multiple traits was likely necessary in the evolution of the H. axyridis invasion syndrome. Furthermore, they show the strength of using artificial selection to identify the traits that are correlated in different selective contexts, which represents a crucial first step in understanding the evolution of complex phenotypic patterns, including invasion syndromes.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Manuscript and figures updated following Peer Community in Evolutionary Biology revision round 2. Datasets and R code made public.

  • https://data.inra.fr/dataset.xhtml?persistentId=doi:10.15454/V9XCA2

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 4.0 International license.
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Posted April 23, 2020.
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How do invasion syndromes evolve? An experimental evolution approach using the ladybird Harmonia axyridis
Julien Foucaud, Ruth A. Hufbauer, Virginie Ravigné, Laure Olazcuaga, Anne Loiseau, Aurélien Ausset, Su Wang, Lian-Sheng Zang, Nicolas Leménager, Ashraf Tayeh, Arthur Weyna, Pauline Gneux, Elise Bonnet, Vincent Dreuilhe, Bastien Poutout, Arnaud Estoup, Benoît Facon
bioRxiv 849968; doi: https://doi.org/10.1101/849968
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How do invasion syndromes evolve? An experimental evolution approach using the ladybird Harmonia axyridis
Julien Foucaud, Ruth A. Hufbauer, Virginie Ravigné, Laure Olazcuaga, Anne Loiseau, Aurélien Ausset, Su Wang, Lian-Sheng Zang, Nicolas Leménager, Ashraf Tayeh, Arthur Weyna, Pauline Gneux, Elise Bonnet, Vincent Dreuilhe, Bastien Poutout, Arnaud Estoup, Benoît Facon
bioRxiv 849968; doi: https://doi.org/10.1101/849968

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