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Section: Evolutionary Biology
Topic: Evolution, Genetics/Genomics, Population biology

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

Foucaud, Julien1 ; Hufbauer, Ruth A.2, 1 ; Ravigné, Virginie3 ; Olazcuaga, Laure1 ; Loiseau, Anne1 ; Ausset, Aurélien1 ; Wang, Su4 ; Zang, Lian-Sheng5 ; Leménager, Nicolas1 ; Tayeh, Ashraf1 ; Weyna, Arthur1 ; Gneux, Pauline1 ; Bonnet, Elise1 ; Dreuilhe, Vincent1 ; Poutout, Bastien1 ; Estoup, Arnaud1 ; Facon, Benoît1
1 UMR CBGP (INRA-IRD-CIRAD, Montpellier SupAgro), Campus International de Baillarguet, CS 30 016, 34988 Montferrier / Lez cedex, France
2 Colorado State Univ, Dept Bioagr Sci & Pest Management, Graduate Degree Program in Ecology, Ft Collins, CO 80523 USA
3 PHIM Plant Health Institute, Univ Montpellier, CIRAD, INRAE, Institut Agro, IRD, Montpellier, France
4 Beijing Academy of Agriculture and Forestry Sciences, China
5 Institute of Biological Control, Jilin Agricultural University, Changchun, China

10.24072/pcjournal.32 - Peer Community Journal, Volume 1 (2021), article no. e33.

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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.

Published online:
DOI: 10.24072/pcjournal.32
Type: Research article
Foucaud, Julien 1; Hufbauer, Ruth A. 2, 1; Ravigné, Virginie 3; Olazcuaga, Laure 1; Loiseau, Anne 1; Ausset, Aurélien 1; Wang, Su 4; Zang, Lian-Sheng 5; Leménager, Nicolas 1; Tayeh, Ashraf 1; Weyna, Arthur 1; Gneux, Pauline 1; Bonnet, Elise 1; Dreuilhe, Vincent 1; Poutout, Bastien 1; Estoup, Arnaud 1; Facon, Benoît 1

1 UMR CBGP (INRA-IRD-CIRAD, Montpellier SupAgro), Campus International de Baillarguet, CS 30 016, 34988 Montferrier / Lez cedex, France
2 Colorado State Univ, Dept Bioagr Sci & Pest Management, Graduate Degree Program in Ecology, Ft Collins, CO 80523 USA
3 PHIM Plant Health Institute, Univ Montpellier, CIRAD, INRAE, Institut Agro, IRD, Montpellier, France
4 Beijing Academy of Agriculture and Forestry Sciences, China
5 Institute of Biological Control, Jilin Agricultural University, Changchun, China
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
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     author = {Foucaud, Julien and Hufbauer, Ruth A. and Ravign\'e, Virginie and Olazcuaga, Laure and Loiseau, Anne and Ausset, Aur\'elien and Wang, Su and Zang, Lian-Sheng and Lem\'enager, Nicolas and Tayeh, Ashraf and Weyna, Arthur and Gneux, Pauline and Bonnet, Elise and Dreuilhe, Vincent and Poutout, Bastien and Estoup, Arnaud and Facon, Beno{\^\i}t},
     title = {How do invasion syndromes evolve? {An} experimental evolution approach using the ladybird {\protect\emph{Harmonia} axyridis}},
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Foucaud, Julien; Hufbauer, Ruth A.; Ravigné, Virginie; Olazcuaga, Laure; Loiseau, Anne; Ausset, Aurélien; Wang, Su; Zang, Lian-Sheng; Leménager, Nicolas; Tayeh, Ashraf; Weyna, Arthur; Gneux, Pauline; Bonnet, Elise; Dreuilhe, Vincent; Poutout, Bastien; Estoup, Arnaud; Facon, Benoît. How do invasion syndromes evolve? An experimental evolution approach using the ladybird Harmonia axyridis. Peer Community Journal, Volume 1 (2021), article  no. e33. doi : 10.24072/pcjournal.32. https://peercommunityjournal.org/articles/10.24072/pcjournal.32/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.evolbiol.100096

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

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