Section: Evolutionary Biology
Topic:
Evolution,
Genetics/Genomics,
Population biology
How do invasion syndromes evolve? An experimental evolution approach using the ladybird Harmonia axyridis
;
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
Corresponding author(s): Foucaud, Julien (julien.foucaud@inrae.fr)
10.24072/pcjournal.32 - Peer Community Journal, Volume 1 (2021), article no. e33.
Get full text PDF Peer reviewed and recommended by PCI
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.
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
CC-BY 4.0
@article{10_24072_pcjournal_32,
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}},
journal = {Peer Community Journal},
eid = {e33},
publisher = {Peer Community In},
volume = {1},
year = {2021},
doi = {10.24072/pcjournal.32},
url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.32/}
}
TY - JOUR AU - Foucaud, Julien AU - Hufbauer, Ruth A. AU - Ravigné, Virginie AU - Olazcuaga, Laure AU - Loiseau, Anne AU - Ausset, Aurélien AU - Wang, Su AU - Zang, Lian-Sheng AU - Leménager, Nicolas AU - Tayeh, Ashraf AU - Weyna, Arthur AU - Gneux, Pauline AU - Bonnet, Elise AU - Dreuilhe, Vincent AU - Poutout, Bastien AU - Estoup, Arnaud AU - Facon, Benoît TI - How do invasion syndromes evolve? An experimental evolution approach using the ladybird Harmonia axyridis JO - Peer Community Journal PY - 2021 VL - 1 PB - Peer Community In UR - https://peercommunityjournal.org/articles/10.24072/pcjournal.32/ DO - 10.24072/pcjournal.32 ID - 10_24072_pcjournal_32 ER -
%0 Journal Article %A Foucaud, Julien %A Hufbauer, Ruth A. %A Ravigné, Virginie %A Olazcuaga, Laure %A Loiseau, Anne %A Ausset, Aurélien %A Wang, Su %A Zang, Lian-Sheng %A Leménager, Nicolas %A Tayeh, Ashraf %A Weyna, Arthur %A Gneux, Pauline %A Bonnet, Elise %A Dreuilhe, Vincent %A Poutout, Bastien %A Estoup, Arnaud %A Facon, Benoît %T How do invasion syndromes evolve? An experimental evolution approach using the ladybird Harmonia axyridis %J Peer Community Journal %D 2021 %V 1 %I Peer Community In %U https://peercommunityjournal.org/articles/10.24072/pcjournal.32/ %R 10.24072/pcjournal.32 %F 10_24072_pcjournal_32
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.
[1] Natural selection on body size is mediated by multiple interacting factors: a comparison of beetle populations varying naturally and experimentally in body size, Ecology and Evolution, Volume 1 (2011) no. 1, pp. 1-14 | DOI
[2] Selection on breeding date and body size in colonizing coho salmon, Oncorhynchus kisutch, Molecular Ecology (2010), pp. 2562-2573 | DOI
[3] Understanding the evolution and stability of the g-matrix, Evolution, Volume 62 (2008) no. 10, pp. 2451-2461 | DOI
[4] As it happens: current directions in experimental evolution, Biology Letters, Volume 9 (2013) no. 1 | DOI
[5] lme4: Linear mixed-effects models using Eigen and S4. Available: http://CRAN.R-project.org/package=lme4, (2014)
[6] Establishment patterns of exotic birds are constrained by non-random patterns in introduction, Journal of Biogeography, Volume 28 (2001) no. 7, pp. 927-939 | DOI
[7] The evolution of an invasive plant: an experimental study with silene latifolia, Ecology, Volume 85 (2004) no. 11, pp. 3035-3042 | DOI
[8] The distribution of genetic variance across phenotypic space and the response to selection, Molecular Ecology, Volume 24 (2015) no. 9, pp. 2056-2072 | DOI
[9] Synergy between pathogen release and resource availability in plant invasion, Proceedings of the National Academy of Sciences, Volume 106 (2009) no. 19, pp. 7899-7904 | DOI
[10] Generalized linear mixed models: a practical guide for ecology and evolution, Trends in Ecology & Evolution, Volume 24 (2009) no. 3, pp. 127-135 | DOI
[11] Phenotypic and genetic differentiation between native and introduced plant populations, Oecologia, Volume 144 (2005) no. 1, pp. 1-11 | DOI
[12] Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid, BioControl, Volume 53 (2008) no. 1, pp. 5-21 | DOI
[13] boot: Bootstrap R (S-Plus) functions. R package version 1.3-16, (2015)
[14] Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework, Diversity and Distributions, Volume 15 (2009) no. 1, pp. 22-40 | DOI
[15] Can behavioral and personality traits influence the success of unintentional species introductions?, Trends in Ecology & Evolution, Volume 27 (2012) no. 1, pp. 57-64 | DOI
[16] Expanding population edges: theories, traits, and trade‐offs, Global Change Biology, Volume 22 (2016) no. 2, pp. 494-512 | DOI
[17] Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation, Molecular Ecology, Volume 24 (2015) no. 9, pp. 1999-2017 | DOI
[18] Evolutionary constraints on adaptive evolution during range expansion in an invasive plant, Proceedings of the Royal Society B: Biological Sciences, Volume 277 (2010) no. 1689, pp. 1799-1806 | DOI
[19] Experimental support for a resource-based mechanistic model of invasibility, Ecology Letters, Volume 4 (2001) no. 5, pp. 421-428 | DOI
[20] Life-history evolution of an invasive tephritid, Journal of Applied Entomology, Volume 132 (2008) no. 9-10, pp. 695-705 | DOI
[21] Invading populations of an ornamental shrub show rapid life history evolution despite genetic bottlenecks, Ecology Letters, Volume 11 (2008) no. 7, pp. 701-709 | DOI
[22] Adaptation costs to constant and alternating polluted environments, Evolutionary Applications, Volume 10 (2017) no. 8, pp. 839-851 | DOI
[23] Evolution and stability of the G-matrix during the colonization of a novel environment, Journal of Evolutionary Biology, Volume 24 (2011) no. 6, pp. 1363-1373 | DOI
[24] Is There a Genetic Paradox of Biological Invasion?, Annual Review of Ecology, Evolution, and Systematics, Volume 47 (2016) no. 1, pp. 51-72 | DOI
[25] Inbreeding Depression Is Purged in the Invasive Insect Harmonia axyridis, Current Biology, Volume 21 (2011) no. 5, pp. 424-427 | DOI
[26] How and When Selection Experiments Might Actually be Useful, Integrative and Comparative Biology, Volume 45 (2005) no. 3, pp. 391-404 | DOI
[27] Assessing How Fish Predation and Interspecific Prey Competition Influence a Crayfish Assemblage, Ecology, Volume 75 (1994) no. 2, pp. 532-547 | DOI
[28] Resource competition in plant invasions: emerging patterns and research needs, Frontiers in Plant Science, Volume 5 | DOI
[29] Rapid Evolution of a Geographic Cline in Size in an Introduced Fly, Science, Volume 287 (2000) no. 5451, pp. 308-309 | DOI
[30] Artificial selection on larval growth curves in Tribolium : correlated responses and constraints, Journal of Evolutionary Biology, Volume 27 (2014) no. 10, pp. 2069-2079 | DOI
[31] Rapid changes in genetic architecture of behavioural syndromes following colonization of a novel environment, Journal of Evolutionary Biology, Volume 29 (2016) no. 1, pp. 144-152 | DOI
[32] Experimental evolution, Trends in Ecology & Evolution, Volume 27 (2012) no. 10, pp. 547-560 | DOI
[33] History, chance and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection, Ecology Letters, Volume 11 (2008) no. 8, pp. 852-866 | DOI
[34] Phenotypic integration and independence: Hormones, performance, and response to environmental change, Integrative and Comparative Biology, Volume 49 (2009) no. 4, pp. 365-379 | DOI
[35] Direct and indirect phenotypic selection on developmental trajectories in Manduca sexta, Functional Ecology, Volume 26 (2012) no. 3, pp. 598-607 | DOI
[36] Species-based risk assessments for biological invasions: advances and challenges, Diversity and Distributions, Volume 19 (2013) no. 9, pp. 1095-1105 | DOI
[37] Increase in Male Reproductive Success and Female Reproductive Investment in Invasive Populations of the Harlequin Ladybird Harmonia axyridis, PLoS ONE, Volume 8 (2013) no. 10 | DOI
[38] Reduced population size can induce quick evolution of inbreeding depression in the invasive ladybird Harmonia axyridis, Biological Invasions, Volume 18 (2016) no. 10, pp. 2871-2881 | DOI
[39] FactoMineR: AnRPackage for Multivariate Analysis, Journal of Statistical Software, Volume 25 no. 1, pp. 1-18 | DOI
[40] Evolutionary mechanisms of habitat invasions, using the copepod Eurytemora affinis as a model system, Evolutionary Applications, Volume 9 (2016) no. 1, pp. 248-270 | DOI
[41] Response to selection and evolvability of invasive populations, Genetica, Volume 129 (2007) no. 2, pp. 179-192 | DOI
[42] Pumping ions: rapid parallel evolution of ionic regulation following habitat invasions, Evolution, Volume 65 (2011) no. 8, pp. 2229-2244 | DOI
[43] Invasion Ecology, 2nd ed , Wiley-Blackwell, Oxford, UK, 2013, 466 pages
[44] Inferring the origin of populations introduced from a genetically structured native range by approximate Bayesian computation: case study of the invasive ladybird Harmonia axyridis, Molecular Ecology, Volume 20 (2011) no. 22, pp. 4654-4670 | DOI
[45] Complementarity of statistical treatments to reconstruct worldwide routes of invasion: the case of the Asian ladybirdHarmonia axyridis, Molecular Ecology, Volume 23 (2014) no. 24, pp. 5979-5997 | DOI
[46] Do larger individuals cope with resource fluctuations better? An artificial selection approach, Proceedings of the Royal Society B: Biological Sciences, Volume 285 (2018) no. 1884 | DOI
[47] Size‐abundance rules? Evolution changes scaling relationships between size, metabolism and demography, Ecology Letters, Volume 22 (2019) no. 9, pp. 1407-1416 | DOI
[48] Biotic homogenization: a few winners replacing many losers in the next mass extinction, Trends in Ecology & Evolution, Volume 14 (1999) no. 11, pp. 450-453 | DOI
[49] Biotic interactions and plant invasions, Ecology Letters, Volume 9 (2006) no. 6, pp. 726-740 | DOI
[50] Correlated responses to selection for developmental period in Bactrocera cucurbitae (Diptera: Tephritidae): time of mating and daily activity rhythms, Behavior Genetics, Volume 27 (1997) no. 5, pp. 489-498 | DOI
[51] Invasion triangle: an organizational framework for species invasion, Ecology and Evolution, Volume 1 (2011) no. 4, pp. 610-625 | DOI
[52] Life-history evolution in range-shifting populations, Ecology, Volume 91 (2010) no. 6, pp. 1617-1627 | DOI
[53] Invasion and the evolution of speed in toads, Nature, Volume 439 (2006) no. 7078, p. 803 | DOI
[54] R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria., (2021)
[55] Experimentally induced life-history evolution in a natural population, Nature, Volume 346 (1990) no. 6282, pp. 357-359 | DOI
[56] Big houses, big cars, superfleas and the costs of reproduction, Trends in Ecology & Evolution, Volume 15 (2000) no. 10, pp. 421-425 | DOI
[57] The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution, Genetica, Volume 112/113 (2001), pp. 183-198 | DOI
[58] From low to high gear: there has been a paradigm shift in our understanding of evolution, Ecology Letters, Volume 22 (2018) no. 2, pp. 233-244 | DOI
[59] Evolutionary Quantitative Genetics, Springer US, Boston, MA, 1997 | DOI
[60] Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids?, BioControl, Volume 56 (2011) no. 4, pp. 451-468 | DOI
[61] The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology, Biological Invasions, Volume 18 (2016) no. 4, pp. 997-1044 | DOI
[62] Current energy state interacts with the developmental environment to influence behavioural plasticity, Animal Behaviour, Volume 148 (2019), pp. 39-51 | DOI
[63] The Population Biology of Invasive Species, Annual Review of Ecology and Systematics, Volume 32 (2001) no. 1, pp. 305-332 | DOI
[64] Adaptive Radiation Along Genetic Lines of Least Resistance, Evolution, Volume 50 (1996) no. 5, pp. 1766-1774 | DOI
[65] Conflicting selection pressures and life history trade-offs, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 246 (1991) no. 1315, pp. 11-17 | DOI
[66] Bioeconomic forecasting of invasive species by ecological syndrome, Ecosphere, Volume 3 (2012) no. 5 | DOI
[67] Environmentally induced changes in correlated responses to selection reveal variable pleiotropy across a complex genetic network, Evolution, Volume 69 (2015) no. 5, pp. 1128-1142 | DOI
[68] The Covariance Structure of Life-History Characters in Daphnia pulex, Evolution, Volume 45 (1991) no. 5 | DOI
[69] The evolution of life histories, Oxford University Press, London, 1992
[70] Comparative quantitative genetics: evolution of the G matrix, Trends in Ecology & Evolution, Volume 17 (2002) no. 7, pp. 320-327 | DOI
[71] Boom‐bust dynamics in biological invasions: towards an improved application of the concept, Ecology Letters, Volume 20 (2017) no. 10, pp. 1337-1350 | DOI
[72] Evolution in biocontrol strains: insight from the harlequin ladybird Harmonia axyridis, Evolutionary Applications, Volume 5 (2012) no. 5, pp. 481-488 | DOI
[73] Cannibalism in invasive, native and biocontrol populations of the harlequin ladybird, BMC Evolutionary Biology, Volume 14 (2014) no. 1 | DOI
[74] Biological invasion and biological control select for different life histories, Nature Communications, Volume 6 (2015) no. 1 | DOI
[75] Correlated responses to artificial body size selection in growth, development, phenotypic plasticity and juvenile viability in yellow dung flies, Journal of Evolutionary Biology, Volume 20 (2007) no. 1, pp. 87-103 | DOI
[76] Trophic ecology of invasive Argentine ants in their native and introduced ranges, Proceedings of the National Academy of Sciences, Volume 104 (2007) no. 52, pp. 20856-20861 | DOI
[77] Nitrogen inputs promote the spread of an invasive marsh grass, Ecological Applications, Volume 17 (2007) no. 7, pp. 1886-1898 | DOI
[78] Data Analysis, Use R!, Springer International Publishing, Cham, 2016, pp. 189-201 | DOI
[79] How Evolution Modifies the Variability of Range Expansion, Trends in Ecology & Evolution, Volume 34 (2019) no. 10, pp. 903-913 | DOI
[80] Body size in ecological networks, Trends in Ecology & Evolution, Volume 20 (2005) no. 7, pp. 402-409 | DOI
Cited by Sources: