Rapid and transient evolution of local adaptation to seasonal host fruits in an invasive pest fly

Author:

Olazcuaga Laure12ORCID,Foucaud Julien1ORCID,Deschamps Candice1ORCID,Loiseau Anne1ORCID,Claret Jean-Loup1ORCID,Vedovato Romain1,Guilhot Robin1ORCID,Sévely Cyril3,Gautier Mathieu1ORCID,Hufbauer Ruth A.24ORCID,Rode Nicolas O.1ORCID,Estoup Arnaud1ORCID

Affiliation:

1. CBGP, INRAE, CIRAD, IRD, Institut Agro, Univ Montpellier Montpellier 34988 France

2. Department of Agricultural Biology Colorado State University Fort Collins Colorado 80523 USA

3. Chambre d'agriculture de l'Hérault Lattes 34875 France

4. Graduate Degree Program in Ecology Colorado State University Fort Collins Colorado 80523 USA

Abstract

AbstractBoth local adaptation and adaptive phenotypic plasticity can influence the match between phenotypic traits and local environmental conditions. Theory predicts that environments stable for multiple generations promote local adaptation, whereas highly heterogeneous environments favor adaptive phenotypic plasticity. However, when environments have periods of stability mixed with heterogeneity, the relative importance of local adaptation and adaptive phenotypic plasticity is unclear. Here, we used Drosophila suzukii as a model system to evaluate the relative influence of genetic and plastic effects on the match of populations to environments with periods of stability from three to four generations. This invasive pest insect can develop within different fruits, and persists throughout the year in a given location on a succession of distinct host fruits, each one being available for only a few generations. Using reciprocal common environment experiments of natural D. suzukii populations collected from cherry, strawberry, and blackberry, we found that both oviposition preference and offspring performance were higher on medium made with the fruit from which the population originated than on media made with alternative fruits. This pattern, which remained after two generations in the laboratory, was analyzed using a statistical method we developed to quantify the contributions of local adaptation and adaptive plasticity in determining fitness. Altogether, we found that genetic effects (local adaptation) dominate over plastic effects (adaptive phenotypic plasticity). Our study demonstrates that spatially and temporally variable selection does not prevent the rapid evolution of local adaptation in natural populations. The speed and strength of adaptation may be facilitated by several mechanisms including a large effective population size and strong selective pressures imposed by host plants.

Publisher

Oxford University Press (OUP)

Subject

Genetics,Ecology, Evolution, Behavior and Systematics

Reference82 articles.

1. Laboratory host selection and development of immature Drosophila suzukii (Diptera: Drosophilidae) on fruits and artificial diets;Aly;J. Phytopathol. Pest Manag.,2018

2. Re-evaluating the costs and limits of adaptive phenotypic plasticity;Auld;Proc. R. Soc. Edinburgh, Sect. B: Biol. Sci.,2010

3. Polygenic adaptation: a unifying framework to understand positive selection;Barghi;Nat Rev Genet,2020

4. Dietary yeast affects preference and performance in Drosophila suzukii;Bellutti;J. Pest Sci.,2018

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