Rapid and transient evolution of local adaptation to seasonal host fruits in an invasive pest fly
Abstract Both 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...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Oxford University Press
2022-12-01
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| Series: | Evolution Letters |
| Subjects: | |
| Online Access: | https://doi.org/10.1002/evl3.304 |
| _version_ | 1797704265282617344 |
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| author | Laure Olazcuaga Julien Foucaud Candice Deschamps Anne Loiseau Jean‐Loup Claret Romain Vedovato Robin Guilhot Cyril Sévely Mathieu Gautier Ruth A. Hufbauer Nicolas O. Rode Arnaud Estoup |
| author_facet | Laure Olazcuaga Julien Foucaud Candice Deschamps Anne Loiseau Jean‐Loup Claret Romain Vedovato Robin Guilhot Cyril Sévely Mathieu Gautier Ruth A. Hufbauer Nicolas O. Rode Arnaud Estoup |
| author_sort | Laure Olazcuaga |
| collection | DOAJ |
| description | Abstract Both 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. |
| first_indexed | 2024-03-12T05:16:43Z |
| format | Article |
| id | doaj.art-7a2c822456874511973d1a38e7474d57 |
| institution | Directory Open Access Journal |
| issn | 2056-3744 |
| language | English |
| last_indexed | 2024-03-12T05:16:43Z |
| publishDate | 2022-12-01 |
| publisher | Oxford University Press |
| record_format | Article |
| series | Evolution Letters |
| spelling | doaj.art-7a2c822456874511973d1a38e7474d572023-09-03T08:02:48ZengOxford University PressEvolution Letters2056-37442022-12-016649050510.1002/evl3.304Rapid and transient evolution of local adaptation to seasonal host fruits in an invasive pest flyLaure Olazcuaga0Julien Foucaud1Candice Deschamps2Anne Loiseau3Jean‐Loup Claret4Romain Vedovato5Robin Guilhot6Cyril Sévely7Mathieu Gautier8Ruth A. Hufbauer9Nicolas O. Rode10Arnaud Estoup11CBGP, INRAE, CIRAD, IRD, Institut Agro, Univ Montpellier Montpellier 34988 FranceCBGP, INRAE, CIRAD, IRD, Institut Agro, Univ Montpellier Montpellier 34988 FranceCBGP, INRAE, CIRAD, IRD, Institut Agro, Univ Montpellier Montpellier 34988 FranceCBGP, INRAE, CIRAD, IRD, Institut Agro, Univ Montpellier Montpellier 34988 FranceCBGP, INRAE, CIRAD, IRD, Institut Agro, Univ Montpellier Montpellier 34988 FranceCBGP, INRAE, CIRAD, IRD, Institut Agro, Univ Montpellier Montpellier 34988 FranceCBGP, INRAE, CIRAD, IRD, Institut Agro, Univ Montpellier Montpellier 34988 FranceChambre d'agriculture de l'Hérault Lattes 34875 FranceCBGP, INRAE, CIRAD, IRD, Institut Agro, Univ Montpellier Montpellier 34988 FranceDepartment of Agricultural Biology Colorado State University Fort Collins Colorado 80523 USACBGP, INRAE, CIRAD, IRD, Institut Agro, Univ Montpellier Montpellier 34988 FranceCBGP, INRAE, CIRAD, IRD, Institut Agro, Univ Montpellier Montpellier 34988 FranceAbstract Both 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.https://doi.org/10.1002/evl3.304Adaptive phenotypic plasticityDrosophila suzukiigenetic effectshost fruitslocal adaptationreciprocal common garden experiment |
| spellingShingle | Laure Olazcuaga Julien Foucaud Candice Deschamps Anne Loiseau Jean‐Loup Claret Romain Vedovato Robin Guilhot Cyril Sévely Mathieu Gautier Ruth A. Hufbauer Nicolas O. Rode Arnaud Estoup Rapid and transient evolution of local adaptation to seasonal host fruits in an invasive pest fly Evolution Letters Adaptive phenotypic plasticity Drosophila suzukii genetic effects host fruits local adaptation reciprocal common garden experiment |
| title | Rapid and transient evolution of local adaptation to seasonal host fruits in an invasive pest fly |
| title_full | Rapid and transient evolution of local adaptation to seasonal host fruits in an invasive pest fly |
| title_fullStr | Rapid and transient evolution of local adaptation to seasonal host fruits in an invasive pest fly |
| title_full_unstemmed | Rapid and transient evolution of local adaptation to seasonal host fruits in an invasive pest fly |
| title_short | Rapid and transient evolution of local adaptation to seasonal host fruits in an invasive pest fly |
| title_sort | rapid and transient evolution of local adaptation to seasonal host fruits in an invasive pest fly |
| topic | Adaptive phenotypic plasticity Drosophila suzukii genetic effects host fruits local adaptation reciprocal common garden experiment |
| url | https://doi.org/10.1002/evl3.304 |
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