Additive genetic variance for traits least related to fitness increases with environmental stress in the desert locust, Schistocerca gregaria
Abstract Under environmental stress, previously hidden additive genetic variation can be unmasked and exposed to selection. The amount of hidden variation is expected to be higher for life history traits, which strongly correlate to individual fitness, than for morphological traits, in which fitness...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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Wiley
2021-10-01
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| Series: | Ecology and Evolution |
| Subjects: | |
| Online Access: | https://doi.org/10.1002/ece3.8099 |
| _version_ | 1818890982083526656 |
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| author | Marie‐Pierre Chapuis Benjamin Pélissié Cyril Piou Floriane Chardonnet Christine Pagès Antoine Foucart Elodie Chapuis Hélène Jourdan‐Pineau |
| author_facet | Marie‐Pierre Chapuis Benjamin Pélissié Cyril Piou Floriane Chardonnet Christine Pagès Antoine Foucart Elodie Chapuis Hélène Jourdan‐Pineau |
| author_sort | Marie‐Pierre Chapuis |
| collection | DOAJ |
| description | Abstract Under environmental stress, previously hidden additive genetic variation can be unmasked and exposed to selection. The amount of hidden variation is expected to be higher for life history traits, which strongly correlate to individual fitness, than for morphological traits, in which fitness effects are more ambiguous. However, no consensual pattern has been recovered yet, and this idea is still debated in the literature. Here, we hypothesize that the classical categorization of traits (i.e., life history and morphology) may fail to capture their proximity to fitness. In the desert locust, Schistocerca gregaria, a model organism for the study of insect polyphenism, we quantified changes in additive genetic variation elicited by lifetime thermal stress for ten traits, in which evolutionary significance is known. Irrespective of their category, traits under strong stabilizing selection showed genetic invariance with environmental stress, while traits more loosely associated with fitness showed a marked increase in additive genetic variation in the stressful environment. Furthermore, traits involved in adaptive phenotypic plasticity (growth compensation) showed either no change in additive genetic variance or a change of moderate magnitude across thermal environments. We interpret this mitigated response of plastic traits in the context of integrated evolution to adjust the entire phenotype in heterogeneous environments (i.e., adaptiveness of initial plasticity, compromise of phenotypic compensation with stress, and shared developmental pathway). Altogether, our results indicate, in agreement with theoretical expectations, that environmental stress can increase available additive genetic variance in some desert locust traits, but those closely linked to fitness are largely unaffected. Our study also highlights the importance of assessing the proximity to fitness of a trait on a case‐by‐case basis and in an ecologically relevant context, as well as considering the processes of canalization and plasticity, involved in the control of phenotypic variation. |
| first_indexed | 2024-12-19T17:33:33Z |
| format | Article |
| id | doaj.art-85f9182d1c114f0ca83e741103d1ab53 |
| institution | Directory Open Access Journal |
| issn | 2045-7758 |
| language | English |
| last_indexed | 2024-12-19T17:33:33Z |
| publishDate | 2021-10-01 |
| publisher | Wiley |
| record_format | Article |
| series | Ecology and Evolution |
| spelling | doaj.art-85f9182d1c114f0ca83e741103d1ab532022-12-21T20:12:23ZengWileyEcology and Evolution2045-77582021-10-011120139301394710.1002/ece3.8099Additive genetic variance for traits least related to fitness increases with environmental stress in the desert locust, Schistocerca gregariaMarie‐Pierre Chapuis0Benjamin Pélissié1Cyril Piou2Floriane Chardonnet3Christine Pagès4Antoine Foucart5Elodie Chapuis6Hélène Jourdan‐Pineau7CIRAD CBGP Montpellier FranceCIRAD CBGP Montpellier FranceCIRAD CBGP Montpellier FranceCIRAD CBGP Montpellier FranceCIRAD UPR B‐AMR Montpellier FranceCIRAD CBGP Montpellier FranceMIVEGEC Université de MontpellierCNRSIRD Montpellier FranceCIRAD CBGP Montpellier FranceAbstract Under environmental stress, previously hidden additive genetic variation can be unmasked and exposed to selection. The amount of hidden variation is expected to be higher for life history traits, which strongly correlate to individual fitness, than for morphological traits, in which fitness effects are more ambiguous. However, no consensual pattern has been recovered yet, and this idea is still debated in the literature. Here, we hypothesize that the classical categorization of traits (i.e., life history and morphology) may fail to capture their proximity to fitness. In the desert locust, Schistocerca gregaria, a model organism for the study of insect polyphenism, we quantified changes in additive genetic variation elicited by lifetime thermal stress for ten traits, in which evolutionary significance is known. Irrespective of their category, traits under strong stabilizing selection showed genetic invariance with environmental stress, while traits more loosely associated with fitness showed a marked increase in additive genetic variation in the stressful environment. Furthermore, traits involved in adaptive phenotypic plasticity (growth compensation) showed either no change in additive genetic variance or a change of moderate magnitude across thermal environments. We interpret this mitigated response of plastic traits in the context of integrated evolution to adjust the entire phenotype in heterogeneous environments (i.e., adaptiveness of initial plasticity, compromise of phenotypic compensation with stress, and shared developmental pathway). Altogether, our results indicate, in agreement with theoretical expectations, that environmental stress can increase available additive genetic variance in some desert locust traits, but those closely linked to fitness are largely unaffected. Our study also highlights the importance of assessing the proximity to fitness of a trait on a case‐by‐case basis and in an ecologically relevant context, as well as considering the processes of canalization and plasticity, involved in the control of phenotypic variation.https://doi.org/10.1002/ece3.8099climate changegrowthlife history evolutionmorphologypest insectspigmentation |
| spellingShingle | Marie‐Pierre Chapuis Benjamin Pélissié Cyril Piou Floriane Chardonnet Christine Pagès Antoine Foucart Elodie Chapuis Hélène Jourdan‐Pineau Additive genetic variance for traits least related to fitness increases with environmental stress in the desert locust, Schistocerca gregaria Ecology and Evolution climate change growth life history evolution morphology pest insects pigmentation |
| title | Additive genetic variance for traits least related to fitness increases with environmental stress in the desert locust, Schistocerca gregaria |
| title_full | Additive genetic variance for traits least related to fitness increases with environmental stress in the desert locust, Schistocerca gregaria |
| title_fullStr | Additive genetic variance for traits least related to fitness increases with environmental stress in the desert locust, Schistocerca gregaria |
| title_full_unstemmed | Additive genetic variance for traits least related to fitness increases with environmental stress in the desert locust, Schistocerca gregaria |
| title_short | Additive genetic variance for traits least related to fitness increases with environmental stress in the desert locust, Schistocerca gregaria |
| title_sort | additive genetic variance for traits least related to fitness increases with environmental stress in the desert locust schistocerca gregaria |
| topic | climate change growth life history evolution morphology pest insects pigmentation |
| url | https://doi.org/10.1002/ece3.8099 |
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