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Wing polyphenism in a water strider is caused by photoperiod-induced expression of the Fat/Hippo pathway
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, 46, allée d’Italie, 69364 Lyon Cedex 07, France.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, 46, allée d’Italie, 69364 Lyon Cedex 07, France.ORCID iD: 0000-0003-0908-483x
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

The genetic mechanisms that allow organisms to incorporate information from the environment into developmental programs that control size, shape and color are important to identify in order to more fully understand developmental plasticity and adaptation to changing environments. Insect polyphenisms provide good models to study such mechanisms because environmental factors are the main source of variation in the trait of study. Here we studied the regulatory mechanism that controls wing length polyphenism in the water strider Gerris buenoi, which is primarily controlled by variation in photoperiod. By sequencing RNA sampled from wing buds across development in different photoperiodic conditions (and therefore alternative wing developmental trajectories) we found that differences in transcriptional activity arose primarily in the late 5th instar stage. Among the differentially expressed genes, the Fat/Hippo and ecdysone signaling pathways, both putative growth regulatory mechanisms that could underlie wing morph determination, were among those that showed significant enrichment. We therefore used RNA interference against the differentially expressed genes Fat, Dachsous and Yorkie to assess whether they play a causative role in photoperiod induced wing length variation in Gerris buenoi. Our results suggest that the conserved Fat/Hippo pathway is a key regulatory network involved in the control of wing polyphenism in this species. Therefore, photoperiod induces wing polyphenism in Gerris buenoi through its regulation of the Fat/Hippo pathway. This study provides an important basis for future comparative studies on the evolution of wing polyphenism and furthers our understanding of the genetic regulation of this process in insects.

Keywords [en]
wing polyphenism, Fat, Dachsous, Yorkie, Fat/Hippo pathway, Hippo pathway, RNAi, water strider
National Category
Biological Sciences
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
URN: urn:nbn:se:uu:diva-495371OAI: oai:DiVA.org:uu-495371DiVA, id: diva2:1731316
Funder
Swedish Research Council, 2020-03349, 2020-04298Available from: 2023-01-26 Created: 2023-01-26 Last updated: 2023-02-02
In thesis
1. From environmental cue to phenotypic variation – a functional investigation of wing polyphenism in an emerging model species
Open this publication in new window or tab >>From environmental cue to phenotypic variation – a functional investigation of wing polyphenism in an emerging model species
2023 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Phenotypic plasticity is a ubiquitous feature of living organisms and enable individuals to adapt to changing environments. A particularly prominent example of plasticity is found in polyphenisms, where environmental cues received during development leads to the generation of discrete variation in populations. In this thesis, I have studied the mechanisms underlying wing polyphenism in the water strider Gerris buenoi in order to contribute to the understanding how environmental factors can act through growth regulatory systems to induce adaptive variation. Specifically, in Paper I, I investigated which environmental factors control wing morph determination in G. buenoi and found that this species most strongly responds to variation in photoperiod conditions, but also to crowding during the juvenile stages. Exposure to challenging nutritional conditions had no effect on wing morph frequencies. Further, I found that the nutrient sensitive insulin/insulin-like growth factor signaling pathway, which have been found to regulate wing polyphenism in species where nutrition is a determinant cue for wing morph induction, has no role in regulating G. buenoi wing polyphenism, an observation in line with data showing that wing morph determination is robust to variation in nutrient conditions. In Paper II, I explored a role for the developmentally important hormones ecdysone and juvenile hormone in G. buenoi wing polyphenism. Here, I used microinjections of 20-hydroxyecdysone and topical application of methoprene, as well as RNAi against hormone receptors for ecdysone and juvenile hormone. In these experiments, I found a small but significant effect of RNAi against the ecdysone receptor, indicating that ecdysone may play a role in wing morph induction. In Paper III, I used RNA sequencing to identify candidate growth regulatory pathways for wing morph induction by photoperiod and found a significant role for the conserved Fat/Hippo pathway in G. buenoi wing morph determination. Taken together, the results presented in this thesis suggest that evolution of genetic mechanisms underlying wing polyphenism may be constrained with regard to the particular environmental cue that is used to predict the future adaptive landscape. Further, the work presented in this thesis demonstrates the power in combining sequencing methods with functional genetic tools in order to more deeply characterize the causal basis to adaptive variation, an approach to ecological and evolutionary studies which I reviewed in Paper IV.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2023. p. 57
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 2231
Keywords
Gerris buenoi, water strider, wing polyphenism, photoperiodism, Fat/Hippo signaling
National Category
Biological Sciences
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-495377 (URN)978-91-513-1697-0 (ISBN)
Public defence
2023-03-17, Ekmanssalen 15:00024, EBC, Norbyvägen 16, Uppsala, 13:30 (English)
Opponent
Supervisors
Available from: 2023-02-23 Created: 2023-01-26 Last updated: 2023-02-23

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Gudmunds, ErikKhila, AbderrahmanHusby, Arild

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Gudmunds, E. & Armisen, D. (2023). Supplementary Data File 1. Wing polyphenism in a water strider is caused by photoperiod-induced expression of the Fat/Hippo pathway.

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