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Egg provisioning explains the penetrance of symbiont-mediated sex allocation distortion in haplodiploids

Heredity volume 131, pages 221–229 (2023)Cite this article

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Abstract

Maternally transmitted symbionts such as Wolbachia can alter sex allocation in haplodiploid arthropods. By biasing population sex ratios towards females, these changes in sex allocation may facilitate the spread of symbionts. In contrast to symbiont-induced cytoplasmic incompatibility (CI), the mechanisms that underpin sex allocation distortion remain poorly understood. Using a nuclear genotype reference panel of the haplodiploid mite Tetranychus urticae and a single Wolbachia variant that is able to simultaneously induce sex allocation distortion and CI, we unraveled the mechanistic basis of Wolbachia-mediated sex allocation distortion. Host genotype was an important determinant for the strength of sex allocation distortion. We further show that sex allocation distortion by Wolbachia in haplodiploid mites is driven by increasing egg size, hereby promoting egg fertilization. This change in reproductive physiology was also coupled to increased male and female adult size. Our results echo previous work on Cardinium symbionts, suggesting that sex allocation distortion by regulating host investment in egg size is a common strategy among symbionts that infect haplodiploids. To better understand the relevance that sex allocation distortion may have for the spread of Wolbachia in natural haplodiploid populations, we parametrized a model based on generated phenotypic data. Our simulations show that empirically derived levels of sex allocation distortion can be sufficient to remove invasion thresholds, allowing CI to drive the spread of Wolbachia independently of the initial infection frequency. Our findings help elucidate the mechanisms that underlie the widespread occurrence of symbionts in haplodiploid arthropods and the evolution of sex allocation.

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Fig. 1: Wolbachia induce two distinct reproductive phenotypes in Tetranychus mites.
Fig. 2: Wolbachia-mediated sex allocation distortion is contingent on the host nuclear genotype.
Fig. 3: Effects of Wolbachia infection on fecundity depend on the host nuclear genotype.
Fig. 4: Wolbachia distort sex allocation in Tetranychus mites by regulating egg provisioning.
Fig. 5: Wolbachia-induced size difference can persist into the adult stage of Tetranychus mites.
Fig. 6: Distortion of host sex allocation is expected to facilitate Wolbachia invasion.

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Acknowledgements

We thank Masahiko Tanahashi for assisting with the Natsumushi analyses, Sara Magalhães and Fabrice Vavre for useful discussions, Martijn Egas for confirming the error in Egas et al. 2002, and Guillaume Martin for his help with identifying the equilibria of the mathematical model. We also thank Bouwe Cattrysse for generating exploratory pilot data for the LonX-c and LonX-w lines. NW was supported by a BOF post-doctoral fellowship (Ghent University, 01P03420) and by a Research Foundation-Flanders (FWO) Research Grant (1513719N). This work was further supported by the FWO Research Network EVENET. This is contribution ISEM-2023-125 of the Institute of Evolutionary Science of Montpellier (ISEM).

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  1. Terrestrial Ecology Unit, Department of Biology, Faculty of Sciences, Ghent University, Ghent, Belgium

    Nicky Wybouw, Emma Van Reempts, Jens Zarka & Dries Bonte

  2. Institute of Evolutionary Science (ISEM), University of Montpellier, CNRS, IRD, EPHE, 34095, Montpellier, France

    Flore Zélé

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Contributions

NW conceived and designed the experiments. NW, EVR, and JZ performed the experiments. FZ extended the model and performed the simulations. NW, FZ, and DB analyzed the data. NW wrote the manuscript with input from FZ and DB. All authors read and approved the final version of the manuscript.

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Correspondence to Nicky Wybouw.

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Wybouw, N., Van Reempts, E., Zarka, J. et al. Egg provisioning explains the penetrance of symbiont-mediated sex allocation distortion in haplodiploids. Heredity 131, 221–229 (2023). https://doi.org/10.1038/s41437-023-00638-1

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