Cardinium Localization During Its Parasitoid Wasp Host’s Development Provides Insights Into Cytoplasmic Incompatibility

Matthew R Doremus,Martha S Hunter,Suzanne E Kelly,Corinne M Stouthamer,Stephan Schmitz-Esser

doi:10.3389/fmicb.2020.606399

Matthew R Doremus, Martha S Hunter + Show 3 more

Open Access

https://doi.org/10.3389/fmicb.2020.606399

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Abstract

Arthropods harbor heritable intracellular symbionts that may manipulate host reproduction to favor symbiont transmission. In cytoplasmic incompatibility (CI), the symbiont sabotages the reproduction of infected males such that high levels of offspring mortality result when they mate with uninfected females. In crosses with infected males and infected females, however (the “rescue” cross), normal numbers of offspring are produced. A common CI-inducing symbiont, Cardinium hertigii, causes variable levels of CI mortality in the parasitoid wasp, Encarsia suzannae. Previous work correlated CI-induced mortality with male development time in this system, although the timing of Cardinium CI-induction and the relationship between development time and CI mortality was not well understood. Here, using a combination of crosses, manipulation of development time, and fluorescence microscopy, we identify the localization and the timing of the CI-induction step in the Cardinium-E. suzannae system. Antibiotic treatment of adult Cardinium-infected males did not reduce the mortality associated with the CI phenotype, suggesting that CI-alteration occurs prior to adulthood. Our results suggest that the alteration step occurs during the pupal period, and is limited by the duration of pupal development: 1) Encarsia produces most sperm prior to adulthood, 2) FISH localization of Cardinium in testes showed an association with sperm nuclei throughout spermatogenesis but not with mature sperm, and 3) two methods of prolonging the pupal period (cool temperatures and the juvenile hormone analog methoprene) both caused greater CI mortality, suggesting the degree of alteration is limited by the duration of the pupal stage. Based on these results, we compare two models for potential mechanisms of Cardinium sperm modification in the context of what is known about analogous mechanisms of Wolbachia, a more extensively studied CI-inducing symbiont.

Highlights

Terrestrial arthropods commonly harbor heritable intracellular bacteria that spread vertically in egg cytoplasm from infected mothers to offspring (Moran et al, 2008)
Encarsia suzannae is a minute parasitoid wasp (Hymenoptera: Aphelinidae) with an unusual life history; females develop within immature whitefly nymphs, while males develop as hyperparasitoids, meaning they are parasitic on conspecific pupal females or other pupal aphelinid wasps (Hunter and Woolley, 2001)
We found that antibiotic treatment of adult male E. suzannae did not interfere with the cytoplasmic incompatibility (CI) phenotype

Summary

Introduction

Terrestrial arthropods commonly harbor heritable intracellular bacteria that spread vertically in egg cytoplasm from infected mothers to offspring (Moran et al, 2008). As these heritable symbionts rely on female host reproduction for their own success, many manipulate host reproduction to favor infected female progeny capable of transmitting the symbiont, often at the expense of male or uninfected hosts (Doremus and Hunter, 2020). A common manipulation by symbionts is cytoplasmic incompatibility (CI), a mating incompatibility that arises between symbiont-infected males and uninfected females The offspring of this cross do not harbor the symbiont, and die early in development. CI acts to drive the symbiont infection through a host population by granting infected females a fitness advantage relative to uninfected females (Turelli, 1994)

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