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Cardinium Localization During Its Parasitoid Wasp Host's Development Provides Insights Into Cytoplasmic
Matthew R Doremus1, Corinne M Stouthamer2, Suzanne E Kelly2
1Graduate Interdisciplinary Program in Entomology and Insect Science, University of Arizona, Tucson, AZ, United States.
Insights
Cardinium hertigii symbionts induce cytoplasmic incompatibility (CI) in Encarsia suzannae wasps. CI-induced mortality is linked to the pupal development duration, suggesting sperm alteration occurs during this stage.
Area of Science:
- Evolutionary Biology
- Microbiology
- Insect Reproduction
Background:
- Heritable intracellular symbionts in arthropods can manipulate host reproduction to enhance symbiont transmission.
- Cytoplasmic incompatibility (CI) is a reproductive manipulation where infected males cause high offspring mortality with uninfected females, but not with infected females.
Purpose of the Study:
- To determine the timing and localization of the CI-induction step by Cardinium hertigii in the parasitoid wasp Encarsia suzannae.
- To investigate the relationship between male development time and CI-induced mortality in this symbiont-host system.
Main Methods:
- Conducted crosses between infected and uninfected male and female Encarsia suzannae.
- Manipulated male development time using cool temperatures and methoprene (a juvenile hormone analog).
- Used fluorescence microscopy and FISH (fluorescence in situ hybridization) to localize Cardinium within male testes.
- Treated adult males with antibiotics to test the timing of CI induction.
Main Results:
- Antibiotic treatment of adult males did not reduce CI-induced mortality, indicating CI alteration occurs before adulthood.
- FISH analysis showed Cardinium associated with sperm nuclei during spermatogenesis but not mature sperm.
- Prolonging pupal development (via cool temperatures or methoprene) increased CI mortality, suggesting alteration is limited by pupal duration.
Conclusions:
- The CI-induction step by Cardinium in Encarsia suzannae occurs during the pupal stage and is dependent on the duration of this developmental period.
- Results suggest Cardinium modifies sperm during spermatogenesis within the pupa, with the extent of modification limited by development time.
- The findings provide insights into potential mechanisms of sperm modification by Cardinium, drawing comparisons to similar processes in Wolbachia.
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.
