Abstract
Wolbachia are obligate intracellular bacteria that are globally distributed in half of all arthropod species. As the most abundant maternally inherited microbe in animals, Wolbachia manipulate host reproduction via reproductive parasitism strategies, including cytoplasmic incompatibility (CI). CI manifests as embryonic death when Wolbachia-modified sperm fertilize uninfected eggs but not maternally infected eggs. Thus, CI can provide a relative fitness advantage to Wolbachia-infected females and drive the infection through a population. In the genetic model Drosophila melanogaster, the Wolbachia strain wMel induces variable CI, making mechanistic studies in D. melanogaster cumbersome. Here, we demonstrate that sons of older paternal D. melanogaster grandmothers induce stronger CI than sons of younger paternal grandmothers, and we term this relationship the "paternal grandmother age effect" (PGAE). Moreover, the embryos and adult sons of older D. melanogaster grandmothers have higher Wolbachia densities, correlating with their ability to induce stronger CI. In addition, we report that Wolbachia density positively correlates with female age and decreases after mating, suggesting that females transmit Wolbachia loads that are proportional to their own titers. These findings reveal a transgenerational impact of age on wMel-induced CI, elucidate Wolbachia density dynamics in D. melanogaster, and provide a methodological advance to studies aimed at understanding wMel-induced CI in the D. melanogaster model.IMPORTANCE Unidirectional cytoplasmic incompatibility (CI) results in a postfertilization incompatibility between Wolbachia-infected males and uninfected females. CI contributes to reproductive isolation between closely related species and is used in worldwide vector control programs to drastically lower arboviral vector population sizes or to replace populations that transmit arboviruses with those resistant to transmission. Despite decades of research on the factors that influence CI, penetrance is often variable under controlled laboratory conditions in various arthropods, suggesting that additional variables influence CI strength. Here, we demonstrate that paternal D. melanogaster grandmother age influences the strength of CI induced by their sons. Older D. melanogaster females have higher Wolbachia densities and produce offspring with higher Wolbachia densities that associate with stronger CI. This work reveals a multigenerational impact of age on CI and expands our understanding of host-Wolbachia interactions and the biology of CI induced by the Wolbachia strain infecting the most widely used arthropod model, D. melanogaster.
Highlights
Wolbachia are obligate intracellular bacteria that are globally distributed in half of all arthropod species
Global vector control efforts have successfully leveraged cytoplasmic incompatibility (CI) to either suppress native populations [16,17,18,19] or promote the spread of disease-resistant Wolbachia strains [20,21,22] through release of mosquitoes transinfected with the wMel Wolbachia strain of Drosophila melanogaster. wMel’s success in these efforts is partially due to the strong CI that it induces in mosquito hosts [23, 24]; in the native host D. melanogaster, wMel’s CI strength can range from an average of nearly 0% to 100% [25,26,27,28,29,30,31,32]
To test the hypothesis that D. melanogaster paternal grandmother age influences the strength of CI, we measured the percentage of surviving offspring produced by sons of differentially aged, infected y1w* grandmothers
Summary
Wolbachia are obligate intracellular bacteria that are globally distributed in half of all arthropod species. There are numerous factors reported to impact the penetrance of wMel-induced CI: Wolbachia density in the testes [25, 33], expression level of the CI genes cifA and cifB [29, 34], male age [30], male mating rate [30, 35], time of male emergence [32], fly rearing density [32], and temperature [30] These factors are not independent, and they have likely hampered the researcher’s ability to use the vast resources of D. melanogaster for the study of reproductive parasitism and endosymbiosis. This work enhances our understanding of Wolbachia-host dynamics and provides methodological techniques of importance to studies of wMel-induced CI in D. melanogaster
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