Population dynamics and rapid spread of Cardinium, a bacterial endosymbiont causing cytoplasmic incompatibility in Encarsia pergandiella (Hymenoptera: Aphelinidae)

Abstract

Cytoplasmic incompatibility (CI) is a common phenotype of maternally inherited bacterial symbionts of arthropods; in its simplest expression, uninfected females produce few or no viable progeny when mated to infected males. Infected females thus experience a reproductive advantage relative to that of uninfected females, with the potential for the symbiont to spread rapidly. CI population dynamics are predicted to depend primarily on the strength of incompatibility, the fitness cost of the infection and how faithfully symbionts are inherited. Although the bacterial symbiont lineage Wolbachia has been most identified with the CI phenotype, an unrelated bacterium, Cardinium may also cause CI. In the first examination of population dynamics of CI-inducing Cardinium, we used population cages of the parasitic wasp Encarsia pergandiella (Hymenoptera: Aphelinidae) with varying initial infection frequencies to test a model of invasion. Cardinium was found to spread rapidly in all populations, even in cases where the initial infection frequency was well below the predicted invasion threshold frequency. The discrepancy between the modeled and actual results is best explained by weaker CI than measured in the lab and a cryptic fitness benefit to the infection.

Unique clade of alphaproteobacterial endosymbionts induces complete cytoplasmic incompatibility in the coconut beetle

“…In Wolbachia, 0-100% CI has been reported in different host species (26)(27)(28). In Cardinium, 70% hatchability has been reported in incompatible crosses in spider mites (5), and incompatible crosses in the parasitoid wasp Encarsia pergandiella produced only 7% and 38% of the number of offspring in compatible crosses and showed an 8% pupation rate (6,7). Therefore, the previously unidentified alphaproteobacterial endosymbiont, which induces complete CI, is a strong candidate agent for biological control of the coconut beetle.…”

An insect-endosymbiont conundrum

“…In 2003, Molly Hunter's group at Tucson discovered a second, unrelated bacterium, Cardinium, which could do the same thing (Hunter et al, 2003). In this issue, Harris et al (2009) provide a rare quantitative test of the theory of bacterial spread by CI. They find that Cardinium spreads more readily than theory predicts and explore why this might be so.…”

“…Based on previous studies and new experiments, Harris et al (2009) were able to estimate these parameters. The strength of CI was not as high as often observed in Wolbachia, and uninfected females lost only about two-thirds of their offspring (s h ¼ 0.62) when mating with infected males.…”

“…Our calculation suggests that the threshold frequency that the Cardinium must attain before it can begin to spread is 0.18/0.62 ¼ 0.29. Harris et al (2009) actually did a more sophisticated calculation (Turelli and Hoffmann, 1991;Vavre et al, 2000), taking into account the rare loss of the symbiont during maternal transmission and the haplodiploid genetics of the host (a parasitoid hymenopteran with a bizarre life history, but that is another story), and predicted the threshold was somewhat higher at B0.33, averaged across the sexes.…”

“…To test this prediction, Harris et al (2009) set up population cages for which the initial frequency of infection was 0.15, B0.33 and 0.55, respectively. They expected that in the first case Cardinium would definitely invade, in the last case it definitely would not, while the middle case could go either way.…”