Wolbachia do not live by reproductive manipulation alone: infection polymorphism in Drosophila suzukii and D. subpulchrella

Abstract

Drosophila suzukii recently invaded North America and Europe. Populations in Hawaii, California, New York and Nova Scotia are polymorphic for Wolbachia, typically with <20% infection frequency. The Wolbachia in D. suzukii, denoted wSuz, is closely related to wRi, the variant prevalent in continental populations of D. simulans. wSuz is also nearly identical to Wolbachia found in D. subpulchrella, plausibly D. suzukii's sister species. This suggests vertical Wolbachia transmission through cladogenesis ('cladogenic transmission'). The widespread occurrence of 7-20% infection frequencies indicates a stable polymorphism. wSuz is imperfectly maternally transmitted, with wild infected females producing on average 5-10% uninfected progeny. As expected from its low frequency, wSuz produces no cytoplasmic incompatibility (CI), that is, no increased embryo mortality when infected males mate with uninfected females, and no appreciable sex-ratio distortion. The persistence of wSuz despite imperfect maternal transmission suggests positive fitness effects. Assuming a balance between selection and imperfect transmission, we expect a fitness advantage on the order of 20%. Unexpectedly, Wolbachia-infected females produce fewer progeny than do uninfected females. We do not yet understand the maintenance of wSuz in D. suzukii. The absence of detectable CI in D. suzukii and D. subpulchrella makes it unlikely that CI-based mechanisms could be used to control this species without transinfection using novel Wolbachia. Contrary to their reputation as horizontally transmitted reproductive parasites, many Wolbachia infections are acquired through introgression or cladogenesis and many cause no appreciable reproductive manipulation. Such infections, likely to be mutualistic, may be central to understanding the pervasiveness of Wolbachia among arthropods.

Keywords: endosymbiont; fecundity; mutualism; reproductive manipulation; transmission.

Fig. 1

Map of D. suzukii samples used in this study (open circles) and timing of first detection by state (modified with permission from Burrack et al. 2012).

Fig. 2

Phylogenetic trees: A) Bayesian phylogeny depicting the relationships among relatives of D. suzukii; B) Neighbor-joining tree of mtDNA haplotypes for D. suzukii and relatives. Wolbachia-infected individuals denoted (+).

Fig. 3

Wolbachia transmission by wild-caught D. suzukii females.

Fig. 4

Scatterplot of the number of male and female offspring produced by Wolbachia-infected (+) and uninfected (–) females (mated to uninfected and infected males, respectively) of D. suzukii and D. subpulchrella. The line denotes 1:1 offspring sex ratios. Female offspring did not occur at a higher rate than males in infected D. suzukii + (binomial test p = 0.5, P = 0.37; N = 179) or D. subpulchrella + (P = 0.47; N = 507), indicating no male killing (or feminization).