Symbiont-mediated feminization imposes unavoidable host fitness costs

Maternally inherited bacterial endosymbionts such as Wolbachia are common in arthropods. Some serve as reproductive manipulators, favoring the production of infected females in host populations despite possible fitness costs to the host. One such manipulation is feminization, in which the symbiont turns genetic males into functional females. To date, all described cases of feminization occur in host systems that are either female heterogametic (ZW-female/ZZ-male) or where females are diploid and males are haploid for sex chromosomes (XX-female/X0-male). Here we test potential fitness costs associated with feminization in the spider Mermessus fradeorum (Linyphiidae), which has a type of XX/X0 sex determination. In addition to a feminizing Wolbachia, this spider can be co-infected with up to four additional maternally-inherited bacterial endosymbionts. Using a series of increasingly speciose symbiont co-infections, including three containing the feminizing Wolbachia, we measured female fecundity and the proportion of developed versus undeveloped offspring. We found that fitness costs were associated only with the feminizing Wolbachia, but not with any of the other symbionts. Eggmasses infected with this Wolbachia had 16% fewer eggs, and 20% of those eggs failed to develop, compared to only 4% failure in eggmasses from other symbiotypes. We hypothesize that the reduced egg viability results from the production of inviable 00 zygotes by feminized X0 individuals, which can provision X chromosomes to only half of their eggs. These results suggest that fitness costs may be an unavoidable consequence of feminization in hosts with an XX/X0 sex determination system, potentially limiting the distribution of this reproductive manipulation phenotype.