The effects of outbreeding on a parasitoid wasp fixed for infection with a parthenogenesis-inducing Wolbachia symbiont

Abstract

Trichogramma wasps can be rendered asexual by infection with the maternally inherited symbiont Wolbachia. Previous studies indicate the Wolbachia strains infecting Trichogramma wasps are host-specific, inferred by failed horizontal transfer of Wolbachia to novel Trichogramma hosts. Additionally, Trichogramma can become dependent upon their Wolbachia infection for the production of female offspring, leaving them irreversibly asexual, further linking host and symbiont. We hypothesized Wolbachia strains infecting irreversibly asexual, resistant to horizontal transfer Trichogramma would show adaptation to a particular host genetic background. To test this, we mated Wolbachia-dependent females with males from a Wolbachia-naïve population to create heterozygous wasps. We measured sex ratios and fecundity, a proxy for Wolbachia fitness, produced by heterozygous wasps, and by their recombinant offspring. We find a heterozygote advantage, resulting in higher fitness for Wolbachia, as wasps will produce more offspring without any reduction in the proportion of females. While recombinant wasps did not differ in total fecundity after 10 days, recombinants produced fewer offspring early on, leading to an increased female-biased sex ratio for the whole brood. Despite the previously identified barriers to horizontal transfer of Wolbachia to and from Trichogramma pretiosum, there were no apparent barriers for Wolbachia to induce parthenogenesis in these non-native backgrounds. This is likely due to the route of infection being introgression rather than horizontal transfer, and possibly the co-evolution of Wolbachia with the mitochondria rather than the nuclear genome. These results help to elucidate the mechanisms by which Wolbachia adapt to hosts and the evolution of host-symbiont phenotypes.

Distinct epigenomic and transcriptomic modifications associated with Wolbachia-mediated asexuality

“…These lines are not infected with Wolbachia: virgin females produce only male offspring. Species identification and Wolbachia infection status were confirmed using molecular methods, as described previously [28,[71][72][73].…”

“…We introgressed the sexual CA9 nuclear genome into the asexual ES865 cytoplasm, and the sexual CA29 nuclear genome into the asexual Insectary cytoplasm (Fig 1A). These pairs were chosen based on the ability to differentiate them at the A9 microsatellite locus, a size-diagnostic amplicon routinely used for identifying unique isofemale lines of this wasp [71]. For example, the Insectary line has an A9 microsatellite of 312 bp in length, and the CA29 line has an PLOS PATHOGENS A9 microsatellite of 220 bp in length-allowing us verify fertilization during introgression: a critical step because Wolbachia induces diploidization of unfertilized eggs, and thus female offspring are produced from both fertilized and unfertilized eggs [16].…”

“…After 24 hours of reproduction as virgins, wasps were mated to virgin males from the appropriate "nuclear-genome-donating line" (either CA9 or CA29), and then allowed to parasitize a separate egg card for the next 24 hours. After these two reproductive periods, the mated females were removed from their egg card, and used for DNA extraction and A9 microsatellite PCR assays, as described previously [71]. At each step of the introgression, we identified mothers who were heterozygous (indicating she was produced via fertilization), and then isolated virgin females originating from her "mated" egg card.…”

Peer Review #3 of "Host and symbiont genetic contributions to fitness in a Trichogramma–Wolbachia symbiosis (v0.1)"

“…Manuscript to be reviewed Alternatively, Wolbachia-mitochondria interactions may play a role in the observed fitness deductions observed for the horizontally transferred lines. Recent results with Trichogramma pretiosum showed that nuclear introgression of novel genetic background appeared to have no negative fecundity fitness effects (Lindsey & Stouthamer 2017b). However, horizontal transfer of Wolbachia was not possible with T. pretiosum, unlike here where Wolbachia were experimentally transferred to novel host nuclear and mitochondrial backgrounds.…”

Host and symbiont genetic contributions to fitness in aTrichogramma–Wolbachiasymbiosis

“…Alternatively, Wolbachia– mitochondria interactions may play a role in the observed fitness deductions observed for the horizontally transferred lines. Recent results with T. pretiosum showed that nuclear introgression of novel genetic background appeared to have no negative fecundity fitness effects ( Lindsey & Stouthamer, 2017b ). However, horizontal transfer of Wolbachia was not possible with T. pretiosum , unlike here where Wolbachia were experimentally transferred to novel host nuclear and mitochondrial backgrounds.…”