Sexual acquisition of beneficial symbionts in aphids

Abstract

A noted cost of mating is the risk of acquiring sexually transmitted infections that are detrimental to the recipient. But many microbial associates of eukaryotes are mutualistic, raising the possibility that sexual contact provides the opportunity to acquire symbionts that are beneficial. In aphids, facultative bacterial symbionts, which benefit hosts by conferring resistance to natural enemies or to heat, are transmitted maternally with high fidelity and are maintained stably throughout hundreds of parthenogenetic generations in the laboratory. Data from field populations indicate that horizontal transfer of these facultative symbionts is frequent, and transfections are readily achieved by microinjection or ingestion in artificial diet. However, no natural mechanism for the horizontal transfer of these symbionts has been identified. Here we demonstrate that during sexual reproduction, male-borne symbionts can be acquired by females and subsequently transferred to sexually and parthenogenetically produced progeny, establishing stable, maternally transmitted associations. In our experiments, sexually transmitted symbionts resulted in (i) infection of previously uninfected matrilines, (ii) a double infection in a matriline already bearing a different symbiont, and (iii) replacement of the maternal symbiont. We also observed some cases in which maternal symbionts failed to become established in sexually produced progeny. Microscopy indicated that symbionts were abundant in the male reproductive system, which demonstrates a natural route of nonmaternal transfer of insect symbionts. Because such transfer can generate coinfections, thereby creating opportunities for symbiont competition and recombination, paternal inheritance has major consequences for expectations regarding symbiont evolution.Acyrthosiphon pisum ͉ mutualism ͉ symbiosis

A novel intracellular mutualistic bacterium in the invasive antCardiocondyla obscurior

“…However, Wolbachia, also present in C. obscurior, could exert effects on host reproduction as well. In contrast to some other intracellular symbionts (Moran and Dunbar, 2006;Damiani et al, 2008;Watanabe et al, 2014), paternal transmission of Westeberhardia is unlikely as we did not detect Westeberhardia DNA in transferred sperm and/or seminal fluids stored in the spermatheca of uninfected queens mated to infected males.…”

Population dynamics of defensive symbionts in aphids

“…Hamiltonella has been detected in A. pisum honeydew, and in laboratory assays A. pisum can become infected with Hamiltonella after feeding on artificial diets containing these bacteria (Darby & Douglas 2003). Moran & Dunbar (2006) recently demonstrated that paternal SS infections are readily transferred to uninfected sexual females and that some of these are stably inherited in the descendant lines of parthenogenetic females. On the other hand, maternal infections are occasionally lost during the sexual egg stage a Denotes that the particular cage fixed at 100 or 0% at end of experiment (12 weeks).…”

“…LogitZln( y/1Ky); yZproportion infected. (Moran & Dunbar 2006). Thus, whether the sexual phase of the life cycle results in a net increase or decrease in infection frequency in nature is unknown.…”

Phage loss and the breakdown of a defensive symbiosis in aphids

“…On the basis of a conservative average of 30 generations per year, we calculated the number of generations with successful vertical transmission [30]. We estimated 1470 generations of successful transfer in APSE-3 infected lines and 540 generations in APSE-free H. defensa-infected lines.…”