Parasitoids as drivers of symbiont diversity in an insect host

Abstract

Immune systems have repeatedly diversified in response to parasite diversity. Many animals have outsourced part of their immune defence to defensive symbionts, which should be affected by similar evolutionary pressures as the host's own immune system.Protective symbionts provide efficient and specific protection and respond to changing selection pressure by parasites. Here, we use the aphid Aphis fabae, its protective symbiont Hamiltonella defensa, and its parasitoid Lysiphlebus fabarum to test whether parasite diversity can maintain diversity in protective symbionts. We exposed aphid populations with the same initial symbiont composition to parasitoid populations that differed in their diversity. As expected, single parasitoid genotypes mostly favoured a single symbiont that was most protective against that particular parasitoid, while multiple symbionts persisted in aphids exposed to more diverse parasitoid populations, which in turn affected aphid population density and rates of parasitism. Parasite diversity may be crucial to maintaining symbiont diversity in nature.

A Link Between Communities of Protective Endosymbionts and Parasitoids of the Pea Aphid Revealed in Unmanipulated Agricultural Systems

“…Additionally, the aforementioned studies highlighted the influence of protective endosymbionts on diversity and structure of parasitoid communities, with potential consequences on food web functioning (Mclean et al, 2016;Mclean, 2019). More recently, in an elegant experimental evolution study (Hafer-Hahmann and Vorburger, 2020), it was discovered that symbiont diversity could be driven by parasitoid diversity, suggesting potential reciprocal influence of these two communities through their shared aphid hosts.…”

Positive association between the diversity of symbionts and parasitoids of aphids in field populations

“…Even though the association was very noisy, it is in line with the hypothesis that protective symbionts and parasites may drive each other’s diversity (reviewed by Hafer and Vorburger 2019). This hypothesis is supported by experimental evidence showing that a more diverse population of parasitoids will maintain a higher diversity of symbiont strains in aphids (Hafer‐Hahmann and Vorburger 2020, Rossbacher and Vorburger 2020). Our findings complement these experiments and indicate that the processes found to shape the interaction of symbionts and parasites under more artificial conditions may indeed play a role in shaping natural communities.…”

“…In turn, parasitoids are well known to drive the frequency of protective symbionts (e.g., K€ ach et al 2018, Ives et al 2020, Rossbacher and Vorburger 2020. In a recent laboratory experiment exposing aphid populations containing multiple strains of H. defensa to different combinations of asexual lines of the parasitoid wasp Lysiphlebus fabarum, we could show that parasitoid diversity can be crucial in maintaining symbiont diversity (Hafer-Hahmann and Vorburger 2020).…”

“…Unlike a simple correlation, these models imply a direction, that is, we tested for an effect of parasitoid diversity on symbiont diversity. We chose this direction since we could show previously that under laboratory conditions, parasitoid diversity can indeed affect symbiont diversity (Hafer‐Hahmann and Vorburger 2020). However, we are aware that due to the correlative nature of our findings, we cannot rule out that any significant effect of parasitoid diversity we observe may rather be an effect of symbiont diversity on parasitoid diversity or be caused by different factors jointly influencing both symbiont and parasitoid diversity.…”

“…In a recent laboratory experiment exposing aphid populations containing multiple strains of H . defensa to different combinations of asexual lines of the parasitoid wasp Lysiphlebus fabarum , we could show that parasitoid diversity can be crucial in maintaining symbiont diversity (Hafer‐Hahmann and Vorburger 2020).…”