Here we show that a bacterial endosymbiont, Regiella insecticola, protects pea aphids (Acyrthosiphon pisum) from the aphidspecific fungal entomopathogen Zoophthora occidentalis but not from the generalist insect fungal pathogen Beauveria bassiana. This finding highlights the complex influence of fungi on the dynamics of this economically important agricultural pest.
Symbiotic relationships between invertebrates and vertically transmitted microbes are widespread. One feature of this mutualistic relationship is that symbionts depend on host resources for their own survival and reproduction (1), and theory therefore predicts that in the absence of manipulation of host reproduction, beneficial symbionts must provide a fitness advantage to spread through a host population (2). Studying ecologically relevant traits conferred to hosts by symbionts is critical for understanding host-microbe dynamics, and researchers have therefore searched for fitness advantages of harboring symbionts in a number of systems. Several recent studies have shown that one advantage conferred by some symbionts is protection against pathogens and parasites (3-7). For example, pea aphids (Acyrthosiphon pisum), which are a model system for the study of host-symbiont dynamics, are protected against the fungal entomopathogen Pandora neoaphidis (Zygomycota: Entomophthorales) by several facultative, vertically transmitted bacteria, including the gammaproteobacteria Regiella insecticola (8, 9). Fungi are important natural pathogens of aphids (10) and are used in biocontrol (11, 12), and symbiont-mediated protection to fungi is likely an important factor influencing the population dynamics of aphids and their symbionts. However, aphids encounter several diverse species of fungal pathogens in the wild (13). It is not known if Regiella-conferred protection is specific to Pandora or if it extends to other species of fungus as well, which would suggest that multiple fungal species are influencing aphid-Regiella dynamics. We therefore exposed pea aphids, with and without symbionts, to two additional species of fungal pathogens: Zoophthora occidentalis (Zygomycota: Entomophthorales), a highly aphid-specific entomopathogen, and Beauveria bassiana (Ascomycota: Hypocreales), a generalist that has been found in a variety of hosts, including species of Coleoptera, Hemiptera, and Diptera (13-15). These fungal species are highly divergent (with some estimates as high as 1,000 million years ago [16]), but both species reproduce by passively releasing spores (conidia) that penetrate the cuticle of a suitable host. Mycelia then colonize the host's body tissue until the death of the host, when new spores are produced and released into the environment.We used two aphid genotypes, both with and without Regiella present (5A, collected in the wild in 1999 near Madison, WI, and subsequently injected with Regiella symbionts from an aphid collected in Tompkins County, NY, in 2000; and LSR1, collected on alfalfa near Ithaca, NY, in 1998 with a natural Regiella infection and t...