Genotypic Variation and the Role of Defensive Endosymbionts in an All-Parthenogenetic Host-Parasitoid Interaction

Abstract

Models of host-parasite coevolution predict pronounced genetic dynamics if resistance and infectivity are genotype-specific or associated with costs, and if selection is fueled by sufficient genetic variation. We addressed these assumptions in the black bean aphid, Aphis fabae, and its parasitoid Lysiphlebus fabarum. Parasitoid genotypes differed in infectivity and host clones exhibited huge variation for susceptibility. This variation occurred at two levels. Clones harboring Hamiltonella defensa, a bacterial endosymbiont known to protect pea aphids against parasitoids, enjoyed greatly reduced susceptibility, yet clones without H. defensa also exhibited significant variation. Although there was no evidence for genotype-specificity in the H. defensa-free clones' interaction with parasitoids, we found such evidence in clones containing the bacterium. This suggests that parasitoid genotypes differ in their ability to overcome H. defensa, resulting in an apparent host × parasitoid genotype interaction that may in fact be due to an underlying symbiont × parasitoid genotype interaction. Aphid susceptibility to parasitoids correlated negatively with fecundity and rate of increase, due to H. defensa-bearing clones being more fecund on average. Hence, possessing symbionts may also be favorable in the absence of parasitoids, which raises the question why H. defensa does not go to fixation and highlights the need to develop new models to understand the dynamics of endosymbiont-mediated coevolution.

Evidence for specificity in symbiont-conferred protection against parasitoids

“…However, the situation in the field may be more complex. Our experiments were carried out using only single inbred lines of parasitoids and so we could not explore genotypeby-genotype specificity between symbionts and parasitoids in the effectiveness of protection, something that has previously been observed in interactions between A. fabae and L. fabarum [23,58]. It is possible that similar genotypic variation could exist within the parasitoid species attacking A. pisum.…”

“…The fullgrown parasitoid larva pupates inside the mummified husk of its host. The symbiont Hamiltonella defensa (Gammaproteobacteria: Enterobacteriaceae) has been shown to protect aphids against a number of parasitoids within the subfamily Aphidiinae (Hymenoptera: Braconidae) [11,12,22,23], although the extent of this protection varies considerably among bacterial isolates [11]. In aphids infected with a protective symbiont, the parasitoid dies during the egg or larval stage.…”

Parasitic wasp responses to symbiont-based defense in aphids

“…This report provides evidence that natural enemies are sometimes able to counteract symbiont-based defense. Recent reports have documented: 1) the evolution of increased A. ervi virulence when faced with symbiont-carrying resistant A. pisum lines [44] and 2) genotypic variation in the parasitoid Lysiphlebus fabarum 's ability to successfully parasitize H. defensa -infected Aphis fabae (black bean aphid) [16]. The experimental design of these studies, however, does not allow conclusive partitioning of increased virulence towards symbiont- versus host-based defensive factors, but these reports do indicate that parasitic wasps likely have additional mechanisms for overcoming symbiont-based resistance.…”

Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps

“…Several bacterial symbionts of aphids confer protection against parasitoid wasps (Oliver et al, 2003(Oliver et al, , 2005Vorburger et al, 2009) and fungi (Scarborough et al, 2005;Lukasik et al, 2012). Spiroplasma bacteria confer protection against fungi in the pea aphid (Lukasik et al, 2012), against a nematode in Drosophila neotestacea (Jaenike et al, 2010b) and against a parasitoid wasp in Drosophila hydei .…”