Independent origins of resistance or susceptibility of parasitic wasps to a defensive symbiont

Abstract

Insect microbe associations are diverse, widespread, and influential. Among the fitness effects of microbes on their hosts, defense against natural enemies is increasingly recognized as ubiquitous, particularly among those associations involving heritable, yet facultative, bacteria. Protective mutualisms generate complex ecological and coevolutionary dynamics that are only beginning to be elucidated. These depend in part on the degree to which symbiont-mediated protection exhibits specificity to one or more members of the natural enemy community. Recent findings in a well-studied defensive mutualism system (i.e., aphids, bacteria, parasitoid wasps) reveal repeated instances of evolution of susceptibility or resistance to defensive bacteria by parasitoids. This study searched for similar patterns in an emerging model system for defensive mutualisms: the interaction of Drosophila, bacteria in the genus Spiroplasma, and wasps that parasitize larval stages of Drosophila. Previous work indicated that three divergent species of parasitic wasps are strongly inhibited by the presence of Spiroplasma in three divergent species of Drosophila, including D. melanogaster. The results of this study uncovered two additional wasp species that are susceptible to Spiroplasma and two that are unaffected by Spiroplasma, implying at least two instances of loss or gain of susceptibility to Spiroplasma among larval parasitoids of Drosophila.

Keywords: Braconidae; Drosophila melanogaster; Figitidae; Mollicutes; defensive mutualism; heritable endosymbiont.

Figure 1

Females of two figitid wasps examined. Top Leptopilina victoriae (strain LvHaw). Bottom: Leptopilina guineaensis (strain LgG500 or LgCAM). Photographs by Matthew Buffington.

Figure 2

Fitness effects of Spiroplasma MSRO in the presence and absence of five wasp species representing three genera from two families. Mean ± Standard Error for four survival/mortality measures. Open bars = Spiroplasma‐free (S ⁻) treatments; Gray bars = Spiroplasma‐infected (S ⁺) treatments. The cladogram above indicates phylogenetic relationships (based on Kacsoh and Schlenke 2012). P‐values for significant (P < 0.05) or borderline nonsignificant effects of Spiroplasma infection are shown. Dashed horizontal lines = 50 and 100% Y‐axis values.

Figure 3

Susceptibility/resistance to Spiroplasma by eight species of parasitoids that attack Drosophila. The degree of fly rescue by Spiroplasma is also indicated. The phylogenetic relationships of the parasitoids are based on Kacsoh and Schlenke (2012).