Complex symbiont acquisition behaviors maintain a horizontally transmitted insect-microbial mutualism

Understanding how horizontally transmitted mutualisms are maintained is a major focus of symbiosis research. Unlike vertical transmission, hosts that rely on horizonal transmission produce symbiont-free offspring that must find and acquire their beneficial microbes from the environment. This strategy is inherently risky and can be vulnerable to transmission mistakes every generation. However, despite these potential costs, horizontal transmission underlies stable, host-specific mutualisms in a large diversity of both plants and animals. One potential way horizontal transmission is maintained is through sophisticated mechanisms that allow hosts to consistently find and acquire symbionts from the environment. Here we examine the symbiont-seeking ability of Anasa tristis, a widespread agricultural pest that require bacterial symbionts in the genus Caballeronia for survival and development. We conduct a series of behavioral and transmission experiments that track strain-level transmission in vivo among individuals in real-time. Using choice tests, we demonstrate that nymphs display significant taxis toward the options containing symbionts. Once nymphs locate the symbionts, they deploy feeding behavior that results in nearly perfect symbiont acquisition success. We further demonstrate that symbiont acquisition results in altered feeding behavior and is mediated, in part, by chemoreceptors in the antennae. Finally, we show this new acquisition behavior is highly host specific. Taken together, our data describe not only the evolution of a reliable horizontal transmission strategy, but also a potential mechanism that drives patterns of species-specific microbial communities among closely related, sympatric host species. Our study demonstrates a tractable approach to understand how horizontally transmitted mutualisms are maintained.