The leaf beetle Chelymorpha alternans propagates a plant pathogen in exchange for pupal protection.

Many insects rely on microbial protection in the early stages of their development. However, in contrast to symbiont-mediated defense of eggs and young instars, the role of microbes in safeguarding pupae remains relatively unexplored, despite the susceptibility of the immobile stage to antagonistic challenges. Here, we outline the importance of symbiosis in ensuring pupal protection by describing a mutualistic partnership between the ascomycete Fusarium oxysporum and Chelymorpha alternans, a leaf beetle. The symbiont rapidly proliferates at the onset of pupation, extensively and conspicuously coating C. alternans during metamorphosis. The fungus confers defense against predation as symbiont elimination results in reduced pupal survivorship. In exchange, eclosing beetles vector F. oxysporum to their host plants, resulting in a systemic infection. By causing wilt disease, the fungus retained its phytopathogenic capacity in light of its symbiosis with C. alternans. Despite possessing a relatively reduced genome, F. oxysporum encodes metabolic pathways that reflect its dual lifestyle as a plant pathogen and a defensive insect symbiont. These include virulence factors underlying plant colonization, along with mycotoxins that may contribute to the defensive biochemistry of the insect host. Collectively, our findings shed light on a mutualism predicated on pupal protection of an herbivorous beetle in exchange for symbiont dissemination and propagation.

For the road: calibrated maternal investment in light of extracellular symbiont transmission.

Faithful transmission of beneficial symbionts is critical for the persistence of mutualisms. Many insect groups rely on extracellular routes that require microbial symbionts to survive outside the host during transfer. However, given a prolonged aposymbiotic phase in offspring, how do mothers mitigate the risk of symbiont loss due to unsuccessful transmission? Here, we investigated symbiont regulation and reacquisition during extracellular transfer in the tortoise beetle, Chelymorpha alternans (Coleoptera: Cassidinae). Like many cassidines, C. alternans relies on egg caplets to vertically propagate its obligate symbiont Candidatus Stammera capleta. On average, each caplet is supplied with 12 symbiont-bearing spheres where Stammera is embedded. We observe limited deviation (±2.3) in the number of spheres allocated to each caplet, indicating strict maternal control over symbiont supply. Larvae acquire Stammera 1 day prior to eclosion but are unable to do so after hatching, suggesting that a specific developmental window governs symbiont uptake. Experimentally manipulating the number of spheres available to each egg revealed that a single sphere is sufficient to ensure successful colonization by Stammera relative to the 12 typically packaged within a caplet. Collectively, our findings shed light on a tightly regulated symbiont transmission cycle optimized to ensure extracellular transfer.