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Abstract:
Symbiont specificity is predicted to stabilize obligate insect-microbe symbioses. Despite the prevalence of nutritional and defensive symbioses in insects, mechanistic insights into the specificity of these interactions are often hampered by the limited ability to disrupt and experimentally exchange symbionts across different host species. Here, we leverage the tractability afforded by an extracellular symbiont transmission route in tortoise leaf beetles (Coleoptera: Cassidinae) to quantify the specificity governing their obligate symbiosis with Candidatus Stammera capleta. Cassidines derive pectin-degrading enzymes from Stammera, allowing them to exploit a leafy diet rich in recalcitrant polysaccharides. Stammera is localized in specialized organs connected to the foregut and extracellularly transmitted from mother to progeny via egg caplets. Caplet removal disrupts symbiont transmission, enabling downstream manipulation and exchange of Stammera across different host lineages. We conducted experimental transfections in aposymbiotic eggs of the tortoise beetle, Chelymorpha alternans, using Stammera derived from three additional Cassidinae species. Symbiont transfection was successful across all treatments, highlighting that Stammera can be exchanged across host lineages. However, we observe differences in the efficacy of symbiont colonization depending on the genetic distance of nonnative Stammera strains relative to the native symbiont. Reflecting this, the fitness of aposymbiotic larvae is restored following symbiont transfection of Stammera, but only in treatments bearing strains that are closely related to the native symbiont. The positive correlation between symbiont genetic distance and host survivorship highlights the strong influence of symbiont genotype on host development. Overall, our findings confirm that the high degree of host-symbiont specificity plays a significant role in obligate symbiont maintenance over long evolutionary timescales.
