ABSTRACTFor insects that depend on one or more bacterial endosymbionts for survival, it is critical that these bacteria are faithfully transmitted between insect generations. Cicadas harbor two essential bacterial endosymbionts, “CandidatusSulcia muelleri” and “CandidatusHodgkinia cicadicola.” In some cicada species,Hodgkiniahas fragmented into multiple distinct but interdependent cellular and genomic lineages that can differ in abundance by more than two orders of magnitude. This complexity presents a potential problem for the host cicada, because low-abundance but essentialHodgkinialineages risk being lost during the symbiont transmission bottleneck from mother to egg. Here we show that all cicada eggs seem to receive the full complement ofHodgkinialineages, and that in cicadas with more complexHodgkiniathis outcome is achieved by increasing the number ofHodgkiniacells transmitted by up to 6-fold. We further show that cicada species with varyingHodgkiniacomplexity do not visibly alter their transmission mechanism at the resolution of cell biological structures. Together these data suggest that a major cicada adaptation to changes in endosymbiont complexity is an increase in the number ofHodgkiniacells transmitted to each egg. We hypothesize that the requirement to increase the symbiont titer is one of the costs associated withHodgkiniafragmentation.IMPORTANCESap-feeding insects critically rely on one or more bacteria or fungi to provide essential nutrients that are not available at sufficient levels in their diets. These microbes are passed between insect generations when the mother places a small packet of microbes into each of her eggs before it is laid. We have previously described an unusual lineage fragmentation process in a nutritional endosymbiotic bacterium of cicadas calledHodgkinia. In some cicadas, a singleHodgkinialineage has split into numerous related lineages, each performing a subset of original function and therefore each required for normal host function. Here we test how this splitting process affects symbiont transmission to eggs. We find that cicadas dramatically increase the titer ofHodgkiniacells passed to each egg in response to lineage fragmentation, and we hypothesize that this increase in bacterial cell count is one of the major costs associated with endosymbiont fragmentation.
Changes in Endosymbiont Complexity Drive Host-Level Compensatory Adaptations in Cicadas
