Life cycle and population dynamics of a protective insect symbiont reveal severe bottlenecks during vertical transmission

Abstract

Insects engage in mutualistic relationships with a wide variety of microorganisms that are usually transmitted vertically to the next generation. During transmission, the symbiont populations often suffer significant bottlenecks that may entail major genetic and genomic consequences. Here we investigated the life-cycle and the severity of transmission bottlenecks in a symbiotic system with an unusual way of post-hatch vertical transmission by using quantitative PCRs and morphological 3D-reconstructions. European beewolves (Philanthus triangulum, Hymenoptera: Crabronidae) harbor symbiotic bacteria (‘Candidatus Streptomyces philanthi’) in specialized antennal gland reservoirs and secrete them into their subterranean brood cells. The symbionts are later taken up by the beewolf larva and incorporated into the cocoon material to provide protection against pathogenic microorganisms. Even after months of hibernation, the symbiont population on the cocoon is estimated to encompass around 1.4 × 105 cells. However, our results indicate that only few of these bacterial cells (about 9.7 × 102) are taken up from the cocoon by the emerging female. The symbiont population subsequently undergoes logistic growth within the antennal gland reservoirs and reaches a maximum of about 1.5 × 107 cells 3–4 days after emergence. The maximum specific growth rate is estimated to be 0.084–0.105 h−1. With a total reduction in cell numbers of about 6.7 × 10−5 during vertical transmission, the symbiont population experiences one of the most severe bottlenecks known for any symbiotic system to date. This extreme bottleneck may have significantly affected the evolution of the beewolf-Streptomyces symbiosis by increased genetic drift, an accumulation of mildly deleterious mutations and genome erosion.