Paleocene origin of a streamlined digestive symbiosis in leaf beetles

Timing the acquisition of a beneficial microbe relative to the evolutionary history of its host can shed light on the adaptive impact of a partnership. Here, we investigated the origin and ecological consequences of an obligate symbiosis between Cassidinae leaf beetles and Candidatus Stammera capleta, a gammaproteobacterium. Residing extracellularly within foregut symbiotic organs, Stammera upgrades the digestive physiology of its host by supplementing plant cell wall-degrading enzymes. We observe that Stammera is a shared symbiont across tortoise and hispine beetles that collectively comprise the Cassidinae subfamily, despite differences in their folivorous habits. Transcriptional profiling revealed that Stammera modulates transcription during the life cycle of Chelymorpha alternans, elevating the expression of genes encoding digestive enzymes at both larval and adult stage, matching the nutritional requirements of its host. Despite a widespread distribution across the Cassidinae, the acquisition of Stammera 62 Mya did not coincide with the Paleocene origin of the subfamily. Early-diverging lineages lack both the symbiont and the specialized organs that house it. The acquisition of Stammera provided non-symbiotic Cassidines with four digestive enzymes, including polygalacturonase, a pectinase that is universally shared. While non-symbiotic cassidines encode polygalacturonase endogenously, their repertoire of plant cell wall-degrading enzymes is more limited compared to symbiotic beetles supplemented with digestive enzymes from Stammera. Highlighting the impact of a symbiotic condition and an upgraded metabolic potential, Stammera-harboring beetles exploit a greater variety of plants and are more speciose compared to non-symbiotic members of the Cassidinae.