Paleocene origin of a streamlined digestive symbiosis in leaf beetles

Abstract

AbstractTiming 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 onset and molecular evolution of an obligate symbiosis between Cassidinae leaf beetles andCandidatusStammera capleta, a γ-proteobacterium. Residing extracellularly within foregut symbiotic organs,Stammeraupgrades the digestive physiology of its host by supplementing plant cell wall-degrading enzymes. We observe thatStammerais a shared symbiont across tortoise and hispine beetles that collectively comprise the Cassidinae subfamily, despite differences in their folivorous habits. In contrast to its transcriptional profile during vertical transmission,Stammeraelevates the expression of genes encoding digestive enzymes while in the foregut symbiotic organs, matching the nutritional requirements of its host. Symbiont acquisition during the Paleocene (∼62 Mya) did not coincide with the origin of Cassidinae beetles, despite the widespread distribution ofStammeraacross the subfamily. Early-diverging lineages lack the symbiont and the specialized organs that house it. Reconstructing the ancestral state of host-beneficial factors revealed thatStammeraencoded three digestive enzymes at the onset of symbiosis, 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 fromStammera. Highlighting the potential 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.