Ecological and Evolutionary Consequences of Symbiont Acquisition, Maintenance, and Loss in Herbivorous Beetles

Abstract

Herbivorous insects often rely on microbial symbionts to overcome the nutritional and chemical barriers of plant-based diets yet the genomic, developmental, and ecological consequences of acquiring, maintaining or losing such partners remain poorly understood. Building on foundational work that established Cassidinae beetles maintain a specialized extracellular symbiosis with Candidatus Stammera capleta to digest plant cell walls, this thesis investigates: (1) How did this nutritional partnership evolve and diversify within Cassidinae? (2) What molecular, morphological, and regulatory mechanisms underlie its maintenance and vertical transmission? (3) What are the ecological and genomic consequences for hosts following symbiont acquisition and loss? Phylogenomic analyses revealed that Stammera is widespread across the Cassidinae but absent from early-diverging lineages, and that its acquisition during the Paleocene (~62 mya) coincided with an increased diversification in Cassidinae and an expanded host plant range. Ancestral state reconstruction across 50 symbiont genomes showed that, at the onset of the association, Stammera encoded three plant cell wall-degrading enzymes, supplementing the limited endogenous repertoires of non-symbiotic beetles. Transcriptomic analyses across host developmental stages indicated that the symbiont elevates the expression of genes encoding digestive enzymes in the foregut symbiotic organs of larvae and adults, matching host nutritional requirements. The symbiont’s unique extracellular localization is supported by specialized transmission mechanisms, including protective matrices formed by a co-opted, female specific Yellow protein and a newly described symbiotic organ. Yellow is expressed in ovary-associated glands, assembled into a proteinaceous matrix, and secreted with the symbiont during oviposition. Functional knockdown disrupts sphere integrity and reduces symbiont viability under low humidity conditions, demonstrating its protective role. Comparative analyses of host genomes across a gradient of symbiotic conditions showed that Stammera acquisition was accompanied by expansions in host gene families related to informational processes and carbohydrate metabolism. Furthermore, symbiont maintenance involves a precise immune modulation in foregut symbiotic organs that permits persistence without compromising defense and host compensation through upregulation of glycolytic genes absent from the symbiont genome. In species that have secondarily lost Stammera, genomic signatures of adaptation include expansion or retention of endogenous plant cell wall-degrading enzymes. Experimental symbiont removal further revealed that symbiont loss disrupts metabolic gene expression and causes nutrient deficits beyond carbohydrate availability. Collectively, this work establishes the Cassidinae-Stammera system as a tractable model for studying extracellular nutritional symbioses, providing new genomic resources and functional tools and offering a framework for understanding how obligate symbioses originate, persist, and shape the diversification, physiology, and ecological success of herbivorous insects.

Die Dissertation ist gesperrt bis zum 31. Mai 2027 !