title: Evolutionary transition in symbiotic syndromes enabled diversification of phytophagous insects on an imbalanced diet.
abstract: Evolutionary adaptations for the exploitation of nutritionally challenging or toxic host plants represent a major force driving the diversification of phytophagous insects. Although symbiotic bacteria are known to have essential nutritional roles for insects, examples of radiations into novel ecological niches following the acquisition of specific symbionts remain scarce. Here we characterized the microbiota across bugs of the family Pyrrhocoridae and investigated whether the acquisition of vitamin-supplementing symbionts enabled the hosts to diversify into the nutritionally imbalanced and chemically well-defended seeds of Malvales plants as a food source. Our results indicate that vitamin-provisioning Actinobacteria (Coriobacterium and Gordonibacter), as well as Firmicutes (Clostridium) and Proteobacteria (Klebsiella) are widespread across Pyrrhocoridae, but absent from the sister family Largidae and other outgroup taxa. Despite the consistent association with a specific microbiota, the Pyrrhocoridae phylogeny is neither congruent with a dendrogram based on the hosts' microbial community profiles nor phylogenies of individual symbiont strains, indicating frequent horizontal exchange of symbiotic partners. Phylogenetic dating analyses based on the fossil record reveal an origin of the Pyrrhocoridae core microbiota in the late Cretaceous (81.2-86.5 million years ago), following the transition from crypt-associated beta-proteobacterial symbionts to an anaerobic community localized in the M3 region of the midgut. The change in symbiotic syndromes (that is, symbiont identity and localization) and the acquisition of the pyrrhocorid core microbiota followed the evolution of their preferred host plants (Malvales), suggesting that the symbionts facilitated their hosts' adaptation to this imbalanced nutritional resource and enabled the subsequent diversification in a competition-poor ecological niche.
authors.affiliation: Insect Symbiosis Research Group, Max Planck Institute for Chemical Ecology, Jena, Germany.
authors.forename: Sailendharan
authors.initials: S
authors.lastname: Sudakaran
authors.affiliation: Insect Symbiosis Research Group, Max Planck Institute for Chemical Ecology, Jena, Germany.
authors.forename: Franziska
authors.initials: F
authors.lastname: Retz
authors.affiliation: Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST) Hokkaido, Sapporo, Japan.
authors.forename: Yoshitomo
authors.initials: Y
authors.lastname: Kikuchi
authors.affiliation: Experimental Ecology and Evolution Research Group, Max Planck Institute for Chemical Ecology, Jena, Germany.|Institute of Microbiology, Friedrich Schiller University, Jena, Germany.
authors.forename: Christian
authors.initials: C
authors.lastname: Kost
authors.affiliation: Insect Symbiosis Research Group, Max Planck Institute for Chemical Ecology, Jena, Germany.
authors.forename: Martin
authors.initials: M
authors.lastname: Kaltenpoth
mesh_terms: D039903:Actinobacteria / Q000235:genetics / Q000302:isolation & purification / Q000502:physiology*; D000818:Animals; D005075:Biological Evolution; D005247:Feeding Behavior; D020062:Heteroptera / Q000145:classification / Q000235:genetics / Q000382:microbiology* / Q000502:physiology*; D010802:Phylogeny; D013559:Symbiosis