Covariation and phenotypic integration in chemical communication displays : biosynthetic constraints and eco-evolutionary implications

Junker, Robert R.; Kuppler, Jonas; Amo, Luisa; Blande, James D.; Borges, Renee M.; Dam, Nicole M. van; Dicke, Marcel; Dötterl, Stefan; Ehlers, Bodil K.; Etl, Florian; Gershenzon, Jonathan; Glinwood, Robert; Gols, Rieta; Groot, Astrid T.; Heil, Martin; Hoffmeister, Mathias; Holopainen, Jarmo K.; Jarau, Stefan; John, Lena; Kessler, Andre; Knudsen, Jette T.; Kost, Christian; Larue-Kontic, Anne Amélie C.; Leonhardt, Sara Diana; Lucas-Barbosa, Dani; Majetic, Cassie J.; Menzel, Florian; Parachnowitsch, Amy L.; Pasquet, Rémy S.; Poelman, Erik H.; Raguso, Robert A.; Ruther, Joachim; Schiestl, Florian P.; Schmitt, Thomas; Tholl, Dorothea; Unsicker, Sybille B.; Verhulst, Niels; Visser, Marcel E.; Weldegergis, Berhane T.; Köllner, Tobias G.


Chemical communication is ubiquitous. The identification of conserved structural elements in visual and acoustic communication is well established, but comparable information on chemical communication displays (CCDs) is lacking. We assessed the phenotypic integration of CCDs in a meta-analysis to characterize patterns of covariation in CCDs and identified functional or biosynthetically constrained modules. Poorly integrated plant CCDs (i.e. low covariation between scent compounds) support the notion that plants often utilize one or few key compounds to repel antagonists or to attract pollinators and enemies of herbivores. Animal CCDs (mostly insect pheromones) were usually more integrated than those of plants (i.e. stronger covariation), suggesting that animals communicate via fixed proportions among compounds. Both plant and animal CCDs were composed of modules, which are groups of strongly covarying compounds. Biosynthetic similarity of compounds revealed biosynthetic constraints in the covariation patterns of plant CCDs. We provide a novel perspective on chemical communication and a basis for future investigations on structural properties of CCDs. This will facilitate identifying modules and biosynthetic constraints that may affect the outcome of selection and thus provide a predictive framework for evolutionary trajectories of CCDs in plants and animals.