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RESEARCH PRODUCT

Nutritional symbionts enhance structural defence against predation and fungal infection in a grain pest beetle

Sthandiwe Nomthandazo KanyileTobias EnglMartin Kaltenpoth

subject

0106 biological sciencesCuticlePhysiologyCuticleBeauveria bassianaZoologyOryzaephilus surinamensisAquatic Science010603 evolutionary biology01 natural sciencesPredation03 medical and health sciencesAposymbioticMutualismSymbiosisCandidatus Shikimatogenerans silvanidophilusOryzaephilus surinamensisSawtoothed grain beetleAnimalsSymbiosisMolecular BiologyEcology Evolution Behavior and Systematics030304 developmental biologyStructural defenceMutualism (biology)0303 health sciencesbiologyBacteroidetesHost (biology)fungi15. Life on landbiology.organism_classificationColeopteraMycosesPredatory BehaviorInsect ScienceAnimal Science and ZoologyResearch Article

description

ABSTRACT Many insects benefit from bacterial symbionts that provide essential nutrients and thereby extend the hosts’ adaptive potential and their ability to cope with challenging environments. However, the implications of nutritional symbioses for the hosts’ defence against natural enemies remain largely unstudied. Here, we investigated whether the cuticle-enhancing nutritional symbiosis of the saw-toothed grain beetle Oryzaephilus surinamensis confers protection against predation and fungal infection. We exposed age-defined symbiotic and symbiont-depleted (aposymbiotic) beetles to two antagonists that must actively penetrate the cuticle for a successful attack: wolf spiders (Lycosidae) and the fungal entomopathogen Beauveria bassiana. While young beetles suffered from high predation and fungal infection rates regardless of symbiont presence, symbiotic beetles were able to escape this period of vulnerability and reach high survival probabilities significantly faster than aposymbiotic beetles. To understand the mechanistic basis of these differences, we conducted a time-series analysis of cuticle development in symbiotic and aposymbiotic beetles by measuring cuticular melanisation and thickness. The results reveal that the symbionts accelerate their host's cuticle formation and thereby enable it to quickly reach a cuticle quality threshold that confers structural protection against predation and fungal infection. Considering the widespread occurrence of cuticle enhancement via symbiont-mediated tyrosine supplementation in beetles and other insects, our findings demonstrate how nutritional symbioses can have important ecological implications reaching beyond the immediate nutrient-provisioning benefits.

https://doi.org/10.1242/jeb.243593