Endosymbiosis allows Sitophilus oryzae to persist in dry conditions

Abstract

Insects frequently associate with intracellular microbial symbionts (endosymbionts) that enhance their ability to cope with challenging environmental conditions. Endosymbioses with cuticle-enhancing microbes have been reported in several beetle families. However, the ecological relevance of these associations has seldom been demonstrated, particularly in the context of dry environments where high cuticle quality can reduce water loss. Thus, we investigated how cuticle-enhancing symbionts of the rice-weevil, Sitophilus oryzae contribute to desiccation resistance. We exposed symbiotic and symbiont-free (aposymbiotic) beetles to long-term stressful (47% RH) or relaxed (60% RH) humidity conditions and measured population growth. We found that symbiont presence benefits host fitness especially under dry conditions, enabling symbiotic beetles to increase their population size by over 33-fold within 3 months, while aposymbiotic beetles fail to increase in numbers beyond the starting population in the same conditions. To understand the mechanisms underlying this drastic effect, we compared beetle size and body water content and found that endosymbionts confer bigger body size and higher body water content. While chemical analyses revealed no significant differences in composition and quantity of cuticular hydrocarbons after long-term exposure to desiccation stress, symbiotic beetles lost water at a proportionally slower rate than did their aposymbiotic counterparts. We posit that the desiccation resistance and higher fitness observed in symbiotic beetles under dry conditions is due to their symbiont-enhanced thicker cuticle, which provides protection against cuticular transpiration. Thus, we demonstrate that the cuticle enhancing symbiosis of Sitophilus oryzae confers a fitness benefit under drought stress, an ecologically relevant condition for grain pest beetles. This benefit likely extends to many other systems where symbiont-mediated cuticle synthesis has been identified, including taxa spanning beetles and ants that occupy different ecological niches.

With a little help from my friends: the roles of microbial symbionts in insect populations and communities

“…B 379: 20230122 facilitate infecting further hosts [61,89,90]. Experiments have consistently shown an increase in survival and/or reproduction of individuals carrying protective symbionts and a decrease in the success and fitness of natural enemies [91][92][93].…”

“…Likewise, symbionts can also confer protection against a wide range of environmentally relevant abiotic stressors. Facultative endosymbionts have been shown to protect their insect hosts against heat [74,75,94,95], water loss and desiccation [92], pesticides [77], and heavy metals [96] (table 1). On the other hand, symbionts' susceptibility to these factors can be the insects' weakness, as demonstrated by heat-disrupted beneficial symbioses of aphids and stinkbugs [97][98][99], or herbicide-disrupted symbioses of bees [100].…”

With a little help from my friends: the roles of microbial symbionts in insect populations and communities.

“…Further, symbionts can aid their hosts by decreasing the success of an attack or infection. Possible mechanisms include altering cuticle properties, especially thickness and density [71,72], the attacked insects' defensive responses [73], or its overall condition that may determine the effectiveness of the defense. However, symbionts' effects on their insect abilities to fight off infections are best known.…”

“…Insects can also enjoy symbiont-conferred protection against a wide range of environmentally relevant abiotic stressors. Facultative endosymbionts have been shown to protect their hosts against heat [80][81][82][83], water loss and desiccation [72], pesticides [84], and heavy metals [85] (Table 1). In all cases, experiments showed a clear increase in survival or reproductive fitnessrelated traits of the exposed individuals that carried protective symbionts.…”

Host-Encoded Aminotransferase Import into the Endosymbiotic Bacteria Nardonella of Red Palm Weevil

“…Nardonella's biological role is to provide the host with tyrosine, which is a precursor necessary for the formation and hardening of the insect epidermis [11]. The prosperity of weevils in terrestrial ecosystems is partly due to their highly sclerotized exoskeleton, which preserves their bodies from desiccation, predators, and pathogens [11][12][13][14]. Therefore, Nardonella is important for the evolutionary success of weevils.…”