Metabolic Cost of a Nutritional Symbiont Manifests in Delayed Reproduction in a Grain Pest Beetle

Abstract

Animals engage in a plethora of mutualistic interactions with microorganisms that can confer various benefits to their host but can also incur context-dependent costs. The sawtoothed grain beetle Oryzaephilus surinamensis harbors nutritional, intracellular Bacteroidetes bacteria that supplement precursors for the cuticle synthesis and thereby enhance desiccation resistance of its host. Experimental elimination of the symbiont impairs cuticle formation and reduces fitness under desiccation stress but does not disrupt the host’s life cycle. For this study, we first demonstrated that symbiont populations showed the strongest growth at the end of metamorphosis and then declined continuously in males, but not in females. The symbiont loss neither impacted the development time until adulthood nor adult mortality or lifespan. Furthermore, lifetime reproduction was not influenced by the symbiont presence. However, symbiotic females started to reproduce almost two weeks later than aposymbiotic ones. Thus, symbiont presence incurs a metabolic and context-dependent fitness cost to females, probably due to a nutrient allocation trade-off between symbiont growth and sexual maturation. The O. surinamensis symbiosis thereby represents an experimentally amenable system to study eco-evolutionary dynamics under variable selection pressures.

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

“…Concordantly, experimentally symbiont depleted (aposymbiotic) beetles exhibit a thinner and less melanised cuticle than their symbiotic counterparts (Hirota et al, 2017;Engl et al, 2018) and show a reduced resistance to desiccation and lower fitness under dry ambient conditions (Engl et al 2018). However, besides delayed reproductive maturation in symbiotic beetles, no further differences between symbiotic and aposymbiotic beetles regarding other life history traits were observed in laboratory rearing conditions (Engl et al, 2020).…”

Insect-host control of obligate, intracellular symbiont density

“…Measuring host fitness in the absence of symbionts is relatively straightforward, as aposymbiotic hosts can be reared by treating mothers with antibiotics. The results of these treatments clearly demonstrate that reproduction, development and immunity are severely compromised in the absence of symbionts [22,[74][75][76][77]. More challenging is manipulating symbiont density and measuring effects on host fitness.…”

“…As well as the benefits acquired by hosts of participating in mutualistic symbioses with bacteria, there are costs to hosts associated with providing the energy and nutrients to maintain a symbiont population (e.g. [ 22 ]). The net benefit to a host is therefore determined by the difference between the benefit and cost, with both benefits and costs potentially depending on the size of the symbiont population.…”

Symbiotic microbial studies in diverse populations of Aphis gossypii, existing on altered host plants in different localities during different times

“…Recent studies showed that symbiotic bacteria contribute to host variation, heat tolerance (Zhang, Leonard, et al., 2019 ), and temperature preference (Hague et al., 2020 ). Meanwhile the host should also bear the metabolic and fitness‐dependent cost to symbiont bacterial presence (Engl et al., 2020 ; Oliver et al., 2008 ); bacterial symbionts even can shape their host evolution (Coffman & Burke, 2020 ). Therefore, it is very important and necessary for insects to maintain a balanced population of symbiotic bacteria.…”

“…Meanwhile the host should also bear the metabolic and fitnessdependent cost to symbiont bacterial presence (Engl et al, 2020;Oliver et al, 2008); bacterial symbionts even can shape their host evolution (Coffman & Burke, 2020). Therefore, it is very important and necessary for insects to maintain a balanced population of symbiotic bacteria.…”