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

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 <i>Oryzaephilus surinamensis</i> harbors nutritional, intracellular Bacteroidetes bacteria t...

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Main Authors: Tobias Engl, Thorsten H. P. Schmidt, Sthandiwe Nomthandazo Kanyile, Dagmar Klebsch
Format: Article
Language:English
Published: MDPI AG 2020-10-01
Series:Insects
Subjects:
Online Access:https://www.mdpi.com/2075-4450/11/10/717
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author Tobias Engl
Thorsten H. P. Schmidt
Sthandiwe Nomthandazo Kanyile
Dagmar Klebsch
author_facet Tobias Engl
Thorsten H. P. Schmidt
Sthandiwe Nomthandazo Kanyile
Dagmar Klebsch
author_sort Tobias Engl
collection DOAJ
description 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 <i>Oryzaephilus surinamensis</i> 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 <i>O. surinamensis</i> symbiosis thereby represents an experimentally amenable system to study eco-evolutionary dynamics under variable selection pressures.
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spelling doaj.art-5052d95de66c4c55857d3903cd82c5ce2023-11-20T17:45:02ZengMDPI AGInsects2075-44502020-10-01111071710.3390/insects11100717Metabolic Cost of a Nutritional Symbiont Manifests in Delayed Reproduction in a Grain Pest BeetleTobias Engl0Thorsten H. P. Schmidt1Sthandiwe Nomthandazo Kanyile2Dagmar Klebsch3Evolutionary Ecology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg-University, 55128 Mainz, GermanyEvolutionary Ecology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg-University, 55128 Mainz, GermanyEvolutionary Ecology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg-University, 55128 Mainz, GermanyEvolutionary Ecology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg-University, 55128 Mainz, GermanyAnimals 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 <i>Oryzaephilus surinamensis</i> 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 <i>O. surinamensis</i> symbiosis thereby represents an experimentally amenable system to study eco-evolutionary dynamics under variable selection pressures.https://www.mdpi.com/2075-4450/11/10/717bacteroidetescuticle synthesismetabolic and fitness costOryzaephilus surinamensissawtoothed grain beetlesymbiosis
spellingShingle Tobias Engl
Thorsten H. P. Schmidt
Sthandiwe Nomthandazo Kanyile
Dagmar Klebsch
Metabolic Cost of a Nutritional Symbiont Manifests in Delayed Reproduction in a Grain Pest Beetle
Insects
bacteroidetes
cuticle synthesis
metabolic and fitness cost
Oryzaephilus surinamensis
sawtoothed grain beetle
symbiosis
title Metabolic Cost of a Nutritional Symbiont Manifests in Delayed Reproduction in a Grain Pest Beetle
title_full Metabolic Cost of a Nutritional Symbiont Manifests in Delayed Reproduction in a Grain Pest Beetle
title_fullStr Metabolic Cost of a Nutritional Symbiont Manifests in Delayed Reproduction in a Grain Pest Beetle
title_full_unstemmed Metabolic Cost of a Nutritional Symbiont Manifests in Delayed Reproduction in a Grain Pest Beetle
title_short Metabolic Cost of a Nutritional Symbiont Manifests in Delayed Reproduction in a Grain Pest Beetle
title_sort metabolic cost of a nutritional symbiont manifests in delayed reproduction in a grain pest beetle
topic bacteroidetes
cuticle synthesis
metabolic and fitness cost
Oryzaephilus surinamensis
sawtoothed grain beetle
symbiosis
url https://www.mdpi.com/2075-4450/11/10/717
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