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Egg survival is reduced by grave-soil microbes in the carrion beetle, Nicrophorus vespilloides

BACKGROUND: Nicrophorus vespilloides eggs are deposited into the soil in close proximity to the decomposing vertebrate carcasses that these insects use as an obligate resource to rear their offspring. Eggs in this environment potentially face significant risks from the bacteria that proliferate in t...

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Autores principales: Jacobs, Chris G C, Wang, Yin, Vogel, Heiko, Vilcinskas, Andreas, van der Zee, Maurijn, Rozen, Daniel E
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4189599/
https://www.ncbi.nlm.nih.gov/pubmed/25260512
http://dx.doi.org/10.1186/s12862-014-0208-x
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author Jacobs, Chris G C
Wang, Yin
Vogel, Heiko
Vilcinskas, Andreas
van der Zee, Maurijn
Rozen, Daniel E
author_facet Jacobs, Chris G C
Wang, Yin
Vogel, Heiko
Vilcinskas, Andreas
van der Zee, Maurijn
Rozen, Daniel E
author_sort Jacobs, Chris G C
collection PubMed
description BACKGROUND: Nicrophorus vespilloides eggs are deposited into the soil in close proximity to the decomposing vertebrate carcasses that these insects use as an obligate resource to rear their offspring. Eggs in this environment potentially face significant risks from the bacteria that proliferate in the grave-soil environment following nutrient influx from the decomposing carcass. Our aims in this paper are twofold: first, to examine the fitness effects of grave-soil bacteria to eggs, and second, to quantify egg immunocompetence as a defence against these bacteria. RESULTS: Our results provide strong evidence that grave-soil microbes significantly reduce the survival of Nicrophorus eggs. Females provided with microbe rich carcasses to rear broods laid fewer eggs that were less likely to hatch than females given uncontaminated carcasses. Furthermore, we show that egg hatch success is significantly reduced by bacterial exposure. Using a split-brood design, which controlled for intrinsic differences in eggs produced by different females, we found that eggs washed free of surface-associated bacteria show increased survival compared to unwashed eggs. By contrast, eggs exposed to the entomopathogen Serratia marcescens show decreased survival compared to unexposed eggs. We next tested the immune competence of eggs under challenge from bacterial infection, and found that eggs lacked endogenous production of antimicrobial peptides, despite well-developed responses in larvae. Finally, we found that despite lacking immunity, N. vespilloides eggs produce an extraembryonic serosa, indicating that the serosa has lost its immune inducing capacity in this species. CONCLUSIONS: The dependency on ephemeral resources might strongly select for fast developing animals. Our results suggest that Nicrophorus carrion beetles, and other species developing on ephemeral resources, face a fundamental trade-off between egg immunity and development time. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-014-0208-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-41895992014-10-09 Egg survival is reduced by grave-soil microbes in the carrion beetle, Nicrophorus vespilloides Jacobs, Chris G C Wang, Yin Vogel, Heiko Vilcinskas, Andreas van der Zee, Maurijn Rozen, Daniel E BMC Evol Biol Research Article BACKGROUND: Nicrophorus vespilloides eggs are deposited into the soil in close proximity to the decomposing vertebrate carcasses that these insects use as an obligate resource to rear their offspring. Eggs in this environment potentially face significant risks from the bacteria that proliferate in the grave-soil environment following nutrient influx from the decomposing carcass. Our aims in this paper are twofold: first, to examine the fitness effects of grave-soil bacteria to eggs, and second, to quantify egg immunocompetence as a defence against these bacteria. RESULTS: Our results provide strong evidence that grave-soil microbes significantly reduce the survival of Nicrophorus eggs. Females provided with microbe rich carcasses to rear broods laid fewer eggs that were less likely to hatch than females given uncontaminated carcasses. Furthermore, we show that egg hatch success is significantly reduced by bacterial exposure. Using a split-brood design, which controlled for intrinsic differences in eggs produced by different females, we found that eggs washed free of surface-associated bacteria show increased survival compared to unwashed eggs. By contrast, eggs exposed to the entomopathogen Serratia marcescens show decreased survival compared to unexposed eggs. We next tested the immune competence of eggs under challenge from bacterial infection, and found that eggs lacked endogenous production of antimicrobial peptides, despite well-developed responses in larvae. Finally, we found that despite lacking immunity, N. vespilloides eggs produce an extraembryonic serosa, indicating that the serosa has lost its immune inducing capacity in this species. CONCLUSIONS: The dependency on ephemeral resources might strongly select for fast developing animals. Our results suggest that Nicrophorus carrion beetles, and other species developing on ephemeral resources, face a fundamental trade-off between egg immunity and development time. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-014-0208-x) contains supplementary material, which is available to authorized users. BioMed Central 2014-09-27 /pmc/articles/PMC4189599/ /pubmed/25260512 http://dx.doi.org/10.1186/s12862-014-0208-x Text en © Jacobs et al.; licensee BioMed Central Ltd. 2014 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Jacobs, Chris G C
Wang, Yin
Vogel, Heiko
Vilcinskas, Andreas
van der Zee, Maurijn
Rozen, Daniel E
Egg survival is reduced by grave-soil microbes in the carrion beetle, Nicrophorus vespilloides
title Egg survival is reduced by grave-soil microbes in the carrion beetle, Nicrophorus vespilloides
title_full Egg survival is reduced by grave-soil microbes in the carrion beetle, Nicrophorus vespilloides
title_fullStr Egg survival is reduced by grave-soil microbes in the carrion beetle, Nicrophorus vespilloides
title_full_unstemmed Egg survival is reduced by grave-soil microbes in the carrion beetle, Nicrophorus vespilloides
title_short Egg survival is reduced by grave-soil microbes in the carrion beetle, Nicrophorus vespilloides
title_sort egg survival is reduced by grave-soil microbes in the carrion beetle, nicrophorus vespilloides
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4189599/
https://www.ncbi.nlm.nih.gov/pubmed/25260512
http://dx.doi.org/10.1186/s12862-014-0208-x
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