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Diplogastrellus nematodes are sexually transmitted mutualists that alter the bacterial and fungal communities of their beetle host

A recent accumulation of studies has demonstrated that nongenetic, maternally transmitted factors are often critical to the health and development of offspring and can therefore play a role in ecological and evolutionary processes. In particular, microorganisms such as bacteria have been championed...

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Autores principales: Ledón-Rettig, Cristina C., Moczek, Armin P., Ragsdale, Erik J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6196496/
https://www.ncbi.nlm.nih.gov/pubmed/30275294
http://dx.doi.org/10.1073/pnas.1809606115
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author Ledón-Rettig, Cristina C.
Moczek, Armin P.
Ragsdale, Erik J.
author_facet Ledón-Rettig, Cristina C.
Moczek, Armin P.
Ragsdale, Erik J.
author_sort Ledón-Rettig, Cristina C.
collection PubMed
description A recent accumulation of studies has demonstrated that nongenetic, maternally transmitted factors are often critical to the health and development of offspring and can therefore play a role in ecological and evolutionary processes. In particular, microorganisms such as bacteria have been championed as heritable, symbiotic partners capable of conferring fitness benefits to their hosts. At the same time, parents may also pass various nonmicrobial organisms to their offspring, yet the roles of such organisms in shaping the developmental environment of their hosts remain largely unexplored. Here, we show that the nematode Diplogastrellus monhysteroides is transgenerationally inherited and sexually transmitted by the dung beetle Onthophagus taurus. By manipulating artificial chambers in which beetle offspring develop, we demonstrate that the presence of D. monhysteroides nematodes enhances the growth of beetle offspring, empirically challenging the paradigm that nematodes are merely commensal or even detrimental to their insect hosts. Finally, our research presents a compelling mechanism whereby the nematodes influence the health of beetle larvae: D. monhysteroides nematodes engineer the bacterial and fungal communities that also inhabit the beetle developmental chambers, including specific taxa known to be involved in biomass degradation, possibly allowing larval beetles better access to their otherwise recalcitrant, plant-based diet. Thus, our findings illustrate that nongenetic inheritance can include intermediately sized organisms that live and proliferate in close association with, and in certain cases enhance, the development of their hosts’ offspring.
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spelling pubmed-61964962018-10-23 Diplogastrellus nematodes are sexually transmitted mutualists that alter the bacterial and fungal communities of their beetle host Ledón-Rettig, Cristina C. Moczek, Armin P. Ragsdale, Erik J. Proc Natl Acad Sci U S A Biological Sciences A recent accumulation of studies has demonstrated that nongenetic, maternally transmitted factors are often critical to the health and development of offspring and can therefore play a role in ecological and evolutionary processes. In particular, microorganisms such as bacteria have been championed as heritable, symbiotic partners capable of conferring fitness benefits to their hosts. At the same time, parents may also pass various nonmicrobial organisms to their offspring, yet the roles of such organisms in shaping the developmental environment of their hosts remain largely unexplored. Here, we show that the nematode Diplogastrellus monhysteroides is transgenerationally inherited and sexually transmitted by the dung beetle Onthophagus taurus. By manipulating artificial chambers in which beetle offspring develop, we demonstrate that the presence of D. monhysteroides nematodes enhances the growth of beetle offspring, empirically challenging the paradigm that nematodes are merely commensal or even detrimental to their insect hosts. Finally, our research presents a compelling mechanism whereby the nematodes influence the health of beetle larvae: D. monhysteroides nematodes engineer the bacterial and fungal communities that also inhabit the beetle developmental chambers, including specific taxa known to be involved in biomass degradation, possibly allowing larval beetles better access to their otherwise recalcitrant, plant-based diet. Thus, our findings illustrate that nongenetic inheritance can include intermediately sized organisms that live and proliferate in close association with, and in certain cases enhance, the development of their hosts’ offspring. National Academy of Sciences 2018-10-16 2018-10-01 /pmc/articles/PMC6196496/ /pubmed/30275294 http://dx.doi.org/10.1073/pnas.1809606115 Text en Copyright © 2018 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Ledón-Rettig, Cristina C.
Moczek, Armin P.
Ragsdale, Erik J.
Diplogastrellus nematodes are sexually transmitted mutualists that alter the bacterial and fungal communities of their beetle host
title Diplogastrellus nematodes are sexually transmitted mutualists that alter the bacterial and fungal communities of their beetle host
title_full Diplogastrellus nematodes are sexually transmitted mutualists that alter the bacterial and fungal communities of their beetle host
title_fullStr Diplogastrellus nematodes are sexually transmitted mutualists that alter the bacterial and fungal communities of their beetle host
title_full_unstemmed Diplogastrellus nematodes are sexually transmitted mutualists that alter the bacterial and fungal communities of their beetle host
title_short Diplogastrellus nematodes are sexually transmitted mutualists that alter the bacterial and fungal communities of their beetle host
title_sort diplogastrellus nematodes are sexually transmitted mutualists that alter the bacterial and fungal communities of their beetle host
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6196496/
https://www.ncbi.nlm.nih.gov/pubmed/30275294
http://dx.doi.org/10.1073/pnas.1809606115
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