Holes in the Hologenome: Why Host-Microbe Symbioses Are Not Holobionts

ABSTRACT The advent of relatively inexpensive tools for characterizing microbial communities has led to an explosion of research exploring the diversity, ecology, and evolution of microbe-host systems. Some now question whether existing conceptual frameworks are adequate to explain microbe-host syst...

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Autores principales:	Angela E. Douglas, John H. Werren
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/fe1f25b833dc4e0fa89e8f24f429fd86
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spelling	oai:doaj.org-article:fe1f25b833dc4e0fa89e8f24f429fd862021-11-15T15:41:42ZHoles in the Hologenome: Why Host-Microbe Symbioses Are Not Holobionts10.1128/mBio.02099-152150-7511https://doaj.org/article/fe1f25b833dc4e0fa89e8f24f429fd862016-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02099-15https://doaj.org/toc/2150-7511ABSTRACT The advent of relatively inexpensive tools for characterizing microbial communities has led to an explosion of research exploring the diversity, ecology, and evolution of microbe-host systems. Some now question whether existing conceptual frameworks are adequate to explain microbe-host systems. One popular paradigm is the “holobiont-hologenome,” which argues that a host and its microbiome evolve as a single cooperative unit of selection (i.e., a superorganism). We argue that the hologenome is based on overly restrictive assumptions which render it an approach of little research utility. A host plus its microbiome is more effectively viewed as an ecological community of organisms that encompasses a broad range of interactions (parasitic to mutualistic), patterns of transmission (horizontal to vertical), and levels of fidelity among partners. The hologenome requires high partner fidelity if it is to evolve as a unit. However, even when this is achieved by particular host-microbe pairs, it is unlikely to hold for the entire host microbiome, and therefore the community is unlikely to evolve as a hologenome. Both mutualistic and antagonistic (fitness conflict) evolution can occur among constituent members of the community, not just adaptations at the “hologenome” level, and there is abundant empirical evidence for such divergence of selective interests among members of host-microbiome communities. We believe that the concepts and methods of ecology, genetics, and evolutionary biology will continue to provide a well-grounded intellectual framework for researching host-microbiome communities, without recourse to the limiting assumption that selection acts predominantly at the holobiont level.Angela E. DouglasJohn H. WerrenAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 2 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Angela E. Douglas John H. Werren Holes in the Hologenome: Why Host-Microbe Symbioses Are Not Holobionts
description	ABSTRACT The advent of relatively inexpensive tools for characterizing microbial communities has led to an explosion of research exploring the diversity, ecology, and evolution of microbe-host systems. Some now question whether existing conceptual frameworks are adequate to explain microbe-host systems. One popular paradigm is the “holobiont-hologenome,” which argues that a host and its microbiome evolve as a single cooperative unit of selection (i.e., a superorganism). We argue that the hologenome is based on overly restrictive assumptions which render it an approach of little research utility. A host plus its microbiome is more effectively viewed as an ecological community of organisms that encompasses a broad range of interactions (parasitic to mutualistic), patterns of transmission (horizontal to vertical), and levels of fidelity among partners. The hologenome requires high partner fidelity if it is to evolve as a unit. However, even when this is achieved by particular host-microbe pairs, it is unlikely to hold for the entire host microbiome, and therefore the community is unlikely to evolve as a hologenome. Both mutualistic and antagonistic (fitness conflict) evolution can occur among constituent members of the community, not just adaptations at the “hologenome” level, and there is abundant empirical evidence for such divergence of selective interests among members of host-microbiome communities. We believe that the concepts and methods of ecology, genetics, and evolutionary biology will continue to provide a well-grounded intellectual framework for researching host-microbiome communities, without recourse to the limiting assumption that selection acts predominantly at the holobiont level.
format	article
author	Angela E. Douglas John H. Werren
author_facet	Angela E. Douglas John H. Werren
author_sort	Angela E. Douglas
title	Holes in the Hologenome: Why Host-Microbe Symbioses Are Not Holobionts
title_short	Holes in the Hologenome: Why Host-Microbe Symbioses Are Not Holobionts
title_full	Holes in the Hologenome: Why Host-Microbe Symbioses Are Not Holobionts
title_fullStr	Holes in the Hologenome: Why Host-Microbe Symbioses Are Not Holobionts
title_full_unstemmed	Holes in the Hologenome: Why Host-Microbe Symbioses Are Not Holobionts
title_sort	holes in the hologenome: why host-microbe symbioses are not holobionts
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/fe1f25b833dc4e0fa89e8f24f429fd86
work_keys_str_mv	AT angelaedouglas holesinthehologenomewhyhostmicrobesymbiosesarenotholobionts AT johnhwerren holesinthehologenomewhyhostmicrobesymbiosesarenotholobionts
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Holes in the Hologenome: Why Host-Microbe Symbioses Are Not Holobionts

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