Is Host Filtering the Main Driver of Phylosymbiosis across the Tree of Life?

ABSTRACT Host-associated microbiota composition can be conserved over evolutionary time scales. Indeed, closely related species often host similar microbiota; i.e., the composition of their microbiota harbors a phylogenetic signal, a pattern sometimes referred to as “phylosymbiosis.” Elucidating the...

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Autores principales:	Florent Mazel, Katherine M. Davis, Andrew Loudon, Waldan K. Kwong, Mathieu Groussin, Laura Wegener Parfrey
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	endosphere gut microbiome holobiont macroevolution plant microbiome rhizosphere Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/fd19c083d4374f498cf4e9c3c4e01d37
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spelling	oai:doaj.org-article:fd19c083d4374f498cf4e9c3c4e01d372021-12-02T19:46:18ZIs Host Filtering the Main Driver of Phylosymbiosis across the Tree of Life?10.1128/mSystems.00097-182379-5077https://doaj.org/article/fd19c083d4374f498cf4e9c3c4e01d372018-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00097-18https://doaj.org/toc/2379-5077ABSTRACT Host-associated microbiota composition can be conserved over evolutionary time scales. Indeed, closely related species often host similar microbiota; i.e., the composition of their microbiota harbors a phylogenetic signal, a pattern sometimes referred to as “phylosymbiosis.” Elucidating the origins of this pattern is important to better understand microbiota ecology and evolution. However, this is hampered by our lack of theoretical expectations and a comprehensive overview of phylosymbiosis prevalence in nature. Here, we use simulations to provide a simple expectation for when we should expect this pattern to occur and then review the literature to document the prevalence and strength of phylosymbiosis across the host tree of life. We demonstrate that phylosymbiosis can readily emerge from a simple ecological filtering process, whereby a given host trait (e.g., gut pH) that varies with host phylogeny (i.e., harbors a phylogenetic signal) filters preadapted microbes. We found marked differences between methods used to detect phylosymbiosis, so we proposed a series of practical recommendations based on using multiple best-performing approaches. Importantly, we found that, while the prevalence of phylosymbiosis is mixed in nature, it appears to be stronger for microbiotas living in internal host compartments (e.g., the gut) than those living in external compartments (e.g., the rhizosphere). We show that phylosymbiosis can theoretically emerge without any intimate, long-term coevolutionary mechanisms and that most phylosymbiosis patterns observed in nature are compatible with a simple ecological process. Deviations from baseline ecological expectations might be used to further explore more complex hypotheses, such as codiversification. IMPORTANCE Phylosymbiosis is a pattern defined as the tendency of closely related species to host microbiota whose compositions resemble each other more than host species drawn at random from the same tree. Understanding the mechanisms behind phylosymbiosis is important because it can shed light on rules governing the assembly of host-associated microbiotas and, potentially, their coevolutionary dynamics with hosts. For example, is phylosymbiosis a result of coevolution, or can it be generated by simple ecological filtering processes? Beyond qualitative theoretical models, quantitative theoretical expectations can provide new insights. For example, deviations from a simple baseline of ecological filtering may be used to test more-complex hypotheses (e.g., coevolution). Here, we use simulations to provide evidence that simple host-related ecological filtering can readily generate phylosymbiosis, and we contrast these predictions with real-world data. We find that while phylosymbiosis is widespread in nature, phylosymbiosis patterns are compatible with a simple ecological model in the majority of taxa. Internal compartments of hosts, such as the animal gut, often display stronger phylosymbiosis than expected from a purely ecological filtering process, suggesting that other mechanisms are also involved.Florent MazelKatherine M. DavisAndrew LoudonWaldan K. KwongMathieu GroussinLaura Wegener ParfreyAmerican Society for Microbiologyarticleendospheregut microbiomeholobiontmacroevolutionplant microbiomerhizosphereMicrobiologyQR1-502ENmSystems, Vol 3, Iss 5 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	endosphere gut microbiome holobiont macroevolution plant microbiome rhizosphere Microbiology QR1-502
spellingShingle	endosphere gut microbiome holobiont macroevolution plant microbiome rhizosphere Microbiology QR1-502 Florent Mazel Katherine M. Davis Andrew Loudon Waldan K. Kwong Mathieu Groussin Laura Wegener Parfrey Is Host Filtering the Main Driver of Phylosymbiosis across the Tree of Life?
description	ABSTRACT Host-associated microbiota composition can be conserved over evolutionary time scales. Indeed, closely related species often host similar microbiota; i.e., the composition of their microbiota harbors a phylogenetic signal, a pattern sometimes referred to as “phylosymbiosis.” Elucidating the origins of this pattern is important to better understand microbiota ecology and evolution. However, this is hampered by our lack of theoretical expectations and a comprehensive overview of phylosymbiosis prevalence in nature. Here, we use simulations to provide a simple expectation for when we should expect this pattern to occur and then review the literature to document the prevalence and strength of phylosymbiosis across the host tree of life. We demonstrate that phylosymbiosis can readily emerge from a simple ecological filtering process, whereby a given host trait (e.g., gut pH) that varies with host phylogeny (i.e., harbors a phylogenetic signal) filters preadapted microbes. We found marked differences between methods used to detect phylosymbiosis, so we proposed a series of practical recommendations based on using multiple best-performing approaches. Importantly, we found that, while the prevalence of phylosymbiosis is mixed in nature, it appears to be stronger for microbiotas living in internal host compartments (e.g., the gut) than those living in external compartments (e.g., the rhizosphere). We show that phylosymbiosis can theoretically emerge without any intimate, long-term coevolutionary mechanisms and that most phylosymbiosis patterns observed in nature are compatible with a simple ecological process. Deviations from baseline ecological expectations might be used to further explore more complex hypotheses, such as codiversification. IMPORTANCE Phylosymbiosis is a pattern defined as the tendency of closely related species to host microbiota whose compositions resemble each other more than host species drawn at random from the same tree. Understanding the mechanisms behind phylosymbiosis is important because it can shed light on rules governing the assembly of host-associated microbiotas and, potentially, their coevolutionary dynamics with hosts. For example, is phylosymbiosis a result of coevolution, or can it be generated by simple ecological filtering processes? Beyond qualitative theoretical models, quantitative theoretical expectations can provide new insights. For example, deviations from a simple baseline of ecological filtering may be used to test more-complex hypotheses (e.g., coevolution). Here, we use simulations to provide evidence that simple host-related ecological filtering can readily generate phylosymbiosis, and we contrast these predictions with real-world data. We find that while phylosymbiosis is widespread in nature, phylosymbiosis patterns are compatible with a simple ecological model in the majority of taxa. Internal compartments of hosts, such as the animal gut, often display stronger phylosymbiosis than expected from a purely ecological filtering process, suggesting that other mechanisms are also involved.
format	article
author	Florent Mazel Katherine M. Davis Andrew Loudon Waldan K. Kwong Mathieu Groussin Laura Wegener Parfrey
author_facet	Florent Mazel Katherine M. Davis Andrew Loudon Waldan K. Kwong Mathieu Groussin Laura Wegener Parfrey
author_sort	Florent Mazel
title	Is Host Filtering the Main Driver of Phylosymbiosis across the Tree of Life?
title_short	Is Host Filtering the Main Driver of Phylosymbiosis across the Tree of Life?
title_full	Is Host Filtering the Main Driver of Phylosymbiosis across the Tree of Life?
title_fullStr	Is Host Filtering the Main Driver of Phylosymbiosis across the Tree of Life?
title_full_unstemmed	Is Host Filtering the Main Driver of Phylosymbiosis across the Tree of Life?
title_sort	is host filtering the main driver of phylosymbiosis across the tree of life?
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/fd19c083d4374f498cf4e9c3c4e01d37
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Is Host Filtering the Main Driver of Phylosymbiosis across the Tree of Life?

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