Phylosymbiosis Impacts Adaptive Traits in <italic toggle="yes">Nasonia</italic> Wasps

ABSTRACT Phylosymbiosis is defined as microbial community relationships that recapitulate the phylogeny of hosts. As evidence for phylosymbiosis rapidly accumulates in different vertebrate and invertebrate holobionts, a central question is what evolutionary forces cause this pattern. We use intra- a...

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Autores principales: Edward J. van Opstal, Seth R. Bordenstein
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Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:ce9012c8657c456e8b138e96d7a2b6bc2021-11-15T16:22:08ZPhylosymbiosis Impacts Adaptive Traits in <italic toggle="yes">Nasonia</italic> Wasps10.1128/mBio.00887-192150-7511https://doaj.org/article/ce9012c8657c456e8b138e96d7a2b6bc2019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00887-19https://doaj.org/toc/2150-7511ABSTRACT Phylosymbiosis is defined as microbial community relationships that recapitulate the phylogeny of hosts. As evidence for phylosymbiosis rapidly accumulates in different vertebrate and invertebrate holobionts, a central question is what evolutionary forces cause this pattern. We use intra- and interspecific gut microbiota transplants to test for evidence of selective pressures that contribute to phylosymbiosis. We leverage three closely related species of the parasitoid wasp model Nasonia that recently diverged between 0.4 and 1 million years ago: N. vitripennis, N. giraulti, and N. longicornis. Upon exposure of germfree larvae to heat-inactivated microbiota from intra- or interspecific larvae, we measure larval growth, pupation rate, and adult reproductive capacity. We report three key findings: (i) larval growth significantly slows when hosts receive an interspecific versus intraspecific gut microbiota, (ii) marked decreases in pupation and resulting adult survival occur from interspecific gut microbiota exposure, and (iii) adult reproductive capacities including male fertility and longevity are unaffected by early life exposure to an interspecific microbiota. Overall, these findings reveal developmental and survival costs to Nasonia upon larval exposures to interspecific microbiota and provide evidence that selective pressures on phenotypes produced by host-microbiota interactions may underpin phylosymbiosis. IMPORTANCE Phylosymbiosis is an ecoevolutionary hypothesis and emerging pattern in animal-microbiota studies whereby the host phylogenetic relationships parallel the community relationships of the host-associated microbiota. A central prediction of phylosymbiosis is that closely related hosts exhibit a lower microbiota beta diversity than distantly related hosts. While phylosymbiosis has emerged as a widespread trend in a field often challenged to find trends across systems, two critical and understudied questions are whether or not phylosymbiosis is consequential to host biology and if adaptive evolutionary forces underpin the pattern. Here, using germfree rearing in the phylosymbiosis model Nasonia, we demonstrate that early life exposure to heat-inactivated microbiota from more distantly related species poses more severe developmental and survival costs than microbiota from closely related or the same species. This study advances a functional understanding of the consequences and potential selective pressures underpinning phylosymbiosis.Edward J. van OpstalSeth R. BordensteinAmerican Society for MicrobiologyarticleNasoniaevolutionmicrobiomephylosymbiosisMicrobiologyQR1-502ENmBio, Vol 10, Iss 4 (2019)
institution DOAJ
collection DOAJ
language EN
topic Nasonia
evolution
microbiome
phylosymbiosis
Microbiology
QR1-502
spellingShingle Nasonia
evolution
microbiome
phylosymbiosis
Microbiology
QR1-502
Edward J. van Opstal
Seth R. Bordenstein
Phylosymbiosis Impacts Adaptive Traits in <italic toggle="yes">Nasonia</italic> Wasps
description ABSTRACT Phylosymbiosis is defined as microbial community relationships that recapitulate the phylogeny of hosts. As evidence for phylosymbiosis rapidly accumulates in different vertebrate and invertebrate holobionts, a central question is what evolutionary forces cause this pattern. We use intra- and interspecific gut microbiota transplants to test for evidence of selective pressures that contribute to phylosymbiosis. We leverage three closely related species of the parasitoid wasp model Nasonia that recently diverged between 0.4 and 1 million years ago: N. vitripennis, N. giraulti, and N. longicornis. Upon exposure of germfree larvae to heat-inactivated microbiota from intra- or interspecific larvae, we measure larval growth, pupation rate, and adult reproductive capacity. We report three key findings: (i) larval growth significantly slows when hosts receive an interspecific versus intraspecific gut microbiota, (ii) marked decreases in pupation and resulting adult survival occur from interspecific gut microbiota exposure, and (iii) adult reproductive capacities including male fertility and longevity are unaffected by early life exposure to an interspecific microbiota. Overall, these findings reveal developmental and survival costs to Nasonia upon larval exposures to interspecific microbiota and provide evidence that selective pressures on phenotypes produced by host-microbiota interactions may underpin phylosymbiosis. IMPORTANCE Phylosymbiosis is an ecoevolutionary hypothesis and emerging pattern in animal-microbiota studies whereby the host phylogenetic relationships parallel the community relationships of the host-associated microbiota. A central prediction of phylosymbiosis is that closely related hosts exhibit a lower microbiota beta diversity than distantly related hosts. While phylosymbiosis has emerged as a widespread trend in a field often challenged to find trends across systems, two critical and understudied questions are whether or not phylosymbiosis is consequential to host biology and if adaptive evolutionary forces underpin the pattern. Here, using germfree rearing in the phylosymbiosis model Nasonia, we demonstrate that early life exposure to heat-inactivated microbiota from more distantly related species poses more severe developmental and survival costs than microbiota from closely related or the same species. This study advances a functional understanding of the consequences and potential selective pressures underpinning phylosymbiosis.
format article
author Edward J. van Opstal
Seth R. Bordenstein
author_facet Edward J. van Opstal
Seth R. Bordenstein
author_sort Edward J. van Opstal
title Phylosymbiosis Impacts Adaptive Traits in <italic toggle="yes">Nasonia</italic> Wasps
title_short Phylosymbiosis Impacts Adaptive Traits in <italic toggle="yes">Nasonia</italic> Wasps
title_full Phylosymbiosis Impacts Adaptive Traits in <italic toggle="yes">Nasonia</italic> Wasps
title_fullStr Phylosymbiosis Impacts Adaptive Traits in <italic toggle="yes">Nasonia</italic> Wasps
title_full_unstemmed Phylosymbiosis Impacts Adaptive Traits in <italic toggle="yes">Nasonia</italic> Wasps
title_sort phylosymbiosis impacts adaptive traits in <italic toggle="yes">nasonia</italic> wasps
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/ce9012c8657c456e8b138e96d7a2b6bc
work_keys_str_mv AT edwardjvanopstal phylosymbiosisimpactsadaptivetraitsinitalictoggleyesnasoniaitalicwasps
AT sethrbordenstein phylosymbiosisimpactsadaptivetraitsinitalictoggleyesnasoniaitalicwasps
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