Insect phylogeny structures the bacterial communities in the microbiome of psyllids (Hemiptera: Psylloidea) in Aotearoa New Zealand

The bacterial microbiome of psyllids has been studied for decades, with a strong focus on the primary and secondary endosymbionts capable of providing essential amino acids for the insects' diet and therefore playing a key role in the insects' ability to radiate on novel plant hosts. Here,...

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Published in:PloS one 2023-05, Vol.18 (5), p.e0285587-e0285587
Main Authors: Martoni, Francesco, Bulman, Simon R, Piper, Alexander M, Pitman, Andrew, Taylor, Gary S, Armstrong, Karen F
Format: Article
Language:English
Subjects:
Adaptive radiation
Amino acids
Analysis
Animals
Auroral kilometric radiation
Bacteria
Bacteria - genetics
Biology and Life Sciences
Computer and Information Sciences
Datasets
Deoxyribonucleic acid
Dispersal
Dispersion
DNA
DNA barcoding
Endosymbionts
Flowers & plants
Genomes
Geographical distribution
Hemiptera - genetics
Host plants
Humans
Hypotheses
Identification and classification
Insects
Microbiomes
Microbiota - genetics
New Zealand
Nutrition research
People and places
Phylogenetics
Phylogeny
Plants
Radiation
Species diversity
Symbionts
Symbiosis - genetics
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cited_by cdi_FETCH-LOGICAL-c594t-7eb3311a52721c09fb4f1f203159f0574c6659f232f06c7c1332e0c65c6147683
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Bulman, Simon R
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Taylor, Gary S
Armstrong, Karen F
description The bacterial microbiome of psyllids has been studied for decades, with a strong focus on the primary and secondary endosymbionts capable of providing essential amino acids for the insects' diet and therefore playing a key role in the insects' ability to radiate on novel plant hosts. Here, we combine metabarcoding analysis of the bacterial communities hosted by psyllids with a multi-gene phylogenetic analysis of the insect hosts to determine what factors influence the bacterial diversity of the psyllids' microbiomes, especially in the context of the dispersal and evolutionary radiation of these insects in Aotearoa New Zealand. Using multi-gene phylogenetics with COI, 18S and EF-1α sequences from 102 psyllid species, we confirmed for the first time monophyly for all the six genera of native/endemic Aotearoa New Zealand psyllids, with indications that they derive from at least six dispersal events to the country. This also revealed that, after its ancestral arrival, the genus Powellia has radiated onto a larger and more diverse range of plants than either Psylla or Ctenarytaina, which is uncommon amongst monophyletic psyllids globally. DNA metabarcoding of the bacterial 16S gene here represents the largest dataset analysed to date from psyllids, including 246 individuals from 73 species. This provides novel evidence that bacterial diversity across psyllid species is strongly associated with psyllid phylogenetic structure, and to a lesser degree to their host plant association and geographic distribution. Furthermore, while the strongest co-phylogenetic signals were derived from the primary and secondary symbionts, a signal of phylosymbiosis was still retained among the remaining taxa of the bacterial microbiome, suggesting potential vertical transmission of bacterial lineages previously unknown to have symbiotic roles.
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Here, we combine metabarcoding analysis of the bacterial communities hosted by psyllids with a multi-gene phylogenetic analysis of the insect hosts to determine what factors influence the bacterial diversity of the psyllids' microbiomes, especially in the context of the dispersal and evolutionary radiation of these insects in Aotearoa New Zealand. Using multi-gene phylogenetics with COI, 18S and EF-1α sequences from 102 psyllid species, we confirmed for the first time monophyly for all the six genera of native/endemic Aotearoa New Zealand psyllids, with indications that they derive from at least six dispersal events to the country. This also revealed that, after its ancestral arrival, the genus Powellia has radiated onto a larger and more diverse range of plants than either Psylla or Ctenarytaina, which is uncommon amongst monophyletic psyllids globally. DNA metabarcoding of the bacterial 16S gene here represents the largest dataset analysed to date from psyllids, including 246 individuals from 73 species. This provides novel evidence that bacterial diversity across psyllid species is strongly associated with psyllid phylogenetic structure, and to a lesser degree to their host plant association and geographic distribution. Furthermore, while the strongest co-phylogenetic signals were derived from the primary and secondary symbionts, a signal of phylosymbiosis was still retained among the remaining taxa of the bacterial microbiome, suggesting potential vertical transmission of bacterial lineages previously unknown to have symbiotic roles.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>37186593</pmid><doi>10.1371/journal.pone.0285587</doi><orcidid>https://orcid.org/0000-0001-8064-4460</orcidid><oa>free_for_read</oa></addata></record>
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subjects Adaptive radiation
Amino acids
Analysis
Animals
Auroral kilometric radiation
Bacteria
Bacteria - genetics
Biology and Life Sciences
Computer and Information Sciences
Datasets
Deoxyribonucleic acid
Dispersal
Dispersion
DNA
DNA barcoding
Endosymbionts
Flowers & plants
Genomes
Geographical distribution
Hemiptera - genetics
Host plants
Humans
Hypotheses
Identification and classification
Insects
Microbiomes
Microbiota - genetics
New Zealand
Nutrition research
People and places
Phylogenetics
Phylogeny
Plants
Radiation
Species diversity
Symbionts
Symbiosis - genetics
title Insect phylogeny structures the bacterial communities in the microbiome of psyllids (Hemiptera: Psylloidea) in Aotearoa New Zealand
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