Partner fidelity and environmental filtering preserve stage‐specific turtle ant gut symbioses for over 40 million years

Hu, Yi; D’Amelio, Catherine L.; Béchade, Benoît; Cabuslay, Christian; Łukasik, Piotr; Sanders, Jon G.; Price, Shauna L.; Fanwick, Emily; Powell, Scott; Moreau, Corrie S.; Russell, Jacob A.

doi:10.1002/ecm.1560

Cited by 13 publications

(41 citation statements)

References 188 publications

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“…As with their free‐living counterparts (Little et al, 2008), the stability of symbiont communities is affected by ecological and evolutionary processes. These include microbial competition and cooperation (Consuegra, Grenier, Akherraz, et al, 2020; Figueiredo & Kramer, 2020; Johnston & Rolff, 2015), priority effects and environmental filtering (Bongrand & Ruby, 2019; Dal Grande et al, 2018; David et al, 2016; Devevey et al, 2015; Hu et al, 2022; Lee et al, 2013; Sprockett et al, 2018; Youngblut et al, 2019), and selection acting at the host level on symbiont‐conferred phenotypes (e.g. Andongma et al, 2022; Hughes et al, 2014; Itoh et al, 2019; Rossi et al, 2015; Theis et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Cryptic community structure and metabolic interactions among the heritable facultative symbionts of the pea aphid

Peng,

Hoban,

Joffe

et al. 2023

Journal of Evolutionary Biology

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Most insects harbour influential, yet non‐essential heritable microbes in their hemocoel. Communities of these symbionts exhibit low diversity. But their frequent multi‐species nature raises intriguing questions on roles for symbiont–symbiont synergies in host adaptation, and on the stability of the symbiont communities, themselves. In this study, we build on knowledge of species‐defined symbiont community structure across US populations of the pea aphid, Acyrthosiphon pisum. Through extensive symbiont genotyping, we show that pea aphids' microbiomes can be more precisely defined at the symbiont strain level, with strain variability shaping five out of nine previously reported co‐infection trends. Field data provide a mixture of evidence for synergistic fitness effects and symbiont hitchhiking, revealing causes and consequences of these co‐infection trends. To test whether within‐host metabolic interactions predict common versus rare strain‐defined communities, we leveraged the high relatedness of our dominant, community‐defined symbiont strains vs. 12 pea aphid‐derived Gammaproteobacteria with sequenced genomes. Genomic inference, using metabolic complementarity indices, revealed high potential for cooperation among one pair of symbionts—Serratia symbiotica and Rickettsiella viridis. Applying the expansion network algorithm, through additional use of pea aphid and obligate Buchnera symbiont genomes, Serratia and Rickettsiella emerged as the only symbiont community requiring both parties to expand holobiont metabolism. Through their joint expansion of the biotin biosynthesis pathway, these symbionts may span missing gaps, creating a multi‐party mutualism within their nutrient‐limited, phloem‐feeding hosts. Recent, complementary gene inactivation, within the biotin pathways of Serratia and Rickettsiella, raises further questions on the origins of mutualisms and host–symbiont interdependencies.

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Section: Introductionmentioning

confidence: 99%

Cryptic community structure and metabolic interactions among the heritable facultative symbionts of the pea aphid

Peng,

Hoban,

Joffe

et al. 2023

Journal of Evolutionary Biology

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“…In other social Hymenoptera, larval microbiota also differ from those of adults and can play important roles. For example, in Cephalotes turtle ants, microbiota change substantially as the larvae develop (Hu et al, 2023), exhibiting a consistent successional pattern of unknown functional importance. Likewise, honeybee larval microbiota are very different from those of adult bees and can play important roles (Anderson et al, 2018; Kapheim et al, 2015; Martinson et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

Microbial symbionts are shared between ants and their associated beetles

Valdivia,

Newton,

von Beeren

et al. 2023

Environmental Microbiology

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The transmission of microbial symbionts across animal species could strongly affect their biology and evolution, but our understanding of transmission patterns and dynamics is limited. Army ants (Formicidae: Dorylinae) and their hundreds of closely associated insect guest species (myrmecophiles) can provide unique insights into interspecific microbial symbiont sharing. Here, we compared the microbiota of workers and larvae of the army ant Eciton burchellii with those of 13 myrmecophile beetle species using 16S rRNA amplicon sequencing. We found that the previously characterized specialized bacterial symbionts of army ant workers were largely absent from ant larvae and myrmecophiles, whose microbial communities were usually dominated by Rickettsia, Wolbachia, Rickettsiella and/or Weissella. Strikingly, different species of myrmecophiles and ant larvae often shared identical 16S rRNA genotypes of these common bacteria. Protein‐coding gene sequences confirmed the close relationship of Weissella strains colonizing army ant larvae, some workers and several myrmecophile species. Unexpectedly, these strains were also similar to strains infecting dissimilar animals inhabiting very different habitats: trout and whales. Together, our data show that closely interacting species can share much of their microbiota, and some versatile microbial species can inhabit and possibly transmit across a diverse range of hosts and environments.

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“…For instance, recent 16S rRNA gene-amplicon studies of microbiota of sponges and coral-reef invertebrates found significant signals of host-species specificity consistent with codiversification in multiple bacterial and archaeal families, including the Endozoicomonadaceaea, Spirochaetaceaea, and Nitrosopumilaceae (O'Brien et al, 2021;Pollock et al, 2018). Similarly, 16S rRNA gene-amplicon studies have detected evidence of co-diversification between gut bacteria and ant lineages (Hu et al, 2023).…”

Section: Signals Of Co-diversification In Complex Microbiotamentioning

confidence: 97%

Assessing co-diversification in host-associated microbiomes

Moeller,

Sanders,

Sprockett

et al. 2023

Journal of Evolutionary Biology

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When lineages of hosts and microbial symbionts engage in intimate interactions over evolutionary timescales, they can diversify in parallel (i.e., co‐diversify), producing associations between the lineages' phylogenetic histories. Tests for co‐diversification of individual microbial lineages and their hosts have been developed previously, and these have been applied to discover ancient symbioses in diverse branches of the tree of life. However, most host–microbe relationships are not binary but multipartite, in that a single host‐associated microbiota can contain many microbial lineages, generating challenges for assessing co‐diversification. Here, we review recent evidence for co‐diversification in complex microbiota, highlight the limitations of prior studies, and outline a hypothesis testing approach designed to overcome some of these limitations. We advocate for the use of microbiota‐wide scans for co‐diversifying symbiont lineages and discuss tools developed for this purpose. Tests for co‐diversification for simple host symbiont systems can be extended to entire phylogenies of microbial lineages (e.g., metagenome‐assembled or isolate genomes, amplicon sequence variants) sampled from host clades, thereby providing a means for identifying co‐diversifying symbionts present within complex microbiota. The relative ages of symbiont clades can corroborate co‐diversification, and multi‐level permutation tests can account for multiple comparisons and phylogenetic non‐independence introduced by repeated sampling of host species. Discovering co‐diversifying lineages will generate powerful opportunities for interrogating the molecular evolution and lineage turnover of ancestral, host‐species specific symbionts within host‐associated microbiota.

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Partner fidelity and environmental filtering preserve stage‐specific turtle ant gut symbioses for over 40 million years

Cited by 13 publications

References 188 publications

Cryptic community structure and metabolic interactions among the heritable facultative symbionts of the pea aphid

Cryptic community structure and metabolic interactions among the heritable facultative symbionts of the pea aphid

Microbial symbionts are shared between ants and their associated beetles

Assessing co-diversification in host-associated microbiomes

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