Insect life history and the evolution of bacterial mutualism

Henry, Lee M.; Maiden, Martin C. J.; Ferrari, Julia; Godfray, H. Charles J.

doi:10.1111/ele.12425

Cited by 152 publications

(245 citation statements)

References 45 publications

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“…Two potential ecological pathways for microbes to be shared between ants and scale insects are: (i) if the ants are 'farming' the scale insects for meat, or (ii) if these bacteria are passed to the ants in low abundance via scale-insect honeydew, as has been shown for some gut-associated bacteria in aphids [15]. This kind of trophic microbial sharing could have nutritional or other effects on the consumers in ant -plant -hemipteran interactions [17].…”

Section: ) Ellipses Indicate 80% Confidence Intervals (Ci)mentioning

confidence: 99%

Community analysis of microbial sharing and specialization in a Costa Rican ant–plant–hemipteran symbiosis

Pringle

Moreau

2017

Proc. R. Soc. B.

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Ants have long been renowned for their intimate mutualisms with trophobionts and plants and more recently appreciated for their widespread and diverse interactions with microbes. An open question in symbiosis research is the extent to which environmental influence, including the exchange of microbes between interacting macroorganisms, affects the composition and function of symbiotic microbial communities. Here we approached this question by investigating symbiosis within symbiosis. Ant–plant–hemipteran symbioses are hallmarks of tropical ecosystems that produce persistent close contact among the macroorganism partners, which then have substantial opportunity to exchange symbiotic microbes. We used metabarcoding and quantitative PCR to examine community structure of both bacteria and fungi in a Neotropical ant–plant–scale-insect symbiosis. Both phloem-feeding scale insects and honeydew-feeding ants make use of microbial symbionts to subsist on phloem-derived diets of suboptimal nutritional quality. Among the insects examined here, Cephalotes ants and pseudococcid scale insects had the most specialized bacterial symbionts, whereas Azteca ants appeared to consume or associate with more fungi than bacteria, and coccid scale insects were associated with unusually diverse bacterial communities. Despite these differences, we also identified apparent sharing of microbes among the macro-partners. How microbial exchanges affect the consumer-resource interactions that shape the evolution of ant–plant–hemipteran symbioses is an exciting question that awaits further research.

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Section: ) Ellipses Indicate 80% Confidence Intervals (Ci)mentioning

confidence: 99%

Community analysis of microbial sharing and specialization in a Costa Rican ant–plant–hemipteran symbiosis

Pringle

Moreau

2017

Proc. R. Soc. B.

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“…; Oliver & Martinez ; Henry et al . ). However, because obligate nutritional symbioses remain more stable over evolutionary times than facultative ones, investigating the ecological factors that govern obligate symbiont turnover requires a wide taxonomic coverage and a solid phylogenetic framework.…”

Section: Introductionmentioning

confidence: 97%

Buchnera has changed flatmate but the repeated replacement of co‐obligate symbionts is not associated with the ecological expansions of their aphid hosts

et al. 2016

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Symbiotic associations with bacteria have facilitated important evolutionary transitions in insects and resulted in long-term obligate interactions. Recent evidence suggests that these associations are not always evolutionarily stable and that symbiont replacement, and/or supplementation of an obligate symbiosis by an additional bacterium, has occurred during the history of many insect groups. Yet, the factors favouring one symbiont over another in this evolutionary dynamic are not well understood; progress has been hindered by our incomplete understanding of the distribution of symbionts across phylogenetic and ecological contexts. While many aphids are engaged into an obligate symbiosis with a single Gammaproteobacterium, Buchnera aphidicola, in species of the Lachninae subfamily, this relationship has evolved into a 'ménage à trois', in which Buchnera is complemented by a cosymbiont, usually Serratia symbiotica. Using deep sequencing of 16S rRNA bacterial genes from 128 species of Cinara (the most diverse Lachninae genus), we reveal a highly dynamic dual symbiotic system in this aphid lineage. Most species host both Serratia and Buchnera but, in several clades, endosymbionts related to Sodalis, Erwinia or an unnamed member of the Enterobacteriaceae have replaced Serratia. Endosymbiont genome sequences from four aphid species confirm that these coresident symbionts fulfil essential metabolic functions not ensured by Buchnera. We further demonstrate through comparative phylogenetic analyses that cosymbiont replacement is not associated with the adaptation of aphids to new ecological conditions. We propose that symbiont succession was driven by factors intrinsic to the phenomenon of endosymbiosis, such as rapid genome deterioration or competitive interactions between bacteria with similar metabolic capabilities.

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“…If two symbionts provide the same service, then one of them might be redundant and thus too costly to the host. This may be the reason why defensive bacterial symbionts are less frequent in aphids protected by ants (Henry, Maiden, Ferrari, & Godfray, ), or why the two defensive symbionts Serratia symbiotica and Hamiltonella defensa rarely co‐occur in pea aphids (Oliver, Moran, & Hunter, ). Also, interactive effects between symbionts make the outcome of a given association difficult to predict.…”

Section: Introductionmentioning

confidence: 99%

Nonrandom associations of maternally transmitted symbionts in insects: The roles of drift versus biased cotransmission and selection

et al. 2019

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Virtually all higher organisms form holobionts with associated microbiota. To understand the biology of holobionts we need to know how species assemble and interact. Controlled experiments are suited to study interactions between particular symbionts, but they only accommodate a tiny portion of the diversity within each species. Alternatively, interactions can be inferred by testing if associations among symbionts in the field are more or less frequent than expected under random assortment. However, random assortment may not be a valid null hypothesis for maternally transmitted symbionts since drift alone can result in associations. Here, we analyse a European field survey of endosymbionts in pea aphids (Acyrthosiphon pisum), confirming that symbiont associations are pervasive. To interpret them, we develop a model simulating the effect of drift on symbiont associations. We show that drift induces apparently nonrandom assortment, even though horizontal transmissions and maternal transmission failures tend to randomise symbiont associations. We also use this model in the approximate Bayesian computation framework to revisit the association between Spiroplasma and Wolbachia in Drosophila neotestacea. New field data reported here reveal that this association has disappeared in the investigated location, yet a significant interaction between Spiroplasma and Wolbachia can still be inferred. Our study confirms that negative and positive associations are pervasive and often induced by symbiont‐symbiont interactions. Nevertheless, some associations are also likely to be driven by drift. This possibility needs to be considered when performing such analyses, and our model is helpful for this purpose.

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Insect life history and the evolution of bacterial mutualism

Cited by 152 publications

References 45 publications

Community analysis of microbial sharing and specialization in a Costa Rican ant–plant–hemipteran symbiosis

Community analysis of microbial sharing and specialization in a Costa Rican ant–plant–hemipteran symbiosis

Buchnera has changed flatmate but the repeated replacement of co‐obligate symbionts is not associated with the ecological expansions of their aphid hosts

Nonrandom associations of maternally transmitted symbionts in insects: The roles of drift versus biased cotransmission and selection

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