Convergent evolution of a labile nutritional symbiosis in ants

Jackson, Raphaella; Monnin, David; Patapiou, Patapios A.; Golding, Gemma; Helanterä, Heikki; Oettler, Jan; Heınze, Jürgen; Wurm, Yannick; Economou, Chloe K.; Chapuisat, Michel; Henry, Lee M.

doi:10.1038/s41396-022-01256-1

Cited by 19 publications

(40 citation statements)

References 83 publications

(100 reference statements)

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“…The cross-fostering experiments confirmed that Blochmannia is relevant for brood development, since brood with reduced Blochmannia titers had a higher egg mortality and slower development rate than brood containing endosymbionts (e.g. (1,16,30)) In particular, these endosymbionts selectively regulate germline genes in early development stages of their hosts to successfully integrate Blochmannia into the Camponotini ants and facilitate the horizontal transfer and biosynthesis pathways (19,24,32). By contrast, the frequency of Blochmannia decreases in older workers and the endosymbionts seem to play a minor role for adult ants (30).…”

Section: Discussionmentioning

confidence: 69%

“…(i) Blochmannia provides access to nutrients necessary for host development (22)(23)(24), while the ants bacteriocytes provide their endosymbionts with a protected environment (16,(26)(27)(28).…”

Section: Discussionmentioning

confidence: 99%

“…The Blochmannia genome contains genes for biosynthesis pathways for essential amino acids (except arginine) necessary for the host's development, especially for sclerotization, recycling of ammonia, and sulfate reduction (22)(23)(24). In contrast, biosynthesis pathways for non-essential amino acids have been lost (20,(23)(24)(25).…”

Section: Introductionmentioning

confidence: 99%

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Blochmanniaendosymbionts reduce brood rearing success in a carpenter ant (Camponotussp.)

Preuss

Czuppon

Ernst

et al. 2022

Preprint

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All ants of the species rich genus Camponotus (carpenter ants) possess the obligate intracellular bacterial mutualist Blochmannia. We tested the relevance of the endosymbiont Blochmannia for offspring rearing using cross-fostering experiments between Camponotus sp. colonies and subcolonies (worker groups), which were either treated with antibiotics to remove Blochmannia or untreated. Our antibiotic treatment reduced the level of Blochmannia endosymbionts in eggs, larvae and workers significantly. Corroborating previous results, we found that eggs from treated colonies had a significantly reduced probability to develop into larvae and almost zero probability to become adults. Surprisingly, subcolonies treated with antibiotics had a significantly higher success in raising their own and foreign eggs from treated and untreated colonies than untreated subcolonies. This might indicate that the Blochmannia symbiosis entails significant costs for the host in terms of brood rearing, i.e., symbiont-free workers are more successful in brood rearing than untreated workers. If confirmed, this would be a rare case where the costs of a symbiosis can be empirically measured and quantified. Alternatively, the antibiotic treatment increased as a side effect the brood rearing effort of workers leading to the differences in brood rearing success of treated workers. But even if that would be the case, it still indicates that workers that have either lost or have a significantly reduced number of endosymbionts can still raise brood from antibiotic treated and untreated colonies better than untreated workers. Thus Blochmannia, although crucial for brood development, may reduce the amount of brood a colony can raise.

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Section: Discussionmentioning

confidence: 69%

Section: Discussionmentioning

confidence: 99%

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Blochmanniaendosymbionts reduce brood rearing success in a carpenter ant (Camponotussp.)

Preuss

Czuppon

Ernst

et al. 2022

Preprint

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“…Westeberhardia cardiocondylae, an endosymbiont with a highly reduced genome that resides in gut-associated bacteriomes, as well as in ovaries in queens [34]. Cardiocondyla minutior carries the symbiont [35] but does not display caste-specific patterns, while a C. obscurior lineage that is naturally free of Cand . Westeberhardia [34,36] and has been maintained in the lab since 2011 shows the patterns (Schultner, pers.…”

Section: Resultsmentioning

confidence: 99%

Maternal control over caste allocation in the ant Cardiocondyla obscurior

Wallner

Schultner

Oettler

2021

Preprint

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Social insects are interesting models for the study of anticipatory developmental plasticity because of the striking differentiation into reproductive queens and functionally sterile workers. A few ant genera, including Cardiocondyla, represent the pinnacle of social evolution in the Hymenoptera, where workers have completely lost their reproductive organs, minimizing reproductive conflicts between queens and workers. Here we show that late embryos and larvae of queens of the ant C. obscurior can be identified by the appearance of urate deposits around the forming ovaries. The discovery of caste-specific urate patterns in C. obscurior and three additional Cardiocondyla species will facilitate future studies of developmental plasticity in ants.

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“…In addition, methylation mediated by endosymbiont has been shown as a regulator of the expression of key host genes in bacteriocytes, which affect aphid hosts' selection of plants for feeding (Kim et al, 2018). Some specific examples of amino acid complementation include i) The aphid host which may play a role in biosynthesizing and thus regulating ornithine for Buchnera, whereas many Buchnera taxa have lost the genes responsible for ornithine biosynthesis (Hansen and Moran, 2014), ii) The case of B. tabaci populations from Asia, where several endosymbiont genomes sampled have lost major components of the vitamin B biosynthesis pathways, and presumably, the host supplements these to the endosymbiont (Zhu et al, 2022), iii) A recent study proving that the only metabolic function consistently retained in symbiont genomes of ants that have cellular endosymbionts, namely Camponotus, Plagiolepis, Formica, and Cardiocondyla, is the capacity to synthesise tyrosine implying that they supplement the host amino acid deficiency (Jackson et al, 2022).…”

Section: Molecular Interactions Between Endosymbionts and Hostsmentioning

confidence: 99%

Evolution and ontogeny of bacteriocytes in insects

Alarcón

Polo²,

Akyüz³

et al. 2022

Front. Physiol.

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The ontogenetic origins of the bacteriocytes, which are cells that harbour bacterial intracellular endosymbionts in multicellular animals, are unknown. During embryonic development, a series of morphological and transcriptional changes determine the fate of distinct cell types. The ontogeny of bacteriocytes is intimately linked with the evolutionary transition of endosymbionts from an extracellular to an intracellular environment, which in turn is linked to the diet of the host insect. Here we review the evolution and development of bacteriocytes in insects. We first classify the endosymbiotic occupants of bacteriocytes, highlighting the complex challenges they pose to the host. Then, we recall the historical account of the discovery of bacteriocytes. We then summarize the molecular interactions between the endosymbiont and the host. In addition, we illustrate the genetic contexts in which the bacteriocytes develop, with examples of the genetic changes in the hosts and endosymbionts, during specific endosymbiotic associations. We finally address the evolutionary origin as well as the putative ontogenetic or developmental source of bacteriocytes in insects.

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Convergent evolution of a labile nutritional symbiosis in ants

Cited by 19 publications

References 83 publications

Blochmanniaendosymbionts reduce brood rearing success in a carpenter ant (Camponotussp.)

Blochmanniaendosymbionts reduce brood rearing success in a carpenter ant (Camponotussp.)

Maternal control over caste allocation in the ant Cardiocondyla obscurior

Evolution and ontogeny of bacteriocytes in insects

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