Gene expression is stronger associated with behaviour than with age and fertility in ant workers

Kohlmeier, Philip; Alleman, Austin; Libbrecht, Romain; Foitzik, Susanne; Feldmeyer, Barbara

doi:10.1101/267336

Cited by 11 publications

(23 citation statements)

References 113 publications

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“…This family belongs to the Burkholderiales, which, as mentioned before, have been shown to recycle nitrogenous waste in turtle ants (Hu et al, ). Thus, metabolic differences between T. nylanderi brood carers and foragers (Kohlmeier et al, ) might explain the difference in relative abundance of Oxalobacteraceae.…”

Section: Discussionmentioning

confidence: 99%

“…Also, it is conceivable that queens have different needs with regard to nutrition than workers and thus may require different nutritional symbionts. However, even within the worker caste, individuals can differ in their physiology, as workers that perform brood care duties are often the youngest, and differ hormonally from the older workers, which take over nest defense or foraging (Kohlmeier, Alleman, Libbrecht, Foitzik, & Feldmeyer, ; Robinson, ). On top of that, outside workers, such as foragers, are more likely to come in contact with foreign bacterial strains than, for example, brood carers whose duties restrict them to the inside of the nest.…”

Section: Introductionmentioning

confidence: 99%

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Abdominal microbial communities in ants depend on colony membership rather than caste and are linked to colony productivity

Segers

Kaltenpoth

Foitzik

2019

Ecology and Evolution

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Gut bacteria aid their host in digestion and pathogen defense, and bacterial communities that differ in diversity or composition may vary in their ability to do so. Typically, the gut microbiomes of animals living in social groups converge as members share a nest environment and frequently interact. Social insect colonies, however, consist of individuals that differ in age, physiology, and behavior, traits that could affect gut communities or that expose the host to different bacteria, potentially leading to variation in the gut microbiome within colonies. Here we asked whether bacterial communities in the abdomen of Temnothorax nylanderi ants, composed largely of the gut microbiome, differ between different reproductive and behavioral castes. We compared microbiomes of queens, newly eclosed workers, brood carers, and foragers by high‐throughput 16S rRNA sequencing. Additionally, we sampled individuals from the same colonies twice, in the field and after 2 months of laboratory housing. To disentangle the effects of laboratory environment and season on microbial communities, additional colonies were collected at the same location after 2 months. There were no large differences between ant castes, although queens harbored more diverse microbial communities than workers. Instead, we found effects of colony, environment, and season on the abdominal microbiome. Interestingly, colonies with more diverse communities had produced more brood. Moreover, the queens' microbiome composition was linked to egg production. Although long‐term coevolution between social insects and gut bacteria has been repeatedly evidenced, our study is the first to find associations between abdominal microbiome characteristics and colony productivity in social insects.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Abdominal microbial communities in ants depend on colony membership rather than caste and are linked to colony productivity

Segers

Kaltenpoth

Foitzik

2019

Ecology and Evolution

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“…Our results pointed to the importance of vitellogenins (Vgs) or Vg-like genes. As these genes have been found in social hymenopterans to play additional roles that are unrelated to reproduction [61][62][63][64][65][66], we did a gene tree analysis with the aim of obtaining more information on the potential function of these genes. We inferred a maximum-likelihood gene tree that included all identified Vgs or Vg-like sequences from our six study species as well as data from the termite Z. nevadensis, the cockroach Blattella germanica and a subset of species used in Kohlmeier et al [63] (see electronic supplementary material, tables S23 and S24; details are described in the electronic supplementary material, §S1.9 and in archive S8 in Dryad [48]).…”

Section: (Ii) Vitellogenin Gene Treesmentioning

confidence: 99%

Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Korb

Meusemann

Aumer

et al. 2021

Phil. Trans. R. Soc. B

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The exceptional longevity of social insect queens despite their lifelong high fecundity remains poorly understood in ageing biology. To gain insights into the mechanisms that might underlie ageing in social insects, we compared gene expression patterns between young and old castes (both queens and workers) across different lineages of social insects (two termite, two bee and two ant species). After global analyses, we paid particular attention to genes of the insulin/insulin-like growth factor 1 signalling (IIS)/target of rapamycin (TOR)/juvenile hormone (JH) network, which is well known to regulate lifespan and the trade-off between reproduction and somatic maintenance in solitary insects. Our results reveal a major role of the downstream components and target genes of this network (e.g. JH signalling, vitellogenins, major royal jelly proteins and immune genes) in affecting ageing and the caste-specific physiology of social insects, but an apparently lesser role of the upstream IIS/TOR signalling components. Together with a growing appreciation of the importance of such downstream targets, this leads us to propose the TI–J–LiFe ( T OR/ I IS– J H– Li fespan and Fe cundity) network as a conceptual framework for understanding the mechanisms of ageing and fecundity in social insects and beyond. This article is part of the theme issue ‘Ageing and sociality: why, when and how does sociality change ageing patterns?’

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“…The positive link between these two life-history traits [15] is possibly the result of a 'rewiring' of endocrine networks. As in solitary insects, vitellogenins and vitellogenin receptors play a major role in the molecular regulation of fecundity in social insects and these yolk protein precursors also exhibit a positive effect on lifespan [8,[17][18][19]. Ant queens from single-queen societies in particular exhibit extraordinary lifespans of up to 30 years and an extremely high fecundity [20][21][22][23][24].…”

Section: Introductionmentioning

confidence: 99%

Molecular regulation of lifespan extension in fertile ant workers

Negroni

Macit

Stoldt

et al. 2021

Phil. Trans. R. Soc. B

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The evolution of sociality in insects caused a divergence in lifespan between reproductive and non-reproductive castes. Ant queens can live for decades, while most workers survive only weeks to a few years. In most organisms, longevity is traded-off with reproduction, but in social insects, these two life-history traits are positively linked. Once fertility is induced in workers, e.g. by queen removal, worker lifespan increases. The molecular regulation of this positive link between fecundity and longevity and generally the molecular underpinnings of caste-specific senescence are not well understood. Here, we investigate the transcriptomic regulation of lifespan and reproduction in fat bodies of three worker groups in the ant Temnothorax rugatulus . In a long-term experiment, workers that became fertile in the absence of the queen showed increased survival and upregulation of genes involved in longevity and fecundity pathways. Interestingly, workers that re-joined their queen after months exhibited intermediate ovary development, but retained a high expression of longevity and fecundity genes. Strikingly, the queen's presence causes a general downregulation of genes in worker fat bodies. Our findings point to long-term consequences of fertility induction in workers, even after re-joining their queen. Moreover, we reveal longevity genes and pathways modulated during insect social evolution. This article is part of the theme issue ‘Ageing and sociality: why, when and how does sociality change ageing patterns?’

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Gene expression is stronger associated with behaviour than with age and fertility in ant workers

Abstract: 19The ecological success of social insects is based on division of labour, not only between queens 20 and workers, but also among workers. Whether a worker tends the brood or forages is strongly

Cited by 11 publications

References 113 publications

Abdominal microbial communities in ants depend on colony membership rather than caste and are linked to colony productivity

Abdominal microbial communities in ants depend on colony membership rather than caste and are linked to colony productivity

Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Molecular regulation of lifespan extension in fertile ant workers

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