More effective transposon regulation in fertile, long‐lived termite queens than in sterile workers

Post, Frederik; Bornberg‐Bauer, Erich; Vasseur-Cognet, Mireille; Harrison, Mark C.

doi:10.1111/mec.16753

Cited by 6 publications

(3 citation statements)

References 51 publications

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“…In the termite Macrotermes bellicosus , TEs were found to be expressed in the heads of old workers but not in those of queens, which are much longer lived (Elsner et al., 2018). TEs were also much more active in the fat body of workers of the termite M. natalensis than in reproductive individuals (Post et al., 2023), leading to the prediction that pathway targeting TEs might be less active in non‐reproductive individuals than in reproductive individuals. We demonstrated that the non‐reproductive and regressed ovaries of nurses and foragers from queenright colonies not only have piRNAs at similar levels to those of queens, but also show ping‐pong signatures and target TEs, all of which are features of an active TE‐silencing piRNA pathway.…”

Section: Discussionmentioning

confidence: 99%

“…In the termite M. bellicosus, TE‐associated genes are upregulated and genes from piRNA pathways are downregulated in old workers with short residual lifespans, compared to long‐lived reproductives (Elsner et al., 2018). Moreover, TE expression in the fat body of the termite Macrotermes natalensis does not rise with increasing queen age, likely due to the protective upregulation of piRNA pathways in this reproductive caste with delayed ageing (Post et al., 2023). Similarly, in A. mellifera , the piRNA repertoire and expression levels are greater in reproductive individuals than in sterile workers, with the ovaries, representing the female germline, being the tissue of highest expression (Wang et al., 2017).…”

Section: Introductionmentioning

confidence: 99%

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Age‐ and caste‐independent piRNAs in the germline and miRNA profiles linked to caste and fecundity in the ant Temnothorax rugatulus

Seistrup,

Choppin,

Govind

et al. 2023

Molecular Ecology

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Social insects are models for studies of phenotypic plasticity. Ant queens and workers vary in fecundity and lifespan, which are enhanced and extended in queens. Yet, the regulatory mechanisms underlying this variation are not well understood. Ant queens live and reproduce for years, so that they need to protect their germline from transposable element (TE) activity, which may be redundant in short‐lived, often sterile workers. We analysed the expression of two protective classes of small RNAs, microRNAs (miRNAs) and Piwi‐interacting RNAs (piRNAs), in various tissues, castes and age classes of the ant Temnothorax rugatulus. In queens, piRNAs were highly abundant in ovaries with TEs being their clear targets, with reduced but still detectable piRNA‐specific ping‐pong signatures in thorax and brains. piRNA pathway activity varied little with age in queens. Moreover, the reduced ovaries of workers also exhibited similar piRNA activity and this not only in young, fertile workers, but also in older foragers with regressed ovaries. Therefore, these ants protect their germline through piRNA activity, regardless of ovarian development, age or caste, even in sterile workers often considered the soma of the superorganism. Our tissue‐specific miRNA analysis detected the expression of 304 miRNAs, of which 105 were expressed in all tissues, 10 enriched in the brain, three in the thorax, whereas 83 were ovarian‐specific. We identified ovarian miRNAs whose expression was related to caste, fecundity and age, and which likely regulate group‐specific gene expression. sRNA shifts in young‐ to middle‐aged queens were minor, suggesting delayed senescence in this reproductive caste.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Age‐ and caste‐independent piRNAs in the germline and miRNA profiles linked to caste and fecundity in the ant Temnothorax rugatulus

Seistrup,

Choppin,

Govind

et al. 2023

Molecular Ecology

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“…Since DNA integration is often linked to the activity of transposable elements (TE), this suggests an increased expression of transposable elements in individuals which show high expression of genes inside the brown module. Previous work in the social termites suggested that TEs are upregulated especially in older workers while reproductive individuals including queens show low TE activity (Elsner et al, 2018) possibly due to differences in transposon regulation (Post et al, 2023). As the DEGs in the brown module showed low expression in the parasitic treatment and conspecific treatment, this would suggest that social interactions occur more often in colonies consisting of nonrelated individuals irrespective of whether they are from the same or a different species and that this potentially has an influence on individual transposon regulation.…”

Section: Antennal Gene Expression As a Predictor Of Individual Behavi...mentioning

confidence: 99%

Brain and antennal transcriptomes of host ants reveal potential links between behaviour and the functioning of socially parasitic colonies

et al. 2023

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Insect social parasites are characterized by exploiting the hosts' social behaviour. Why exactly hosts direct their caring behaviour towards these parasites and their offspring remains largely unstudied. One hypothesis is that hosts do not perceive their social environment as altered and accept the parasitic colony as their own. We used the ant Leptothorax acervorum, host of the dulotic, obligate social parasite Harpagoxenus sublaevis, to shed light on molecular mechanisms underlying behavioural exploitation by contrasting tissue‐specific transcriptomes in young host workers. Host pupae were experimentally (re‐)introduced into fragments of their original, another conspecific, heterospecific or parasitic colony. Brain and antennal mRNA was extracted and sequenced from adult ants after they had lived in the experimental colony for at least 50 days after eclosion. The resulting transcriptomes of L. acervorum revealed that ants were indeed affected by their social environment. Host brain transcriptomes were altered by the presence of social parasites, suggesting that the parasitic environment influences brain activity, which may be linked to behavioural changes. Transcriptional activity in the antennae changed most with the presence of unrelated individuals, regardless of whether they were conspecifics or parasites. This suggests early priming of odour perception, which was further supported by sensory perception of odour as an enriched function of differentially expressed genes. Furthermore, gene expression in the antennae, but not in the brain corresponded to ant worker behaviour before sampling. Our study demonstrated that the exploitation of social behaviours by brood parasites correlates with transcriptomic alterations in the central and peripheral nervous systems.

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Termite primary queen — ancestral, but highly specialized eusocial phenotype

Hellemans,

Hanus

2024

Current Opinion in Insect Science

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More effective transposon regulation in fertile, long‐lived termite queens than in sterile workers

Cited by 6 publications

References 51 publications

Age‐ and caste‐independent piRNAs in the germline and miRNA profiles linked to caste and fecundity in the ant Temnothorax rugatulus

Age‐ and caste‐independent piRNAs in the germline and miRNA profiles linked to caste and fecundity in the ant Temnothorax rugatulus

Brain and antennal transcriptomes of host ants reveal potential links between behaviour and the functioning of socially parasitic colonies

Termite primary queen — ancestral, but highly specialized eusocial phenotype

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