0000000000235013

AUTHOR

Romain Libbrecht

0000-0003-4397-000x

Supplementary TextS26 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

This Supplement includes Supplementary Methods and Results; Table S4; List of Captions for Supplementary Tables and Supplementary Figures; List of Supplementary Archives deposited at DRYAD and Supplementary References.

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Social regulation of insulin signaling and the evolution of eusociality in ants

The benefits of being well fed In eusocial insects, the vast majority of individuals sacrifice their reproductive potential to support the reproductive queen. Although this system has evolved repeatedly, there is still much debate surrounding its origin. Working with seven different species of ants, Chandra et al. used a transcriptomic approach to show that a single gene is consistently up-regulated in queens. This gene seems to confer reproductive status through integration with increased nutrition. In a clonal ant, larval signals disrupt this gene up-regulation, destabilizing the division of reproductive labor. Increasing levels of the associated peptide override these larval signals and …

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Gene expression is more strongly associated with behavioural specialization than with age or fertility in ant workers.

The ecological success of social insects is based on division of labour, not only between queens and workers, but also among workers. Whether a worker tends the brood or forages is influenced by age, fertility and nutritional status, with brood carers being younger, more fecund and more corpulent. Here, we experimentally disentangle behavioural specialization from age and fertility in Temnothorax longispinosus ant workers and analyse how these parameters are linked to whole-body gene expression. A total of 3,644 genes were associated with behavioural specialization which is ten times more than associated with age and 50 times more than associated with fertility. Brood carers were characteri…

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Time course analysis of the brain transcriptome during transitions between brood care and reproduction in the clonal raider ant

AbstractDivision of labor between reproductive queens and non-reproductive workers that perform brood care is the hallmark of insect societies. However, the molecular basis of this fundamental dichotomy remains poorly understood, in part because the caste of an individual cannot typically be experimentally manipulated at the adult stage. Here we take advantage of the unique biology of the clonal raider ant,Ooceraea biroi, where reproduction and brood care behavior can be experimentally manipulated in adults. To study the molecular regulation of reproduction and brood care, we induced transitions between both states, and monitored brain gene expression at multiple time points. We found that …

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Experimental increase of worker diversity benefits brood production in ants

Background The reproductive division of labor of eusocial insects, whereby one or several queens monopolize reproduction, evolved in a context of high genetic relatedness. However, many extant eusocial species have developed strategies that decrease genetic relatedness in their colonies, suggesting some benefits of the increased diversity. Multiple studies support this hypothesis by showing positive correlations between genetic diversity and colony fitness, as well as finding effects of experimental manipulations of diversity on colony performance. However, alternative explanations could account for most of these reports, and the benefits of diversity on performance in eusocial insects stil…

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Supplementary Information from Oxidative stress and senescence in social insects—a significant but inconsistent link?

Additional methods tables and figures

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Offspring reverse transcriptome responses to maternal deprivation when reared with pathogens in an insect with facultative family life

Offspring of species with facultative family life are able to live with and without parents (i.e. to adjust to extreme changes in their social environment). While these adjustments are well understood on a phenotypic level, their genetic underpinnings remain surprisingly understudied. Investigating gene expression changes in response to parental absence may elucidate the genetic constraints driving evolutionary transitions between solitary and family life. Here, we manipulated maternal presence to observe gene expression changes in the fat body of juvenile European earwigs, an insect with facultative family life. Because parents typically protect offspring against pathogens, expression chan…

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

AbstractThe ecological success of social insects is based on division of labour, not only between queens and workers, but also among workers. Whether a worker tends the brood or forages is strongly influenced by age, fertility and nutritional status, with brood carers being younger, more fecund and corpulent. Here, we experimentally disentangle behaviour from age and fertility inTemnothorax longispinosusant workers and analyse how these parameters are linked to whole-body gene expression. Our transcriptome analysis reveals four times more genes associated with behaviour than with age and only few fertility-associated genes. Brood carers exhibited an upregulation of genes involved in lipid b…

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Genetics and Evolution of Social Behavior in Insects

The study of insect social behavior has offered tremendous insight into the molecular mechanisms mediating behavioral and phenotypic plasticity. Genomic applications to the study of eusocial insect species, in particular, have led to several hypotheses for the processes underlying the molecular evolution of behavior. Advances in understanding the genetic control of social organization have also been made, suggesting an important role for supergenes in the evolution of divergent behavioral phenotypes. Intensive study of social phenotypes across species has revealed that behavior and caste are controlled by an interaction between genetic and environmentally mediated effects and, further, tha…

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Supplementary Table1: ANOVA II results from Queen loss increases worker survival in leaf-cutting ants under paraquat-induced oxidative stress

Longevity is traded off with fecundity in most solitary species, but the two traits are positively linked in social insects. The most fecund individuals (queens and kings) live longer than the non-reproductive individuals, the workers. In many species, workers may become fertile following queen loss, and recent evidence suggests that worker fecundity extends worker lifespan. We postulated that this effect is in part due to improved resilience to oxidative stress, and tested this hypothesis in three Myrmicine ants: Temnothorax rugatulus, and the leaf-cutting ants Atta colombica and Acromyrmex echinatior. We removed the queen from colonies to induce worker reproduction and subjected workers t…

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

This supplement includes Supplementary Figure S1-S17.

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Queen loss increases worker survival in leaf-cutting ants under paraquat-induced oxidative stress

Longevity is traded off with fecundity in most solitary species, but the two traits are positively linked in social insects. In ants, the most fecund individuals (queens and kings) live longer than the non-reproductive individuals, the workers. In many species, workers may become fertile following queen loss, and recent evidence suggests that worker fecundity extends worker lifespan. We postulated that this effect is in part owing to improved resilience to oxidative stress, and tested this hypothesis in three Myrmicine ants: Temnothorax rugatulus, and the leaf-cutting ants Atta colombica and Acromyrmex echinatior . We removed the queen from colonies to induce worker reproduction and subjec…

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

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…

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Fecundity determines the outcome of founding queen associations in ants

AbstractAnimal cooperation evolved because of its benefits to the cooperators. Pleometrosis in ants - the cooperation of queens to found a colony - benefits colony growth, but also incurs costs for some of the cooperators because only one queen usually survives the association. While several traits are associated with queen survival, they tend to be confounded and it is unclear which factor specifically determines the outcome of pleometrosis. In this study, we used the ant Lasius niger to monitor offspring production in colonies founded by one or two queens. Then, we experimentally paired queens that differed in fecundity but not in size, and vice versa, to disentangle the effect of these f…

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Oxidative stress and senescence in social insects: A significant but inconsistent link?

The life-prolonging effects of antioxidants have long entered popular culture, but the scientific community still debates whether free radicals and the resulting oxidative stress negatively affect longevity. Social insects are intriguing models for analysing the relationship between oxidative stress and senescence because life histories differ vastly between long-lived reproductives and the genetically similar but short-lived workers. Here, we present the results of an experiment on the accumulation of oxidative damage to proteins, and a comparative analysis of the expression of 20 selected genes commonly involved in managing oxidative damage, across four species of social insects: a termit…

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Back to the roots: the importance of using simple insect societies to understand the molecular basis of complex social life

The evolutionary trajectories toward insect eusociality come in two broad forms. In species like wasps, bees, and ants, the first helpers remained at the nest primarily to help with brood care. In species like aphids and termites, on the other hand, nest defense was initially the primary ecological driving force. To better understand the molecular basis of these two alternative evolutionary trajectories, it is therefore important to study the mechanistic basis of brood care and nest defense behavior. So far, most studies have compared morphologically distinct castes in advanced eusocial species of ants, bees, wasps, and termites. However, the interpretation of such comparisons is limited by…

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A Role of Histone Acetylation in the Regulation of Circadian Rhythm in Ants

Summary In many organisms, circadian rhythms and associated oscillations in gene expression are controlled by post-translational modifications of histone proteins. Although epigenetic mechanisms influence key aspects of insect societies, their implication in regulating circadian rhythms has not been studied in social insects. Here we ask whether histone acetylation plays a role in adjusting circadian activity in the ant Temnothorax longispinosus. We characterized activity patterns in 20 colonies to reveal that these ants exhibit a diurnal rhythm in colony-level activity and can rapidly respond to changes in the light regime. Then we fed T. longispinosus colonies with C646, a chemical inhibi…

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Social isolation causes downregulation of immune and stress response genes and behavioural changes in a social insect

Humans and other social mammals experience isolation from their group as stressful, triggering behavioural and physiological anomalies that reduce fitness. While social isolation has been intensely studied in social mammals, it is less clear how social insects, which evolved sociality independently, respond to isolation. Here we examined whether the typical mammalian responses to social isolation, e.g., an impaired ability to interact socially and immune suppression are also found in social insects. We studied the consequences of social isolation on behaviour and brain gene expression in the ant Temnothorax nylanderi. Following isolation, workers interacted moderately less with adult nestma…

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Table S5 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Table S1 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM 1.

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Data from: Gene expression is more strongly associated with behavioural specialisation than with age or fertility in ant workers

The ecological success of social insects is based on division of labour, not only between queens and workers, but also among workers. Whether a worker tends the brood or forages is influenced by age, fertility and nutritional status, with brood carers being younger, more fecund and more corpulent. Here, we experimentally disentangle behavioural specialisation from age and fertility in Temnothorax longispinosus ant workers and analyse how these parameters are linked to whole-body gene expression. A total of 3644 genes were associated with behavioural specialisation which is ten times more than associated with age and 50 times more than associated with fertility. Brood carers were characteriz…

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Table S16 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Table S6 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Table S20 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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R script survival analysis from Queen loss increases worker survival in leaf-cutting ants under paraquat-induced oxidative stress

Longevity is traded off with fecundity in most solitary species, but the two traits are positively linked in social insects. The most fecund individuals (queens and kings) live longer than the non-reproductive individuals, the workers. In many species, workers may become fertile following queen loss, and recent evidence suggests that worker fecundity extends worker lifespan. We postulated that this effect is in part due to improved resilience to oxidative stress, and tested this hypothesis in three Myrmicine ants: Temnothorax rugatulus, and the leaf-cutting ants Atta colombica and Acromyrmex echinatior. We removed the queen from colonies to induce worker reproduction and subjected workers t…

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Table S12 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Table S3 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Table S10 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Table S26 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Table S24 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Ox stress Bayes from Oxidative stress and senescence in social insects—a significant but inconsistent link?

zip file containing the original data, the r-script and the r-save files.

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Table S3 from Oxidative stress and senescence in social insects—a significant but inconsistent link?

Details of genes identified in our four study species following Corona and colleagues (Corona et al. 2006).

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Table S5 A, B, C from Oxidative stress and senescence in social insects—a significant but inconsistent link?

Correlation and p-values between the 20 antioxidant genes; PC axis that separated castes in C. secundus, A. mellifera capensis and E. viridissima; PC axis that separated young and old individuals of P. punctata and E. viridissima.

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Table S15 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Table S19 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Table S4 A, B from Oxidative stress and senescence in social insects—a significant but inconsistent link?

Genes unambiguously identified in our study species; Normalised read counts identified in our study species

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Table S2 from Oxidative stress and senescence in social insects—a significant but inconsistent link?

Genes involved in the enzymatic antioxidant system following Corona and Robinson (2006) identified in Apis, Anopheles and/or Drosophila.

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Table S7 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Table S11 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Table S2 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Table S17 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Figure S1 from Offspring reverse transcriptome responses to maternal deprivation when reared with pathogens in an insect with facultative family life

Genes affected by the presence of the pathogen, independently of maternal presence. Y-axis represents normalized expression across samples per gene (Z-Score).

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Table S21 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Table S23 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Table S25 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Raw data A.echinatior from Queen loss increases worker survival in leaf-cutting ants under paraquat-induced oxidative stress

Longevity is traded off with fecundity in most solitary species, but the two traits are positively linked in social insects. The most fecund individuals (queens and kings) live longer than the non-reproductive individuals, the workers. In many species, workers may become fertile following queen loss, and recent evidence suggests that worker fecundity extends worker lifespan. We postulated that this effect is in part due to improved resilience to oxidative stress, and tested this hypothesis in three Myrmicine ants: Temnothorax rugatulus, and the leaf-cutting ants Atta colombica and Acromyrmex echinatior. We removed the queen from colonies to induce worker reproduction and subjected workers t…

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Table S13 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Table S9 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Raw dat A. colombica from Queen loss increases worker survival in leaf-cutting ants under paraquat-induced oxidative stress

Longevity is traded off with fecundity in most solitary species, but the two traits are positively linked in social insects. The most fecund individuals (queens and kings) live longer than the non-reproductive individuals, the workers. In many species, workers may become fertile following queen loss, and recent evidence suggests that worker fecundity extends worker lifespan. We postulated that this effect is in part due to improved resilience to oxidative stress, and tested this hypothesis in three Myrmicine ants: Temnothorax rugatulus, and the leaf-cutting ants Atta colombica and Acromyrmex echinatior. We removed the queen from colonies to induce worker reproduction and subjected workers t…

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Table S22 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Table S18 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Table S8 from Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

Overview of all Supplementary tables provided as separate Excel files, except Table S4 which is included in ESM1.

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Tables S1 & S2 from Offspring reverse transcriptome responses to maternal deprivation when reared with pathogens in an insect with facultative family life

Table S1. Comparisons of different transcriptome assemblies. The table on the sheet "Transrate output" shows data obtained using Transrate v.1.03 (Smith-unna et al., 2016). We compared assemblies created using Trinity and CLC Assembly Cell, as well as a merged "hybrid" obtained using CAP3 (Huang and Madan, 1999). The assembly comparison was used to determine the best assembly for continued analyses. Table S2. Full list of all DEGs revealed by the LRTs testing for main and interaction effects, as well as the associated annotations and read counts per sample. Note that no DEGs depended on maternal presence alone. Table headers are default DEseq2 headers, while the Blast annotation was added b…

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Raw data T. rugatulus from Queen loss increases worker survival in leaf-cutting ants under paraquat-induced oxidative stress

Longevity is traded off with fecundity in most solitary species, but the two traits are positively linked in social insects. The most fecund individuals (queens and kings) live longer than the non-reproductive individuals, the workers. In many species, workers may become fertile following queen loss, and recent evidence suggests that worker fecundity extends worker lifespan. We postulated that this effect is in part due to improved resilience to oxidative stress, and tested this hypothesis in three Myrmicine ants: Temnothorax rugatulus, and the leaf-cutting ants Atta colombica and Acromyrmex echinatior. We removed the queen from colonies to induce worker reproduction and subjected workers t…

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