Methyl farnesoate epoxidase (mfe) gene expression and juvenile hormone titers in the life cycle of a highly eusocial stingless bee, Melipona scutellaris

Cardoso-Júnior, Carlos Antônio Mendes; Silva, Renato Pereira; Borges, Naiara Araújo; Carvalho, Wender Santana; Wälter, Stephanie; Simões, Zilá Luz Paulino; Bitondi, Márcia Maria Gentile; Vieira, Carlos Ueira; Bonetti, Ana Maria; Hartfelder, Klaus

doi:10.1016/j.jinsphys.2017.08.001

Cited by 27 publications

(30 citation statements)

References 65 publications

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“…For T. angustula we found supporting evidence of the involvement of vg in nursing behaviour, nonetheless JH genes were not highly expressed in foragers. This supports the hypothesis that in stingless bees the typical vg/ JH double repressor network observed in honeybees is also not functional, and vg is distinctly regulated 32,38 .…”

Section: Discussionsupporting

confidence: 87%

Multiple lineages, same molecular basis: task specialization is commonly regulated across all eusocial bee groups

Araujo

Arias

2020

Preprint

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14A striking feature of advanced insect societies is the existence of workers that forgo 15 reproduction. Two broad types of workers exist in eusocial bees: nurses which care 16 for their young siblings and the queen, and foragers who guard the nest and forage for 17 food. Comparisons between this two worker subcastes have been performed in 18 honeybees, but data from other bees are scarce. To understand whether similar 19 molecular mechanisms are involved in nurse-forager differences across distinct 20 species, we compared gene expression and DNA methylation profiles between nurses 21 and foragers of the buff-tailed bumblebee Bombus terrestris and of the stingless bee 22Tetragonisca angustula. These datasets were then discussed comparatively to 23 previous findings on honeybees. Our analyses revealed that although the expression 24 pattern of genes is often species-specific, many of the biological processes and 25 molecular pathways involved are common. Moreover, DNA methylation and gene 26 expression correlation were dependent on the nucleotide context. 27 subcastes evolved it is necessary to differentiate such more recent changes -that 53 could be species-specific -from those shared across species, and thus likely ancestral. 54The highly eusocial stingless bees have age-based division of labour 18 , similarly to 55 that of honeybees despite their most common ancestor being 50 to 80 million years 56 ago 19,20 . To date, no global expression or epigenetic studies have been performed in 57 stingless bees to understand worker task specialization. Similarly, while primitively 58 eusocial bumblebees are largely studied ecological biological models and important 59 wild and managed pollinators, we know comparatively little about the molecular 60 underpinnings of differences between its worker subcastes. Indeed, studies have been 61 restricted to few genes, leaving many open questions [21][22][23] . A major limiting element 62 for these studies is that this species display a somewhat fluctuating division of labour 63 with indistinctive separation between subcastes 10,21,23 . 64We aim to fill in this knowledge gap through the analyses of the global gene 65 expression differences between nurses and foragers, and the characterization of nurses 66 DNA methylation profile in two eusocial bee species, the primitively eusocial buff-67 tailed bumblebee, Bombus terrestris, and the highly eusocial stingless bee, 68Tetragonisca angustula. Combined, these two bee species and the honeybee represent 69 the three evolutionary branches of eusocial corbiculates sharing a common social 70 origin 24 . Hence, in addition to using the generated datasets to uncover unique and 71 more recent molecular traits linked to task division in B. terrestris and T. angustula, 72 we also verified whether common genes and pathways could be involved in task 73 specialization across all the eusocial bee groups. 74 75Results 76 task-dependent foraging gene expression in the bumblebee Bombus terrestris. Arch. Insect

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Section: Discussionsupporting

confidence: 87%

Multiple lineages, same molecular basis: task specialization is commonly regulated across all eusocial bee groups

Araujo

Arias

2020

Preprint

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“…Moreover, downstream analyses (e.g., GO term enrichment, gene network analyses and metabolic pathway comparisons) will also be affected, possibly leading to wrong conclusions. The use of age‐confounded data sets might therefore have contributed to the lack of consensus on clear transcriptomic patterns of worker specialized on different behaviours, as many studies investigating gene expression in different behavioural castes did not control for age and fertility (Cardoso‐Júnior et al, ; Feldmeyer et al, ; Ingram et al, ; Johnson & Jasper, ; Khamis et al, ; Manfredini et al, ; Qiu et al, ; Scheiner, Entler, et al, ; Scheiner, Reim, et al, ; Zhao et al, ). Similar conclusions were recently drawn from a gene expression comparison between queens and workers, as uncontrolled variation was added by confounding age when comparing gene expression between castes (Lucas et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…The inconsistency across studies in the association between gene expression and worker task choice may reflect species‐specific mechanisms regulating behavioural specialization or differences across studies regarding experimental design. Gene expression patterns associated with behavioural specialization of workers are typically identified by comparing brood carers and foragers that not only differ in behaviour but also in age and fertility (Cardoso‐Júnior et al, ; Feldmeyer et al, ; Ingram et al, ; Johnson & Jasper, ; Khamis et al, ; Manfredini et al, ; Qiu et al, ; Scheiner, Entler, Barron, Scholl, & Thamm, ; Zhao et al, ), two factors that are linked to gene expression (Alaux et al, ; Feldmeyer et al, ; Harrison, Hammond, & Mallon, ; Lucas, Romiguier, & Keller, ; Nilsen et al, ; Whitfield, Cziko, & Robinson, ). Not experimentally controlling for age or fertility (in species with potentially fertile workers) when contrasting brood carer and forager transcriptomes could thus lead to confounded data sets and the identification of transcriptomic patterns being linked to any of the three factors or combinations thereof.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2019

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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 characterized by an upregulation of three Vitellogenin (Vg) genes, one of which, Vg‐like A, was the most differentially expressed gene that was recently shown experimentally to control the switch from brood to worker care. The expression of Conventional Vg was unlinked to behavioural specialization, age or fertility, which contrasts to studies on bees and some ants. Diversity in Vg/Vg‐like copy number and expression bias across ants supports subfunctionalization of Vg genes and indicates that some regulatory mechanisms of division of labour diverged in different ant lineages. Simulations revealed that our experimental dissociation of co‐varying factors reduced transcriptomic noise, suggesting that confounding factors could potentially explain inconsistencies across transcriptomic studies of behavioural specialization in ants. Thus, our study reveals that worker gene expression is mainly linked to the worker's function for the colony and provides novel insights into the evolution of sociality in ants.

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“…The use of age confounded datasets might therefore have contributed to the lack of consensus on clear transcriptomic patterns of worker behaviour, as many studies investigating gene expression in different behavioural castes did not control for age and fertility [e.g. 28,31,56,57,69–73]. Similar conclusions were recently drawn from a gene expression comparison between queens and workers, as uncontrolled variation was added by confounding age when comparing gene expression between both castes [68].…”

Section: Discussionmentioning

confidence: 99%

“…As age and fertility additionally influence gene expression [22,28,67,68], studies that did not experimentally control for age and physiology when comparing gene expression between brood carers and foragers [e.g. 28,31,46,56,57,69–73] might have produced results driven not only by behaviour, but also by age and fertility. Such confounded transcriptomic analyses are not a problem specific to research on insect behaviour but occur across study systems and contexts.…”

Section: Introductionmentioning

confidence: 99%

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

Kohlmeier

Alleman

Libbrecht

et al. 2018

Preprint

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Methyl farnesoate epoxidase (mfe) gene expression and juvenile hormone titers in the life cycle of a highly eusocial stingless bee, Melipona scutellaris

Cited by 27 publications

References 65 publications

Multiple lineages, same molecular basis: task specialization is commonly regulated across all eusocial bee groups

Multiple lineages, same molecular basis: task specialization is commonly regulated across all eusocial bee groups

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

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

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