Function and evolution of microRNAs in eusocial Hymenoptera

Søvik, Eirik; Bloch, Guy; Ben‐Shahar, Yehuda

doi:10.3389/fgene.2015.00193

Cited by 20 publications

(19 citation statements)

References 103 publications

(126 reference statements)

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“…After filtering out RNA corresponding to potential commensal microorganisms (including the known symbiont, Blochmannia floridanus ; Supplementary file 1) and other organic food components, we detected 64 miRNAs. Forty-six of these were identified based upon their homology to miRNAs of the honey bee Apis mellifera (Guo et al, 2013; Søvik et al, 2015; Greenberg et al, 2012), while 18 sequences (bearing the structural stem-loop hallmarks of miRNA transcripts) were specific to C. floridanus (Figure 2, Figure 2—source data 1). The most abundant of the 64 miRNAs was miR-750, followed by three C. floridanus -specific microRNAs.…”

Section: Resultsmentioning

confidence: 99%

“…Unfortunately, even in Drosophila mechanisms of JH uptake by tissues are still unclear (Rodríguez-Vázquez et al, 2015; Engelmann and Mala, 2000; Suzuki et al, 2011; Parra-Peralbo and Culi, 2011). Extracellular miRNAs are secreted and transported through a variety of pathways, but the functional relevance of such molecules is still controversial (Sarkies and Miska, 2013; Turchinovich et al, 2016; Masood et al, 2016; Søvik et al, 2015; Rayner and Hennessy, 2013). …”

Section: Discussionmentioning

confidence: 99%

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Oral transfer of chemical cues, growth proteins and hormones in social insects

LeBoeuf

Waridel

Brent

et al. 2016

eLife

114

123

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Social insects frequently engage in oral fluid exchange – trophallaxis – between adults, and between adults and larvae. Although trophallaxis is widely considered a food-sharing mechanism, we hypothesized that endogenous components of this fluid might underlie a novel means of chemical communication between colony members. Through protein and small-molecule mass spectrometry and RNA sequencing, we found that trophallactic fluid in the ant Camponotus floridanus contains a set of specific digestion- and non-digestion related proteins, as well as hydrocarbons, microRNAs, and a key developmental regulator, juvenile hormone. When C. floridanus workers’ food was supplemented with this hormone, the larvae they reared via trophallaxis were twice as likely to complete metamorphosis and became larger workers. Comparison of trophallactic fluid proteins across social insect species revealed that many are regulators of growth, development and behavioral maturation. These results suggest that trophallaxis plays previously unsuspected roles in communication and enables communal control of colony phenotypes.DOI: http://dx.doi.org/10.7554/eLife.20375.001

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Oral transfer of chemical cues, growth proteins and hormones in social insects

LeBoeuf

Waridel

Brent

et al. 2016

eLife

114

123

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“…Given that these DE miRNAs are present in both hemi‐ and holometabolous insects, these miRNAs are considered to have existed in the last common ancestor of all insects. The mir‐2765 group was previously described as being a highly conserved, Hymenoptera‐specific miRNA group without any base‐pair changes (Søvik et al , ). We found orthologous miRNAs of the mir‐2765 group in termite genomes.…”

Section: Discussionmentioning

confidence: 99%

Caste‐specific microRNA expression in termites: insights into soldier differentiation

Matsunami

Nozawa

Suzuki

et al. 2018

Insect Molecular Biology

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Eusocial insects have polyphenic caste systems in which each caste exhibits characteristic morphology and behaviour. In insects, caste systems arose independently in different lineages, such as Isoptera and Hymenoptera. Although partial molecular mechanisms for the development of eusociality in termites have been clarified by the functional analysis of genes and hormones, the contribution of microRNAs (miRNAs) to caste differentiation is unknown. To understand the role of miRNAs in termite caste polyphenism, we performed small RNA sequencing in a subterranean termite (Reticulitermes speratus) and identified the miRNAs that were specifically expressed in the soldier and worker castes. Of the 550 miRNAs annotated in the R. speratus genome, 74 were conserved in insects and 174 were conserved in other termite species. We found that eight miRNAs (mir-1, mir-125, mir-133, mir-2765, mir-87a and three termite-specific miRNAs) are differentially expressed (DE) in soldiers and workers of R. speratus. This differential expression was experimentally verified for five miRNAs by real-time quantitative PCR. Further, four of the eight DE miRNAs in soldier and worker termite castes were also differentially expressed in hymenopteran castes. The finding that Isoptera and Hymenoptera shared several DE miRNAs amongst castes suggests that these miRNAs evolved independently in these phylogenetically distinct lineages.

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“…There is accumulating evidence for a role of miRNAs in regulating the social lives of insects. While most miRNAs seem to be conserved in major lineages of insects [15, 16], expression levels vary across individuals performing different social functions, such as between workers performing different tasks in honey bees [17–19]. MiRNAs may also play a role in caste determination, as queen- and worker-destined larvae express different sets of miRNAs throughout development in honey bees [20–22] and bumble bees [23].…”

Section: Introductionmentioning

confidence: 99%

“…These solitary and social species shared a common ancestor ∼75-110 mya [26]. Previous comparative studies of miRNAs associated with eusociality have relied on the parasitoid wasp, Nasonia vitripennis , as a solitary comparison [16]. This is a far more distant relative to the social insects, sharing a last common ancestor with bees nearly 200 mya [26].…”

Section: Introductionmentioning

confidence: 99%

Brain microRNAs among social and solitary bees

Kapheim

Jones

Søvik

et al. 2019

Preprint

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37Evolutionary transitions to a social lifestyle in insects are associated with lineage-specific 38 changes in gene expression, but the key nodes that drive these regulatory changes are largely 39 unknown. We tested the hypothesis that changes in gene regulation associated with social 40 evolution are facilitated by lineage-specific function of microRNAs (miRNAs). Genome scans 41 across 12 bee species showed that miRNA copy-number is mostly conserved and not associated 42 with sociality. However, deep sequencing of small RNAs in six bee species revealed a 43 substantial proportion (20-35%) of detected miRNAs had lineage-specific expression in the 44 brain, 24-72% of which did not have homologs in other species. Lineage-specific miRNAs 45 disproportionately target lineage-specific genes, and have lower expression levels than shared 46 miRNAs. The predicted targets of lineage-specific miRNAs are enriched for genes related to 47 social behavior in social species, but they are not enriched for genes under positive selection. 48Together, these results suggest that novel miRNAs may contribute to lineage-specific patterns of 49 social evolution. Our analyses also support the hypothesis that many new miRNAs are purged by 50 selection due to deleterious effects on mRNA targets, and suggest genome structure is not as 51 influential in regulating bee miRNA evolution as has been shown for mammalian miRNAs. 52 53 specific 55 56 57Eusociality has evolved several times in the hymenopteran insects. In its most basic form, 58 this lifestyle involves reproductive queens living with their worker daughters who forego direct 59 reproduction to cooperatively defend the nest, care for their siblings, and forage for the colony. 60 Due to the complex nature of this lifestyle, the evolution of eusociality likely requires 61 modification of molecular pathways related to development, behavior, neurobiology, physiology, 62 and morphology [1]. The evolution of eusociality is thus expected to involve both genetic 63 changes as well as changes in the way the genome responds to the environment [2]. It is 64therefore unsurprising that recent studies aimed at identifying the genomic signatures of eusocial 65 evolution in insects have found that social species share an increased capacity for gene regulation 66 [3,4]. Evidence for this comes from signatures of rapid evolution of genes involved in 67 transcription and translation, gene family expansions of transcription factors, and increasing 68 potential for DNA methylation and transcription factor binding activity in conserved genes. 69Interestingly, while these types of regulatory changes are common to independent origins and 70 elaborations of eusociality, the specific genes and regulatory elements involved are unique to 71 each lineage [3][4][5]. This suggests that lineage-specific processes are influential in generating new 72 patterns of gene regulation that contribute to social behavior. 73 74 Small, non-coding RNAs such as microRNAs (miRNAs) may be an important source of 75 regulatory novel...

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Function and evolution of microRNAs in eusocial Hymenoptera

Cited by 20 publications

References 103 publications

Oral transfer of chemical cues, growth proteins and hormones in social insects

Oral transfer of chemical cues, growth proteins and hormones in social insects

Caste‐specific microRNA expression in termites: insights into soldier differentiation

Brain microRNAs among social and solitary bees

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