Diet and Cell Size Both Affect Queen-Worker Differentiation through DNA Methylation in Honey Bees (Apis mellifera, Apidae)

Shi, Yuan; Zhi, Huang; Zeng, Zhi; Wang, Zi Long; Wu, Xiao; Yan, Wei

doi:10.1371/journal.pone.0018808

Cited by 83 publications

(77 citation statements)

References 13 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The sequencing of more species with different levels of plasticity and multiple phenotypes will be required to confirm this hypothesis (6). However, the available data suggest that these hallmarks contrast with those hallmarks of eusocial insects with low plasticity like the honey bee and most ants, where a large proportion of genes, functionality, and network differentiation are associated with phenotypic differentiation (44,(53)(54)(55)(56)(57)(58), and where phenotypes appear to be regulated by DNA methylation (24,25,30,34,35,37,(59)(60)(61)(62). Comparisons of species with contrasting evolutionary histories, as in our study species, will be especially valuable in revealing the molecular signatures at the origin of social evolution (e.g., in P. canadensis) and in reversions from complex to simple behaviors (e.g., in D. quadriceps).…”

Section: Discussionmentioning

confidence: 99%

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Patalano

Vlasova

Wyatt

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

195

278

View full text Add to dashboard Cite

Phenotypic plasticity is important in adaptation and shapes the evolution of organisms. However, we understand little about what aspects of the genome are important in facilitating plasticity. Eusocial insect societies produce plastic phenotypes from the same genome, as reproductives (queens) and nonreproductives (workers). The greatest plasticity is found in the simple eusocial insect societies in which individuals retain the ability to switch between reproductive and nonreproductive phenotypes as adults. We lack comprehensive data on the molecular basis of plastic phenotypes. Here, we sequenced genomes, microRNAs (miRNAs), and multiple transcriptomes and methylomes from individual brains in a wasp (Polistes canadensis) and an ant (Dinoponera quadriceps) that live in simple eusocial societies. In both species, we found few differences between phenotypes at the transcriptional level, with little functional specialization, and no evidence that phenotype-specific gene expression is driven by DNA methylation or miRNAs. Instead, phenotypic differentiation was defined more subtly by nonrandom transcriptional network organization, with roles in these networks for both conserved and taxon-restricted genes. The general lack of highly methylated regions or methylome patterning in both species may be an important mechanism for achieving plasticity among phenotypes during adulthood. These findings define previously unidentified hypotheses on the genomic processes that facilitate plasticity and suggest that the molecular hallmarks of social behavior are likely to differ with the level of social complexity.

show abstract

Section: Discussionmentioning

confidence: 99%

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Patalano

Vlasova

Wyatt

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

195

278

View full text Add to dashboard Cite

show abstract

“…Interestingly, when Dnmt3 is knocked down in honeybees using siRNA, they are born with queen-like characteristics such as developed ovaries, mimicking the effects of a royal jelly diet (Kucharski et al, 2008). This study was complimented by the finding that DNMT3 activity reduced with each day that larvae were fed royal jelly (tested at days 3,4 and 5) (Shi et al, 2011). The existence of MBDs in the honeybee is unclear, with Mbd3 being the only classical-type MBD apparent in the genome (Table 1).…”

Section: Honeybee -Apis Melliferamentioning

confidence: 93%

DNA Methylation in Mammalian and Non-Mammalian Organisms

Moffat¹,

Reddington²,

Pennings³

et al. 2012

DNA Methylation - From Genomics to Technology

View full text Add to dashboard Cite

“…They furthermore described large differences in the amount -but not distribution -of 5mC between different subspecies of honey bees (africanised and european honey bees) (Cingolani et al, 2013). Similar differences in global methylation levels were observed between gametes and larvae compared to adults (Ikeda et al, 2011;Drewell et al, 2014) and between bee castes (Shi et al, 2011). In most cases it is not clear yet what the functional importance of the different global methylation levels is.…”

Section: Dna Methylation and Demethylation In Honey Beesmentioning

confidence: 88%

“…It also has to be noted that the queens and workers compared in Lyko et al (2010) were of different ages and methylation changes with age (Lockett et al, 2012;Shi et al, 2013). On the other hand, methylomes of queen and worker larvae also show differential methylation (Foret et al, 2012;Shi et al, 2013) and studies of methylation in individual genes could detect differences (Ikeda et al, 2011;Shi et al, 2011). This suggest that even though Dnmt3 seems to be crucial for queen development (Kucharski et al, 2008), the 5mC pattern in queen and larvae brains fluctuates considerably and may be most different in the larval stage (Foret et al, 2012;Shi et al, 2013) and in older adults (Lyko et al, 2010), but similar in young adults (Herb et al, 2012).…”

Section: Dna Methylation and Demethylation In Honey Beesmentioning

confidence: 94%

“…The presence of DNA methylation and DNA hydroxymethylation as well as that of the full DNA methylation machinery indicates the demand of tight regulation of gene expression in the nervous system of bees. In honey bees DNA methylation is crucial during caste and subcaste development (Elango et al, 2009;Guan et al, 2013;Herb et al, 2012;Kucharski et al, 2008;Lyko et al, 2010;Shi et al, 2013Shi et al, , 2011. DNA methylation also impairs memory extinction (Lockett et al, 2010) and DNA methylation and memory formation in bees stimulus-specific olfactory long-term memory formation (Biergans et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

DNA methylation and the regulation of stimulus-specific memory formation

Biergans¹

View full text Add to dashboard Cite

Memory formation is a crucial task of the brain. It allows animals to dynamically respond to a changing environment by combining information about current and previous experiences. Thus, it promotes complex behaviours such as living in social groups and elaborate foraging tactics. The ability to form memories is present across the animal kingdom in a variety of forms. The honeybee -an eusocial insect -is capable of both 'simple' associative and complex rule learning. Despite decades of research into the mechanisms of memory formation, however, much remains unknown.One little-understood aspect is the regulation of molecular mechanisms during memory formation.Understanding regulation of transcription is particularly important in this context, as transcription is a requirement for any stable memory. Epigenetic mechanisms regulate transcription by directly interacting with chromatin. Importantly, epigenetic mechanisms are conserved across species as distinct as humans and honeybees. This thesis aims to investigate one particular epigenetic mechanism -DNA methylation -and its role in honey bee memory formation by using behavioural, physiological and molecular assays.First, I studied the role of DNA methyltransferases (Dnmts), which catalyse DNA methylation, after olfactory reward learning. Bees were trained to associate an odour with a sugar reward. Dnmts were then blocked after conditioning using a pharmacological inhibitor. 24 hours later, bees were tested for memory retention and generalisation. Dnmt inhibition increased the generalisation to an odour that was not present during the training, thus impairing stimulus-specific memory. This effect was learning-dependent, as bees' response to odours or sugar water alone did not change after treatment. Furthermore, this effect was robust against alterations in the training paradigm, but the directionality depended on the number of training trials. Next, I used Ca2+ -imaging of the bees' primary olfactory centre (i.e. antennal lobe, AL) to investigate whether Dnmts affect changes in AL processing established during memory formation. The AL is involved in odour discrimination and olfactory learning; both processes are also crucial for stimulus-specific memory formation. If Dnmts were inhibited after olfactory reward learning, the AL response to a new odour changed 48 hours later. This effect potentially serves as a functional explanation for the behavioural phenotype observed after Dnmt inhibition. Furthermore, this study provides the first in vivo evidence for Dnmt-mediated regulation of neuronal networks during memory formation.As DNA methylation regulates transcription, I next investigated the effect of Dnmt inhibition on gene expression. Using qPCR I studied 30 memory-associated genes. In response to Dnmt inhibition, 9 genes were upregulated after conditioning. For some of these genes I then investigated their i methylation patterns using a bisulfite conversion based Mass spectrometry approach. Memory formation changed the methylation pattern compared to both...

show abstract

Diet and Cell Size Both Affect Queen-Worker Differentiation through DNA Methylation in Honey Bees (Apis mellifera, Apidae)

Cited by 83 publications

References 13 publications

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

DNA Methylation in Mammalian and Non-Mammalian Organisms

DNA methylation and the regulation of stimulus-specific memory formation

Contact Info

Product

Resources

About