MicroRNAs Associated with Caste Determination and Differentiation in a Primitively Eusocial Insect

Collins, David H.; Mohorianu, Irina; Beckers, Matthew; Moulton, Vincent; Dalmay, Tamás; Bourke, Andrew F. G.

doi:10.1038/srep45674

Cited by 42 publications

(32 citation statements)

References 60 publications

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“…Histone modifications have been shown to be involved with plasticity, for example changes in histone acetylation alter the behavior of major workers of the ant species Camponotus floridanus, making them more similar to the behavior of minor workers (Simola et al 2016). Variation in microRNA expression levels has been identified in both honeybee (Ashby et al 2016) and bumblebee (Collins et al 2017) castes. However, the most active research in this area has been focused on DNA methylation (Glastad et al 2015).…”

Section: Impact Summarymentioning

confidence: 99%

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Methylation and gene expression differences between reproductive and sterile bumblebee workers

2019

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Phenotypic plasticity is the production of multiple phenotypes from a single genome and is notably observed in social insects. Multiple epigenetic mechanisms have been associated with social insect plasticity, with DNA methylation being explored to the greatest extent. DNA methylation is thought to play a role in caste determination in Apis mellifera, and other social insects, but there is limited knowledge on its role in other bee species. In this study, we analyzed whole genome bisulfite sequencing and RNA‐seq data sets from head tissue of reproductive and sterile castes of the eusocial bumblebee Bombus terrestris. We found that genome‐wide methylation in B. terrestris is similar to other holometabolous insects and does not differ between reproductive castes. We did, however, find differentially methylated genes between castes, which are enriched for multiple biological processes including reproduction. However, we found no relationship between differential methylation and differential gene expression or differential exon usage between castes. Our results also indicate high intercolony variation in methylation. These findings suggest that methylation is associated with caste differences but may serve an alternate function, other than direct caste determination in this species. This study provides the first insights into the nature of a bumblebee caste‐specific methylome as well as its interaction with gene expression and caste‐specific alternative splicing, providing greater understanding of the role of methylation in phenotypic plasticity within social bee species. Future experimental work is needed to determine the function of methylation and other epigenetic mechanisms in insects.

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Section: Impact Summarymentioning

confidence: 99%

“…) and bumblebee (Collins et al. ) castes. However, the most active research in this area has been focused on DNA methylation (Glastad et al.…”

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confidence: 99%

Methylation and gene expression differences between reproductive and sterile bumblebee workers

2019

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“…Histone modifications have been shown to be involved with plasticity, for example changes in histone acetylation alter the behaviour of major workers of the ant species Camponotus floridanus , making them more similar to the behaviour of minor workers (Simola et al , 2016). Variation in microRNA expression levels has been identified in both honeybee (Ashby et al , 2016) and bumblebee (Collins et al , 2017) castes. However the most active research in this area has been focused on DNA methylation (Glastad et al , 2015).…”

Section: Introductionmentioning

confidence: 99%

Methylation and Gene Expression Differences Between Reproductive Castes of Bumblebee Workers

Marshall

Lonsdale

Mallon

2019

Preprint

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word count: 244. 4 Document work count: 6353. 5 Abstract 7Phenotypic plasticity is the production of multiple phenotypes from a single genome and is 8 notably observed in social insects. Multiple epigenetic mechanisms have been associated with 9 social insect plasticity, with DNA methylation being explored to the greatest extent. DNA 10 methylation is thought to play a role in caste determination in Apis mellifera, and other social 11 insects, but there is limited knowledge on it's role in other bee species. In this study we analysed 12 whole genome bisulfite sequencing and RNA-seq data sets from head tissue of reproductive and 13 sterile castes of the eusocial bumblebee Bombus terrestris. We found genome-wide methylation 14 in B. terrestris is similar to other social insects and does not differ between reproductive castes. 15 We did, however, find differentially methylated genes between castes, which are enriched for 16 multiple biological processes including reproduction. However we found no relationship between 17 differential methylation and differential gene expression or differential exon usage between castes. 18 Our results also indicate high inter-colony variation in methylation. These findings suggest 19 methylation is associated with caste differences but may serve an alternate function, other than 20 direct caste determination in this species. This study provides the first insights into the nature 21 of a bumblebee caste specific methylome as well as it's interaction with gene expression and 22 caste specific alternative splicing, providing greater understanding of the role of methylation in 23 phenotypic plasticity within social bee species. Future experimental work is needed to determine 24 the function of methylation and other epigenetic mechanisms in social insects. 25 1 Methylation Differences in Bumblebee Workers Impact Summary 26 Social insects, such as ants, termites, bees and wasps, can produce individuals with extreme physical 27 and behavioural differences within the same colony known as castes (e.g. workers/soldiers/queens). 28 These individuals have similar genomes and many studies have associated epigenetic mechanisms 29 with the differences observed. Epigenetic modifications are changes that affect how genes are 30 expressed without changing the underlying DNA code. Here we investigated differences in DNA 31 methylation (a well researched modified base) between different reproductive castes of the bumblebee, 32Bombus terrestris, an economically and environmentally important pollinator species. We found B. 33terrestris has a similar methylation profile to other social insect species in terms of the distribution of 34 methylation throughout the genome and the relationship between methylation and gene expression. 35Genes that have differences in methylation between reproductive castes are involved in multiple 36 biological processes, including reproduction, suggesting methylation may hold multiple functions 37 in this species. These differentially methylated genes...

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“…Functional genomic techniques, such as RNA‐Seq, provide an unbiased view into genome‐wide transcriptional changes and have been applied to microparasite–insect systems to elucidate genes underlying complex altered host phenotypes (Choi et al ., ; Geffre et al ., ). For the bumblebee, recent developments in genomics and transcriptomics have provided the tools to explore important aspects of host biology, including phenotypic polymorphism (Colgan et al ., ; Harrison et al ., ), caste differentiation (Collins et al ., ; Woodard et al ., ), mating success (Manfredini et al ., ) and diapause regulation (Amsalem et al ., ). In relation to pathogen response, previous transcriptomic studies have identified changes in host immune expression in response to the trypanosomatid Crithidia bombi (Barribeau et al ., ) and bacterial challenge (Barribeau et al ., ).…”

Section: Introductionmentioning

confidence: 99%

Infection by the castrating parasitic nematode Sphaerularia bombi changes gene expression in Bombus terrestris bumblebee queens

Colgan

Carolan

Sumner

et al. 2019

Insect Molecular Biology

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Parasitism can result in dramatic changes in host phenotype, which are themselves underpinned by genes and their expression. Understanding how hosts respond at the molecular level to parasites can therefore reveal the molecular architecture of an altered host phenotype. The entomoparasitic nematode Sphaerularia bombi is a parasite of bumblebee (Bombus) hosts where it induces complex behavioural changes and host castration. To examine this interaction at the molecular level, we performed genome‐wide transcriptional profiling using RNA‐Sequencing (RNA‐Seq) of S. bombi‐infected Bombus terrestris queens at two critical time‐points: during and just after overwintering diapause. We found that infection by S. bombi affects the transcription of genes underlying host biological processes associated with energy usage, translation, and circadian rhythm. We also found that the parasite affects the expression of immune genes, including members of the Toll signalling pathway providing evidence for a novel interaction between the parasite and the host immune response. Taken together, our results identify host biological processes and genes affected by an entomoparasitic nematode providing the first steps towards a molecular understanding of this ecologically important host–parasite interaction.

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MicroRNAs Associated with Caste Determination and Differentiation in a Primitively Eusocial Insect

Cited by 42 publications

References 60 publications

Methylation and gene expression differences between reproductive and sterile bumblebee workers

Methylation and gene expression differences between reproductive and sterile bumblebee workers

Methylation and Gene Expression Differences Between Reproductive Castes of Bumblebee Workers

Infection by the castrating parasitic nematode Sphaerularia bombi changes gene expression in Bombus terrestris bumblebee queens

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