title: Making a queen: an epigenetic analysis of the robustness of the honeybee (Apis mellifera) queen developmental pathway.
abstract: Specialized castes are considered a key reason for the evolutionary and ecological success of the social insect lifestyle. The most essential caste distinction is between the fertile queen and the sterile workers. Honeybee (Apis mellifera) workers and queens are not genetically distinct, rather these different phenotypes are the result of epigenetically regulated divergent developmental pathways. This is an important phenomenon in understanding the evolution of social insect societies. Here, we studied the genomic regulation of the worker and queen developmental pathways, and the robustness of the pathways by transplanting eggs or young larvae to queen cells. Queens could be successfully reared from worker larvae transplanted up to 3 days age, but queens reared from older worker larvae had decreased queen body size and weight compared with queens from transplanted eggs. Gene expression analysis showed that queens raised from worker larvae differed from queens raised from eggs in the expression of genes involved in the immune system, caste differentiation, body development and longevity. DNA methylation levels were also higher in 3-day-old queen larvae raised from worker larvae compared with that raised from transplanted eggs identifying a possible mechanism stabilizing the two developmental paths. We propose that environmental (nutrition and space) changes induced by the commercial rearing practice result in a suboptimal queen phenotype via epigenetic processes, which may potentially contribute to the evolution of queen-worker dimorphism. This also has potentially contributed to the global increase in honeybee colony failure rates.
authors.affiliation: Honeybee Research Institute, Jiangxi Agricultural University, Nanchang, Jiangxi, 330045, China.
authors.forename: Xu Jiang
authors.initials: XJ
authors.lastname: He
authors.affiliation: Honeybee Research Institute, Jiangxi Agricultural University, Nanchang, Jiangxi, 330045, China.
authors.forename: Lin Bin
authors.initials: LB
authors.lastname: Zhou
authors.affiliation: Honeybee Research Institute, Jiangxi Agricultural University, Nanchang, Jiangxi, 330045, China.
authors.forename: Qi Zhong
authors.initials: QZ
authors.lastname: Pan
authors.affiliation: Department of Biological Sciences, Macquarie University, North Ryde, NSW, 2109, Australia.
authors.forename: Andrew B
authors.initials: AB
authors.lastname: Barron
authors.affiliation: Honeybee Research Institute, Jiangxi Agricultural University, Nanchang, Jiangxi, 330045, China.
authors.forename: Wei Yu
authors.initials: WY
authors.lastname: Yan
authors.affiliation: Honeybee Research Institute, Jiangxi Agricultural University, Nanchang, Jiangxi, 330045, China.
authors.forename: Zhi Jiang
authors.identifier: http://orcid.org/0000-0001-7445-8944
authors.initials: ZJ
authors.lastname: Zeng
mesh_terms: D000818:Animals; D001516:Bees / Q000235:genetics* / Q000254:growth & development*; D019175:DNA Methylation; D044127:Epigenesis, Genetic; D005260:Female; D018507:Gene Expression Regulation, Developmental; D007814:Larva; D010063:Ovum; D010641:Phenotype
keywords: DNA methylation; epigenetic analysis; gene expression; honeybee; immunity; queen