Effects of commercial queen rearing methods on queen fecundity and genome methylation

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Original article

Effects of commercial queen rearing methods on queen fecundity and genome methylation Yao YI1,2 , Yi-Bo LIU1 , Andrew B. BARRON3 , Zhi-Jiang ZENG1 1

Honeybee Research Institute, Jiangxi Agricultural University, Nanchang 330045 Jiangxi, People’s Republic of China 2 Jiangxi University of traditional Chinese Medicine, Nanchang 330004 Jiangxi, People’s Republic of China 3 Department of Biological Sciences, Macquarie University, North Ryde, NSW 2109, Australia Received 7 April 2020 – Revised 14 September 2020 – Accepted 29 September 2020

Abstract – The queen and worker castes of the honey bee are very distinct phenotypes that result from different epigenomically regulated developmental programs. In commercial queen rearing, it is common to produce queens by transplanting worker larvae to queen cells to be raised as queens. Here, we examined the consequences of this practice for queen ovary development and genome-wide methylation. Queens reared from transplanted older worker larvae weighed less and had fewer ovarioles than queens reared from transplanted eggs. Methylome analyses revealed a large number of genomic regions in comparisons of egg reared and larvae reared queens. The methylation differences became more pronounced as the age of the transplanted larva increased. Differentially methylated genes had functions in reproduction, longevity, immunity, and metabolic functions suggesting that the methylome of larval reared queens was compromised and more worker-like than the methylome of queens reared from eggs. These findings caution that queens reared from worker larvae are likely less fecund and less healthy than queens reared from transplanted eggs. Apis mellifera / Queen rearing / Fecundity / Genome methylation / Caste differentiation

1. INTRODUCTION The honey bee presents one of the most impressive documented cases of developmental plasticity (Shell and Rehan 2018; Wheeler 1986). There are no genetic differences between the queen and worker castes. Both castes develop from divergent developmental pathways Electronic supplementary material The online version of this article (https://doi.org/10.1007/s13592-020-00817-7) contains supplementary material, which is available to authorized users.

Corresponding author: Z. ZENG, [email protected] Yao YI and Yi-Bo LIU contributed equally to this work. The Illumina sequencing data are accessible through NCBI’s database: DNA methylation data of E, L1, L2 and L3: NCBI Bioproject: PRJNA623058 (SUB7215133). Manuscript editor: Cedric Alaux

(Winston 1991). Recent and rapid progress in comparative functional genomics has revealed how the developmental and nutritional environment in the early larval stages establishes a cascade of epigenomic changes that alter patterns of both gene methylation and gene expression that ultimately result in different developmental systems and two radically different phenotypes (He et al. 2017; Kucharski et al. 2008; Yin et al. 2018). In nature, the developmental environment is established by both the queen and the workers. Worker