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.

Female Developmental Environment Delays Development of Male Honeybee (Apis Mellifera)

“…6; Table S7, S8 and S11). The mTOR, Wnt, Notch, transforming growth factor-beta (TGF-β) and hippo signaling pathways play an essential role in the developmental processes, such as caste differentiation, embryogenesis, morphogenesis, imaginal disc development and organ size regulation in honeybees and other insects [24][25][26][27][28][29][30]. These results demonstrated a clear difference in gene expression between honeybee male larvae developed from drone cells and female cells.…”

“…Fold Change ≥ 1 and p < 0.05 were used as the screening criteria to identify signi cant DEGs among three groups. We selected 61 and 50 interesting genes that are involved in caste differentiation and development regulation [9,[25][26][27][28][29][30] from comparisons at larval and adult stages respectively. The log10 fold change values of these genes were used for heatmap analysis in R package [40]…”

Effects of Queen Cell Size and Caging Days of Mother Queen on Rearing Young Honey Bee Queens Apis mellifera L.

“…The nutrition and the amount of food given to young larvae cause the caste determination of worker and queen regulated developmental pathways. The more the larvae are given, the better the reared queen would be (Kucharski et al, 2008;Maleszka, 2008;He et al, 2017). However, when the larvae had enough royal jelly for food, the quality of food was very important for the development of larvae.…”

“…When rearing young honey bee queens, 1 st star larvae are usually grafted into queen cells and are inserted into a queenless colony. However, the quality of reared queens are affected by many such factors as genetic background, rearing season, queen breeding methods and the age of larvae used for rearing queen (Gilley, Tarpy, & Land, 2003;Koç & Karacaoglu, 2004;Liu et al, 2011;Zhang et al, 2013;Hatjina et al, 2014;He et al, 2017). Beyond that, external environmental factors also affect the quality of reared queens, such as the intensity of the colony, food-storage and weather (Nabors, 2000;Liao et al, 2016).…”

Experimental improvement of honey bee (Apis mellifera) queen quality through nutritional and hormonal supplementation

“…Because female larvae are totipotent until their third day of larval development, they are equally capable of developing into workers or queens. Those fed constantly with royal jelly are effectively raised as queens (Weaver 1957;He et al 2017). Whether queens are reared naturally or artificially, they are nonetheless a critical component to colony fitness and productivity.…”