Vitellogenin expression in the ovaries of adult honeybee workers provides insights into the evolution of reproductive and social traits

Abstract

Social insects are notable for having two female castes that exhibit extreme differences in their reproductive capacity. The molecular basis of these differences is largely unknown. Vitellogenin (Vg) is a powerful antioxidant and insulin‐signalling regulator used in oocyte development. Here we investigate how Royal Jelly (the major food of honeybee queens) and queen mandibular pheromone (a major regulator of worker fertility), affect the longevity and reproductive status of honey bee workers, the expression of Vg, its receptor VgR and associated regulatory proteins. We find that Vg is expressed in the ovaries of workers and that workers fed a queen diet of Royal Jelly have increased Vg expression in the ovaries. Surprisingly, we find that expression of Vg is not associated with ovary activation in workers, suggesting that this gene has potentially acquired non‐reproductive functions. Therefore, Vg expression in the ovaries of honeybee workers provides further support for the Ovarian Ground Plan Hypothesis, which argues that genes implicated in the regulation of reproduction have been co‐opted to regulate behavioural differences between queens and workers.

Physiological and Immunological Status of Adult Honeybees (Apis mellifera) Fed Sugar Syrup Supplemented with Pentadecapeptide BPC 157

“…Except in the queen, it is possible to detect vitellogenin in hemolymph of workers [ 52 ], and its concentrations can be changed similar to a response to diet, so it is also a marker of nutritional [ 53 ] and immunity status due to an ability to bind to multiple pathogens [ 54 , 55 ]. Furthermore, worker bees that fed a royal jelly have increased vitellogenin expression in the ovaries, but it has non-reproductive functions such as regulation of behavior patterns [ 56 ]. In our study, vitellogenin concentrations in adult honeybee hemolymph sampled on the 11th and 15th day of the experiment under laboratory-controlled conditions showed a significant increase in comparison with honeybees fed only sugar syrup.…”

DNA methylation is not a driver of gene expression reprogramming in young honey bee workers

“…Samples from six of these colonies (colonies queenright A–C and queenless A–C) were initially used for methylome sequencing and subsequently also for the region‐specific analyses, whereas the other six colonies (colonies queenright D–F and queenless D–F) were used for the region‐specific analyses only, which served to validate and confirm the reproducibility of the methylome results. The brains and ovaries of the workers were dissected as described elsewhere (Cardoso‐Júnior et al, 2020, 2021).…”

A long non-coding RNA is a key factor in the evolution of insect eusociality

“…3C and Table S5). Furthermore, the expression pattern of lncov1 was exactly opposite to the ovary activation score (Cardoso-Júnior et al, 2021a), indicating that lncov1 expression is negatively associated with ovary activation in adult worker (Fig. S3, Two-tailed Spearman’s correlation test, ρ = -0.6, p < 0.0001, n = 76).…”

“…Second, we investigated whether the adult workers’ diet affects the lncov1 /Tudor-SN module. For this we fed newly emerged workers a queen-like diet consisting of highly nutritious royal jelly (RJ) mixed with honey to induce ovary activation (Cardoso-Júnior et al, 2021a), or a worker (control) diet, consisting of 50% honey. Workers kept in RJ or control cages, exposed or not to QMP, were provided pollen (protein source) and water ab libitum .…”