Multi-organ proteome reveals different nursing ability between two honeybee srocks.

High royal jelly production is an adaptive reproductive investment syndrome in honey bees that enhances their nursing ability to queen bee larvae. However, the biological basis of this reproduction investment at the multi-organ level remains elusive. In this study, proteome across 11 organs of two bee stocks: high royal jelly production bees (RJBs) and Italian bees (ITBs) was compared. Our analysis revealed significant differences in protein expression profiles in brain, fat body, mandibular gland, and Malpighian tubule, highlighting their crucial roles in regulating royal jelly secretion in RJBs. The increased energy turnover, protein synthesis, and lipid synthesis observed in RJBs compared to ITBs highlight their enhanced metabolic activity, which is essential for the robust secretion of royal jelly in RJBs. The elevated abundance of major royal jelly proteins (MRJPs), hexamerins, and vitellogenin suggests their critical contributions to the nutritional and material requirement necessary for royal jelly secretion. Furthermore, the high level of vitellogenin and juvenile hormone esterase may suppress juvenile hormones, which contribute to a strong royal jelly secretion and sensitivity of RJBs to larval pheromones relative to ITBs. This comprehensive dataset contributes to a better understanding of nursing behavior and reproductive investment in honey bees. Significiance. The royal jelly secretion syndrome is a colony level social trait dominated by the intricate interplay of multiple organs. However, previous studies have primarily focused on individual organs. In this study, the proteome of 11 organs was compared between high royal jelly production bees (RJBs) and Italian bees (ITBs) to provide knowledge on how multiple organs cooperate to boost the elevated royal jelly production by RJBs. Nutrition supply was sufficient at multiple organs of RJBs when compared to ITBs, indicating that nutrition plays an essential role in boosting energy metabolism, protein and lipid synthesis, and directly contributes to the amount of royal jelly secretion. The high level of secretion of storage proteins, such as MRJPs, hex, and vitellogenin, provides sufficient nutrition and material for royal jelly secretion. Moreover, the higher levels of vitellogenin and juvenile hormone esterase may suppress juvenile hormone synthesis, and contributing to stronger sense of RJBs to larval pheromone relative to ITBs. This suggests that nutrition can influence the hormone levels and sensory abilities of RJBs nurse bees to promote their royal jelly secretion ability. The reported data provide insights into the systematic regulation strategy of honeybee nursing behavior and reproductive investment.