Reproduction involves the investment of resources into offspring. Although variation in reproductive effort often affects the number of offspring, adjustments of propagule size are also found in numerous species, including the Western honey bee, Apis mellifera. However, the proximate causes of these adjustments are insufficiently understood, especially in oviparous species with complex social organization in which adaptive evolution is shaped by kin selection. Here, we show in a series of experiments that queens predictably and reversibly increase egg size in small colonies and decrease egg size in large colonies, while their ovary size changes in the opposite direction. Additional results suggest that these effects cannot be solely explained by egg-laying rate and are due to the queens' perception of colony size. Egg-size plasticity is associated with quantitative changes of 290 ovarian proteins, most of which relate to energy metabolism, protein transport, and cytoskeleton. Based on functional and network analyses, we further study the small GTPase Rho1 as a candidate regulator of egg size. Spatio-temporal expression analysis via RNAscope and qPCR supports an important role of Rho1 in egg-size determination, and subsequent RNAi-mediated gene knockdown confirmed that Rho1 has a major effect on egg size in honey bees. These results elucidate how the social environment of the honey bee colony may be translated into a specific cellular process to adjust maternal investment into eggs. It remains to be studied how widespread this mechanism is and whether it has consequences for population dynamics and epigenetic influences on offspring phenotype in honey bees and other species.
Keywords: Apis mellifera; cytoskeleton; evolutionary biology; oocyte; reproduction; resource allocation; social evolution.
Honey bees are social insects that live in large colonies containing tens of thousands of individuals. The vast majority of bees are sterile females known as worker bees. They perform most of the activities essential for the survival of the colony, including foraging for pollen and nectar and taking care of eggs and larvae. An individual known as the queen bee is the mother of the colony and is normally the only female who reproduces. She has two massive ovaries and can produce up to two thousand eggs per day. Previous studies indicate that the number and size of the eggs vary according to the conditions inside the colony and in the surrounding environment. Larger eggs contain more nutrients so the resulting embryos may have a better chance of survival. However, producing bigger eggs requires the queen to invest more resources, which is costly to the colony as a whole. It remains unclear which mechanisms regulate the size of honey bee eggs. To address this question, Han, Wei, Amiri et al. carried out a series of experiments on the Western honey bee, Apis mellifera. The experiments showed that queen bees in small colonies had smaller ovaries and produced bigger eggs than those in large colonies. The difference in egg size appeared to be due to the queen bee’s perception of the size of the colony, rather than its actual size. An approach called proteomics revealed that 290 ovarian proteins were produced at different levels in big-egg producing ovaries compared to small-egg producing ovaries. Further experiments suggested that a protein known as Rho1 regulates the size of the eggs the queen bees produce. These findings provide an explanation for how the social environment of the Western honey bee colony may influence the queen bee’s reproductive investment at the molecular level. Further studies to confirm and expand on this work may help to improve honey bee health and also contribute to our general understanding of this life stage in bees and other insects.