The molecular basis of socially induced egg size plasticity in honey bees
Abstract
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 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 knock-down 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.
Data availability
The LC−MS/MS data and search results were deposited in ProteomeXchange Consortium (http://proteomecentral.proteomexchange.org) via the iProX partner repository with the dataset identifier IPX0002748002.All other data are provided as supplementary files.
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Honeybee queen ovary proteomicsProteomeXchange: IPX0002748002.
Article and author information
Author details
Funding
National Natural Science Foundation of China (31970428)
- Bin Han
China Scholarship Council (201903250009)
- Bin Han
National Research Council (Postdoctoral Fellowship)
- Esmaeil Amiri
Agricultural Science and Technology Innovation Program (CAAS-ASTIP-2015-IAR)
- Shufa Xu
Earmarked Fund for Modern Agro-industry Technology Research System (CARS-44)
- Jianke Li
Army Research Office (W911NF1920161)
- Olav Rueppell
Army Research Office (W911NF2210195)
- Olav Rueppell
Natural Sciences and Engineering Research Council of Canada (RGPIN-2022-03629)
- Olav Rueppell
Alberta Beekeepers Commission
- Olav Rueppell
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
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