The molecular basis of socially induced egg size plasticity in honey bees

  1. Bin Han
  2. Qiaohong Wei
  3. Esmaeil Amiri
  4. Han Hu
  5. Lifeng Meng
  6. Micheline K Strand
  7. David R Tarpy
  8. Shufa Xu
  9. Jianke Li  Is a corresponding author
  10. Olav Rueppell  Is a corresponding author
  1. Chinese Academy of Agricultural Sciences, China
  2. Mississippi State University, United States
  3. United States Army Research Office, United States
  4. North Carolina State University, United States
  5. University of Alberta, Canada

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.

The following data sets were generated

Article and author information

Author details

  1. Bin Han

    Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6974-8699
  2. Qiaohong Wei

    Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Esmaeil Amiri

    Delta Research and Extension Center, Mississippi State University, Stoneville, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Han Hu

    Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Lifeng Meng

    Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Micheline K Strand

    Biological and Biotechnology Sciences Branch, United States Army Research Office, Research Triangle Park, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. David R Tarpy

    Department of Applied Ecology, North Carolina State University, Raleigh, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8601-6094
  8. Shufa Xu

    Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Jianke Li

    Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, China
    For correspondence
    apislijk@126.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9344-0886
  10. Olav Rueppell

    Department of Biological Sciences, University of Alberta, Edmonton, Canada
    For correspondence
    olav@ualberta.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5370-4229

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.

Reviewing Editor

  1. Rosalyn Gloag, University of Sydney, Australia

Publication history

  1. Received: May 23, 2022
  2. Accepted: November 7, 2022
  3. Accepted Manuscript published: November 8, 2022 (version 1)

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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  1. Bin Han
  2. Qiaohong Wei
  3. Esmaeil Amiri
  4. Han Hu
  5. Lifeng Meng
  6. Micheline K Strand
  7. David R Tarpy
  8. Shufa Xu
  9. Jianke Li
  10. Olav Rueppell
(2022)
The molecular basis of socially induced egg size plasticity in honey bees
eLife 11:e80499.
https://doi.org/10.7554/eLife.80499
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