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.

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.

Metrics

  • 1,301
    views
  • 251
    downloads
  • 7
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

https://doi.org/10.7554/eLife.80499

Further reading

    1. Evolutionary Biology
    Matthew Osmond, Graham Coop
    Research Article

    Spatial patterns in genetic diversity are shaped by individuals dispersing from their parents and larger-scale population movements. It has long been appreciated that these patterns of movement shape the underlying genealogies along the genome leading to geographic patterns of isolation by distance in contemporary population genetic data. However, extracting the enormous amount of information contained in genealogies along recombining sequences has, until recently, not been computationally feasible. Here we capitalize on important recent advances in genome-wide gene-genealogy reconstruction and develop methods to use thousands of trees to estimate per-generation dispersal rates and to locate the genetic ancestors of a sample back through time. We take a likelihood approach in continuous space using a simple approximate model (branching Brownian motion) as our prior distribution of spatial genealogies. After testing our method with simulations we apply it to Arabidopsis thaliana. We estimate a dispersal rate of roughly 60km2 per generation, slightly higher across latitude than across longitude, potentially reflecting a northward post-glacial expansion. Locating ancestors allows us to visualize major geographic movements, alternative geographic histories, and admixture. Our method highlights the huge amount of information about past dispersal events and population movements contained in genome-wide genealogies.

    1. Evolutionary Biology
    Mattias Siljestam, Claus Rueffler
    Research Article

    The majority of highly polymorphic genes are related to immune functions and with over 100 alleles within a population, genes of the major histocompatibility complex (MHC) are the most polymorphic loci in vertebrates. How such extraordinary polymorphism arose and is maintained is controversial. One possibility is heterozygote advantage (HA), which can in principle maintain any number of alleles, but biologically explicit models based on this mechanism have so far failed to reliably predict the coexistence of significantly more than ten alleles. We here present an eco-evolutionary model showing that evolution can result in the emergence and maintenance of more than 100 alleles under HA if the following two assumptions are fulfilled: first, pathogens are lethal in the absence of an appropriate immune defence; second, the effect of pathogens depends on host condition, with hosts in poorer condition being affected more strongly. Thus, our results show that HA can be a more potent force in explaining the extraordinary polymorphism found at MHC loci than currently recognized.