Morphological and genomic shifts in mole-rat 'queens' increase fecundity but reduce skeletal integrity

  1. Rachel A Johnston  Is a corresponding author
  2. Philippe Vullioud
  3. Jack Thorley
  4. Henry Kirveslahti
  5. Leyao Shen
  6. Sayan Mukherjee
  7. Courtney M Karner
  8. Tim Clutton-Brock
  9. Jenny Tung  Is a corresponding author
  1. Duke University, United States
  2. University of Cambridge, United Kingdom
  3. Duke University School of Medicine, United States
  4. University of Texas Southwestern Medical Center, United States

Abstract

In some mammals and many social insects, highly cooperative societies are characterized by reproductive division of labor, in which breeders and nonbreeders become behaviorally and morphologically distinct. While differences in behavior and growth between breeders and nonbreeders have been extensively described, little is known of their molecular underpinnings. Here, we investigate the consequences of breeding for skeletal morphology and gene regulation in highly cooperative Damaraland mole-rats. By experimentally assigning breeding 'queen' status versus nonbreeder status to age-matched littermates, we confirm that queens experience vertebral growth that likely confers advantages to fecundity. However, they also up-regulate bone resorption pathways and show reductions in femoral mass, which predicts increased vulnerability to fracture. Together, our results show that, as in eusocial insects, reproductive division of labor in mole-rats leads to gene regulatory rewiring and extensive morphological plasticity. However, in mole-rats, concentrated reproduction is also accompanied by costs to bone strength.

Data availability

All RNA sequencing data generated during this study are available in the NCBI Gene Expression Omnibus (series accession GSE152659). ATAC-Seq data are available in the NCBI Sequence Read Archive (BioProject accession number PRJNA649596). μCT data from this study are available on MorphoSource (http://www.morphosource.org, project 1056). All code used for the study are available at https://github.com/rachelj98/MoleratBones.

The following data sets were generated

Article and author information

Author details

  1. Rachel A Johnston

    Department of Evolutionary Anthropology, Duke University, Durham, United States
    For correspondence
    racheljohnston7@gmail.com
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8965-1162
  2. Philippe Vullioud

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    No competing interests declared.
  3. Jack Thorley

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    No competing interests declared.
  4. Henry Kirveslahti

    Department of Statistical Science, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
  5. Leyao Shen

    Department of Orthopaedic Surgery, Duke Orthopaedic Cellular, Developmental, and Genome Laboratories, Duke University School of Medicine, Durham, United States
    Competing interests
    No competing interests declared.
  6. Sayan Mukherjee

    Department of Statistical Science; Department of Computer Science; Department of Mathematics; Department of Bioinformatics & Biostatistics, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
  7. Courtney M Karner

    Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    No competing interests declared.
  8. Tim Clutton-Brock

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    No competing interests declared.
  9. Jenny Tung

    Evolutionary Anthropology, Biology, Duke University, Durham, NC, United States
    For correspondence
    jenny.tung@duke.edu
    Competing interests
    Jenny Tung, Jenny Tung is a Reviewing Editor at eLife..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0416-2958

Funding

European Research Council (294494)

  • Tim Clutton-Brock

National Institutes of Health (AR076325)

  • Courtney M Karner

National Institutes of Health (AR071967)

  • Courtney M Karner

European Research Council (742808)

  • Tim Clutton-Brock

Human Frontier Science Program (RGP0051-2017)

  • Sayan Mukherjee
  • Tim Clutton-Brock
  • Jenny Tung

National Science Foundation (IOS-7801004)

  • Jenny Tung

National Institutes of Health (F32HD095616)

  • Rachel A Johnston

Sloan Foundation Early Career Research Fellowship

  • Jenny Tung

Foerster-Bernstein Postdoctoral Fellowship

  • Rachel A Johnston

Natural Environment Research Council (Doctoral Training Program Grant)

  • Jack Thorley

North Carolina Biotechnology Center (2016-IDG-1013)

  • Jenny Tung

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: Animals were deeply anesthetized with isoflurane and sacrificed with decapitation following USGS National Wildlife Health Center guidelines and under approval from the Animal Ethics Committee of the University of Pretoria (Permit #EC081-17).

Reviewing Editor

  1. George H Perry, Pennsylvania State University, United States

Version history

  1. Received: December 15, 2020
  2. Accepted: April 11, 2021
  3. Accepted Manuscript published: April 12, 2021 (version 1)
  4. Version of Record published: May 7, 2021 (version 2)

Copyright

© 2021, Johnston et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Rachel A Johnston
  2. Philippe Vullioud
  3. Jack Thorley
  4. Henry Kirveslahti
  5. Leyao Shen
  6. Sayan Mukherjee
  7. Courtney M Karner
  8. Tim Clutton-Brock
  9. Jenny Tung
(2021)
Morphological and genomic shifts in mole-rat 'queens' increase fecundity but reduce skeletal integrity
eLife 10:e65760.
https://doi.org/10.7554/eLife.65760

Share this article

https://doi.org/10.7554/eLife.65760

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