Morphological and genomic shifts in mole-rat 'queens' increase fecundity but reduce skeletal integrity
- Duke University, United States
- University of Cambridge, United Kingdom
- Duke University School of Medicine, United States
- 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.
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Morphological and genomic shifts in mole-rat queens increase fecundity but reduce skeletal integrityNCBI Gene Expression Omnibus, series accession, GSE152659.
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Morphological and genomic shifts in mole-rat queens increase fecundity but reduce skeletal integrityNCBI Sequence Read Archive, BioProject accession number, PRJNA649596.
Article and author information
Author details
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.
Reviewing Editor
- George H Perry, Pennsylvania State University, United States
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).
Version history
- Received: December 15, 2020
- Accepted: April 11, 2021
- Accepted Manuscript published: April 12, 2021 (version 1)
- 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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Morphological and genomic shifts in mole-rat 'queens' increase fecundity but reduce skeletal integrity
eLife 10:e65760.
https://doi.org/10.7554/eLife.65760
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