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

Abstract
Data availability
Article and author information
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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

1. Johnston RA
2. Vullioud P
3. Thorley J
4. Kirveslahti H
5. Shen L
6. Mukherjee S
7. Karner C
8. Clutton-Brock T
9. Tung J
(2020) Morphological and genomic shifts in mole-rat queens increase fecundity but reduce skeletal integrity
NCBI Gene Expression Omnibus, series accession, GSE152659.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE152659
1. Johnston RA
2. Vullioud P
3. Thorley J
4. Kirveslahti H
5. Shen L
6. Mukherjee S
7. Karner C
8. Clutton-Brock T
9. Tung J
(2020) Morphological and genomic shifts in mole-rat queens increase fecundity but reduce skeletal integrity
NCBI Sequence Read Archive, BioProject accession number, PRJNA649596.

https://www.ncbi.nlm.nih.gov/sra/PRJNA649596
1. Johnston RA
2. Vullioud P
3. Thorley J
4. Kirveslahti H
5. Shen L
6. Mukherjee S
7. Karner C
8. Clutton-Brock T
9. Tung J
(2020) Assessment of effects of breeding status on bone morphology of female Damaraland mole-rats (Fukomys damarensis)
MorphoSource, project 1056.

https://www.morphosource.org/Detail/ProjectDetail/Show/project_id/1056

Article and author information

Author details

Rachel A Johnston

Department of Evolutionary Anthropology, Duke University, Durham, United States

For correspondence
racheljohnston7@gmail.com

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-8965-1162
Philippe Vullioud

Department of Zoology, University of Cambridge, Cambridge, United Kingdom

Competing interests
No competing interests declared.
Jack Thorley

Department of Zoology, University of Cambridge, Cambridge, United Kingdom

Competing interests
No competing interests declared.
Henry Kirveslahti

Department of Statistical Science, Duke University, Durham, United States

Competing interests
No competing interests declared.
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.
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.
Courtney M Karner

Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas, United States

Competing interests
No competing interests declared.
Tim Clutton-Brock

Department of Zoology, University of Cambridge, Cambridge, United Kingdom

Competing interests
No competing interests declared.
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..

"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).

Copyright

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.