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

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 extensive...

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Autores principales: Johnston, Rachel A, Vullioud, Philippe, Thorley, Jack, Kirveslahti, Henry, Shen, Leyao, Mukherjee, Sayan, Karner, Courtney M, Clutton-Brock, Tim, Tung, Jenny
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8104968/
https://www.ncbi.nlm.nih.gov/pubmed/33843584
http://dx.doi.org/10.7554/eLife.65760
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author Johnston, Rachel A
Vullioud, Philippe
Thorley, Jack
Kirveslahti, Henry
Shen, Leyao
Mukherjee, Sayan
Karner, Courtney M
Clutton-Brock, Tim
Tung, Jenny
author_facet Johnston, Rachel A
Vullioud, Philippe
Thorley, Jack
Kirveslahti, Henry
Shen, Leyao
Mukherjee, Sayan
Karner, Courtney M
Clutton-Brock, Tim
Tung, Jenny
author_sort Johnston, Rachel A
collection PubMed
description 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 upregulate 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.
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spelling pubmed-81049682021-05-11 Morphological and genomic shifts in mole-rat ‘queens’ increase fecundity but reduce skeletal integrity Johnston, Rachel A Vullioud, Philippe Thorley, Jack Kirveslahti, Henry Shen, Leyao Mukherjee, Sayan Karner, Courtney M Clutton-Brock, Tim Tung, Jenny eLife Chromosomes and Gene Expression 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 upregulate 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. eLife Sciences Publications, Ltd 2021-04-12 /pmc/articles/PMC8104968/ /pubmed/33843584 http://dx.doi.org/10.7554/eLife.65760 Text en © 2021, Johnston et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Chromosomes and Gene Expression
Johnston, Rachel A
Vullioud, Philippe
Thorley, Jack
Kirveslahti, Henry
Shen, Leyao
Mukherjee, Sayan
Karner, Courtney M
Clutton-Brock, Tim
Tung, Jenny
Morphological and genomic shifts in mole-rat ‘queens’ increase fecundity but reduce skeletal integrity
title Morphological and genomic shifts in mole-rat ‘queens’ increase fecundity but reduce skeletal integrity
title_full Morphological and genomic shifts in mole-rat ‘queens’ increase fecundity but reduce skeletal integrity
title_fullStr Morphological and genomic shifts in mole-rat ‘queens’ increase fecundity but reduce skeletal integrity
title_full_unstemmed Morphological and genomic shifts in mole-rat ‘queens’ increase fecundity but reduce skeletal integrity
title_short Morphological and genomic shifts in mole-rat ‘queens’ increase fecundity but reduce skeletal integrity
title_sort morphological and genomic shifts in mole-rat ‘queens’ increase fecundity but reduce skeletal integrity
topic Chromosomes and Gene Expression
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8104968/
https://www.ncbi.nlm.nih.gov/pubmed/33843584
http://dx.doi.org/10.7554/eLife.65760
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