Morphological and genomic shifts in mole-rat ‘queens’ increase fecundity but reduce skeletal integrity
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Curated by eLife
Evaluation Summary:
This manuscript takes a deep dive into the skeletal effects of burrowing and eusocial Damaraland mole rats. By exploring the genetic and skeletal consequences of breeding restricted to a single queen with multiple and closely-timed pregnancies and lactation, this study offers a compelling story that will bolster textbooks on skeletal biology, mammalian evolution, and ethology. The results show the molecular mechanisms driving adaptive plasticity within the unusually expanded lumbar spine and thin limb bones of queens are an adaptive consequence of breeding status.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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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 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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Reviewer #2 (Public Review):
This manuscript set out to address several outstanding questions concerning the impact of 'eusocial' behaviour in mammals, here represented by the experimental model of the Damaraland mole-rat, on skeletal remodelling. Specifically, the transition to breeding status (queen) for some individuals in the colony is accompanied by changes that support high fecundity. The authors investigate the extent to which changes are localised in the skeleton and the underlying regulatory changes that are associated with these morphological features. The paper is well-written, the experiments have been planned thoughtfully and described carefully, and the panel figures convey information without over-crowding. Overall, I thoroughly enjoyed reading this manuscript, which represents as a multi-pronged approach to advancing …
Reviewer #2 (Public Review):
This manuscript set out to address several outstanding questions concerning the impact of 'eusocial' behaviour in mammals, here represented by the experimental model of the Damaraland mole-rat, on skeletal remodelling. Specifically, the transition to breeding status (queen) for some individuals in the colony is accompanied by changes that support high fecundity. The authors investigate the extent to which changes are localised in the skeleton and the underlying regulatory changes that are associated with these morphological features. The paper is well-written, the experiments have been planned thoughtfully and described carefully, and the panel figures convey information without over-crowding. Overall, I thoroughly enjoyed reading this manuscript, which represents as a multi-pronged approach to advancing understanding of the unusual biology and phenotype of queen mole rats.
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Reviewer #1 (Public Review):
The authors provide a novel case-study of the skeletal consequences of queen-only breeding in Damaraland mole-rats, one of the few eusocial mammals. Out of a population of adults, a queen will be selected as the sole female to breed with a male, and the non-breeders will provide support in the highly cooperative society. Once selected, a new queen will undergo a rapid skeletal transformation in which lumbar vertebrae expand. Supporting closely-timed pregnancies and lactation, mineral reserves will be excavated by bone-specific macrophages along the inner, or endosteal, lining of some limb bones. Unlike most other mammals, the skeletons of queens do not typically recover to their pre-pregnancy phenotype as rapid sequential pregnancies continually erode the limbs, leaving them vulnerable to fracture.
To …
Reviewer #1 (Public Review):
The authors provide a novel case-study of the skeletal consequences of queen-only breeding in Damaraland mole-rats, one of the few eusocial mammals. Out of a population of adults, a queen will be selected as the sole female to breed with a male, and the non-breeders will provide support in the highly cooperative society. Once selected, a new queen will undergo a rapid skeletal transformation in which lumbar vertebrae expand. Supporting closely-timed pregnancies and lactation, mineral reserves will be excavated by bone-specific macrophages along the inner, or endosteal, lining of some limb bones. Unlike most other mammals, the skeletons of queens do not typically recover to their pre-pregnancy phenotype as rapid sequential pregnancies continually erode the limbs, leaving them vulnerable to fracture.
To understand the molecular mechanisms driving these phenotypic changes associated with breeding in queens, the authors artificially selected queens in captivity, recreated a eusocial society, and then tracked gene expression along with skeletal phenotypes throughout breeding cycles. After lumbar expansion in queens had completed only long bones showed gene expression consistent with breeding status. Specifically, results showed upregulation of differentiation and activity of bone-specific macrophages, call osteoclasts. These cells liberate minerals from bone and make components of the extracellular matrix available metabolism and development of embryos.
To understand if these changes were driven by the presence of sex-steroids, multiple cell types were harvested from the marrow of lumbar vertebrae and limb bones and treated with estradiol. No significant effect was found. Data, therefore, suggest that mechanisms shaping the postcranial skeleton were not consequences of sex-steroid mediated signaling pathways.
Non-recoverable bone loss in queens is unusual among mammals and is a vulnerability that potentially limits the number of pups a queen can produce. Vulnerable queens may therefore be protected in cooperative societies in which non-breeders can work more and offer queens more rest.
This study furthers the field of skeletal biology by exploring how enduring bone resorption contributes to the greater fecundity of one of the world's few eusocial mammals but has a potentially life-long consequence on limb performance and fracture resistance. The authors weave together multiple lines of evidence to better illustrate the enormous and rapid changes that occur as a female ascends to queen status, and what she sacrifices to build her colony. Results offer compelling and transdisciplinary insights into an extreme skeletal strategy and the impact of this work can be bolstered by only minor changes.
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Evaluation Summary:
This manuscript takes a deep dive into the skeletal effects of burrowing and eusocial Damaraland mole rats. By exploring the genetic and skeletal consequences of breeding restricted to a single queen with multiple and closely-timed pregnancies and lactation, this study offers a compelling story that will bolster textbooks on skeletal biology, mammalian evolution, and ethology. The results show the molecular mechanisms driving adaptive plasticity within the unusually expanded lumbar spine and thin limb bones of queens are an adaptive consequence of breeding status.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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