Abstract
22 min readArticle Figures and data Abstract eLife digest Introduction Results Discussion Materials and methods Data availability References Decision letter Author response Article and author information Metrics 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. eLife digest Some social animals are highly cooperative creatures that live in tight-knit colonies. Bees and ants are perhaps the most well-known examples of social insects, while Damaraland mole-rats and naked mole-rats, two rodent species found in southern and eastern Africa, are among the most cooperative mammal species. In these colony-forming animals, only one or a few females reproduce and these fertile females are frequently referred to as “queens”. When an animal becomes a queen, her body shape can change dramatically to support the demands of high fertility and frequent reproduction. The molecular basis of such changes has been well-described in social insects. However, they are poorly understood in mammals. To address this knowledge gap, Johnston et al. studied how transitioning to queen status affects bone growth and structural integrity in Damaraland mole-rats, as well as body shape and size. The experiments compared non-breeding female mole-rats with other adult females recently paired with a male to become the sole breeder of a new colony. Johnston et al. also used bone-derived cells grown in the laboratory to assess underlying gene regulatory changes in new queen mole-rats. Johnston et al. showed that transitioning to the role of queen leads to a cascade of skeletal changes accompanied by shifts in the regulation of genetic pathways linked to bone growth. Queen mole-rats show accelerated growth in the spinal column of their lower back. These bones are called lumbar vertebrae and this likely allows them to have larger litters. However, queen mole-rats also lose bone growth potential in their leg bones and develop thinner thigh bones, which may increase the risk of bone fracture. Therefore, unlike highly social insects, mole-rats do not seem to have escaped the physical costs of intensive reproduction. This work adds to our understanding of the genes and physical traits that have evolved to support cooperative behaviour in social animals, including differences between insects and mammals. It also shows, with a striking example, how an animal’s genome responds to social cues to produce a diverse range of traits that reflect their designated social role. Introduction A hallmark of highly cooperative societies is reproductive division of labor. This phenomenon is best understood in eusocial insects, where environmental cues lead to reproductively and morphologically specialized castes, including one or few highly fecund ‘queens’ (Wilson, 1971). These changes help support the reproductive role of queens by differentiating them from nonbreeding colony members, who forage, care for young, and engage in colony defense (Wilson, 1971; Keller and Genoud, 1997). Queens are frequently much larger than their sterile colony mates (e.g., twice as large in honey bees and Pharaoh ants; Berndt and Eichler, 1987; Page and Peng, 2001), reflecting dramatically altered growth and development programs that are explained by changes in gene regulation (Smith et al., 2008). Social insects thus exemplify the tight evolutionary links between reproductive division of labor, cooperative behavior, and extreme morphological plasticity. Systems in which breeding is restricted to a single female supported by multiple nonbreeding helpers are also observed in vertebrates, including birds and mammals (Koenig and Dickinson, 2016). Here, breeding status is not determined during early development, but instead occurs in adulthood, and breeding is only achieved by those individuals who have the opportunity to transition into a reproductive role. In some species, new breeders undergo a period of accelerated growth, which may be important either for maintaining dominance or for supporting high fecundity (Clutton-Brock et al., 2006; Huchard et al., 2016; O'Riain et al., 2000; Russell et al., 2004; Thorley et al., 2018; Young and Bennett, 2010). While substantial gene regulatory divergence with breeding status has been described for the brain and some peripheral organs (Bens et al., 2018; Mulugeta et al., 2017; Sahm et al., 2020), we know little about the gene regulatory shifts responsible for breeder-associated patterns in growth. Because morphological change is often crucial for ramping up offspring production, these processes are key to understanding both the basis for, and limits of, status-driven differences in growth and development. Here, we investigate the morphological and molecular consequences of experimental transitions to breeding status in female Damaraland mole-rats (Fukomys damarensis). Like naked mole-rats (Heterocephalus glaber), Damaraland mole-rats are frequently classified as ‘eusocial’ (Bennett and Faulkes, 2000; Jarvis, 1981; Jarvis and Bennett, 1993), and female helpers who transition to queens experience accelerated vertebral growth associated with increases in fecundity (O'Riain et al., 2000; Thorley et al., 2018). However, it is not clear what triggers skeletal remodeling, where it is localized within the vertebral column, or whether it extends to other parts of the skeleton. Further, the gene regulatory changes that support skeletal remodeling in mole-rat queens are not known, nor are their consequences for skeletal growth potential and integrity. To address these questions, we experimentally assigned age-matched, female littermates to become queens or remain as nonbreeders and evaluated gene regulatory and morphological changes induced by the transition to queen status. Our results indicate that, as in eusocial insects, females that acquire breeding status experience substantial morphological remodeling, associated with pathway-specific changes in gene regulation. Notably, we found that queens not only experience lengthening of their lumbar vertebrae (LV), but also show reductions in the growth potential and structural integrity of their long bones. These changes result from increased rates of bone resorption that may increase the risk of fracture, indicating that the presence of helpers does not annul the costs of reproduction to queens. Results Adaptive plasticity in the skeleton of Damaraland mole-rat queens Adult female Damaraland mole-rats were randomly assigned to either transition to queen status (n = 12) or remain as nonbreeders (n = 18) for the duration of the experiment (Figure 1A–C; Supplementary file 1). Age at assignment (mean age = 19.4 ± 4.4 s.d. months) was consistent with the age at dispersal observed in wild Damaraland mole-rats (1–3 years, Thorley and Clutton-Brock, unpublished data). To resolve whether skeletal changes are a function of the queen transition per se versus release from reproductive suppression in the natal colony, nonbreeders were either kept in their natal colonies as helpers or placed into solitary housing in the absence of a breeding queen, recapitulating extended periods of dispersal in this species (Jarvis and Bennett, 1993) (n = 10 helpers and n = 8 solitaires). At the time of assignment, females assigned to the queen, helper, and solitaire treatments were statistically indistinguishable in body mass, age, and vertebral length (as measured by LV5; unpaired t-tests between all pairwise combinations of treatments: p>0.05; Figure 1—figure supplement 1). When possible, we assigned age-matched littermates to queen versus nonbreeding treatments (26 of 30 experimental animals were in sets of littermate sisters; Supplementary file 1). Six nonexperimental animals (one queen and five nonbreeders) were also included in the sample, resulting in a total sample size of 13 breeders and 23 nonbreeders (Supplementary file 1). Figure 1 with 3 supplements see all Download asset Open asset Transition to queen status leads to lumbar vertebral (LV) lengthening. (a) A breeding ‘queen’ (top) and nonbreeding female (bottom) Damaraland mole-rat, shown at the same scale. Animals are dye marked to allow for individual identification. Photo credit James Bird. (b) An x-ray of a female breeder, with lines depicting the x-ray measurements taken (LV1–LV7, right femur, right tibia, and zygomatic arch). Three developing offspring are visible within the abdomen (highlighted by increased brightness and contrast), and span the length of the LV. (c) Experimental design: nonbreeding adult female () littermates were randomly assigned to transition to queen status (purple ) by being paired with an unrelated male (), or to remain in a nonbreeding treatment (cyan). Duration of treatment ranged from 12 to 22 months. (d) Queens (purple dots) show more rapid growth in LV5 in the first four months of the experiment, relative to nonbreeders (cyan diamonds; treatment by time point interaction: β = 0.078, n = 49, p=3.47×10−3). Dots show means ± standard errors (bars). (e) At the start of the experiment (0 months, left panel), the LV of breeders do not differ from those of nonbreeders (unpaired t-tests, all p>0.05). However, at 12 months (right panel), queens have longer LV relative to nonbreeders (unpaired t-tests, * indicates p<0.05). Dots show means ± standard errors (bars). Lengths of LV above the plots are scaled to indicate the mean lengths of queens (top) and nonbreeders (bottom) at each time point; vertebrae highlighted in purple are significantly longer in queens relative to nonbreeders. (f) Litter size is positively correlated with maternal body length in the Damaraland mole-rat colony (β = 0.353, n = 328 litters, p=1.35×10−3). Females assigned to the queen treatment were each transferred to a new tunnel system containing only an unrelated adult male, simulating the natural process of dispersal and new colony formation in the wild (Jarvis and Bennett, 1993). This pairing procedure, which defines the queen treatment, typically leads to immediate sexual activity and rapid activation of the reproductive axis, including initiation of ovulation and the potential for conception (Bennett et al., 1996; Snyman et al., 2006). Queens gave birth to a mean of 6.92 ± 5.57 s.d. live offspring during the 12–22-month follow-up period, produced in a mean of 2.85 ± 1.75 s.d. litters (range: 0–6; Supplementary file 1). As expected, helpers and solitaires produced no offspring, and did not differ from each other in body mass or vertebral length after the 12–22-month follow-up period (unpaired t-tests, all p>0.05; Figure 1—figure supplement 2). Because helpers and solitaires were morphologically indistinguishable, and also exhibited no differences in gene expression in our subsequent genomic assays (Supplementary file 2), we grouped them together into a single ‘nonbreeder’ treatment for the remainder of our analyses. Compared to nonbreeders, queens showed rapid growth in the LV in the first 12 months post-pairing (Figure 1D, E), especially in the vertebrae toward the caudal end of the vertebral column (LV5 and LV6). Based on longitudinal measurements, most of this differential growth was concentrated soon after the breeding status transition. Specifically, we observed a significant interaction between breeding status (queen versus nonbreeder) and post-pairing time point in the first four months of the experiment (Figure 1D; β = 0.0794, p=3.13×10−3; n = 49 x-rays from 28 animals), but not for measurements taken in later time point intervals (4 versus 8 months; 8 versus 12 months, 12 versus 16 months, 16 versus 22 months; all p>0.05). Moreover, in the first four months, only queens that had already experienced pregnancy showed accelerated vertebral lengthening relative to nonbreeders (unpaired t-test; LV5 of pregnant queens versus nonbreeders: t = −5.735, df = 16.871, p=2.50×10−5; LV5 of queens not yet pregnant versus nonbreeders: t = −0.789, df = 13.007, p=0.444; n = 14 nonbreeders, five pregnant queens, and two queens not yet pregnant). As a result of accelerated vertebral growth in queens post-transition, size differences persisted throughout the study. After 12 months, the absolute length of LV5 in queens was, on average, 4.8% longer than nonbreeders (Figure 1E; LV5: unpaired t-test, t = 2.509, df = 21.095, p=0.020), and the absolute length of the LV column in queens relative to nonbreeders was 3.5% longer, although the latter difference was not significant (unpaired t-test, t = 1.945, df = 22.49, p=0.064). Differences between queens and nonbreeders were even more apparent if LV measures were scaled by zygomatic arch (head) width, as in previous studies (O'Riain et al., 2000; Thorley et al., 2018; Dengler-Crish and Catania, 2009) (LV5: 9.3% longer, unpaired t-test, t = 4.12, df = 15.135, p=8.87×10−4; LV column length: 7.9% longer, unpaired t-test, t = 4.34, df = 15.37, p=5.58×10−4). Thus, transitions to queen status induce reproductive investment, which in turn leads to organism-wide allometric changes that generate an elongated phenotype. The elongated phenotype appears to subsequently facilitate future fecundity. Queens with longer bodies (which correlates with longer LV, Pearson’s r = 0.856, p=5.99×10−59; Figure 1—figure supplement 3) had more pups per litter (Figure 1F; β = 0.353, p=1.35×10−3, n = 328 litters from all breeding groups maintained in the same breeding facility; Supplementary file 3). Controlling for litter size, longer queens also had larger pups: for every additional centimeter of maternal body length, pup body mass increased by 2.9% (β = 0.29, p=0.032, n = 971 pups). Thus, the elongated queen phenotype is a strong candidate for adaptive plasticity that supports increased fertility in queen mole-rats. Breeding status induces gene regulatory changes in the queen mole-rat skeleton To identify the gene regulatory changes associated with skeletal plasticity, we cultured cells enriched for bone marrow-derived mesenchymal stromal cells (bMSCs) isolated from the LV (pooled LV1–LV5) of queens and nonbreeders (n = 5 queens, 11 nonbreeders). bMSC cultures include multipotent skeletal stem cells, the precursor of the osteoblast and chondrocyte lineages responsible for bone growth. In parallel, we cultured cells enriched for bMSCs from the pooled long bones (humerus, ulna, radius, left femur, and left tibia) of the same animals, which do not show increased elongation in queens (femur at 12 months: unpaired t-test, t = −0.202, df = 19.326, p=0.842; tibia at 12 months: unpaired t-test, t = −0.860, df = 16.759, p=0.402). To evaluate the potential role of sex steroid hormone signaling on bone growth, we treated cells from each bone sample for 24 hr with either 10 nM estradiol or vehicle control, resulting in 47 total samples. We then performed RNA-Seq on each sample to screen for genes that were systematically differentially expressed in the bone cells of queens versus nonbreeders. Of 10,817 detectably expressed genes, 171 genes showed a significant effect of breeding status at a false discovery rate (FDR) threshold of 10% in the long bones (329 at an FDR of 20%; Supplementary file 4). Surprisingly, no genes showed a significant effect of breeding status in the LV at either FDR threshold. However, effect sizes were highly correlated between bone types overall (R2 = 0.75, p=4.60×10−53), with more pronounced effects of breeding status in the long bone samples than in the LV (paired t-test on breeding status effects in long bone versus vertebrae: t = 3.97, df = 317.67, p=8.73×10−5). Importantly, breeding status-related differences were not readily attributable to differences in bone cell composition. Based on both canonical markers of bMSC lineage cells and deconvolution of the RNA-Seq data using data from 27 mesenchymal or hematopoietic lineage mouse cell types, the majority cell type in both queen and nonbreeder samples was most similar to cells from the bMSC lineage (Dominici et al., 2006; Hume et al., 2010; Newman et al., 2015; Figure 2—figure supplements 1 and 2). Additionally, the top three principal components summarizing estimated cell-type proportions did not differ between queens and nonbreeders (all FDR > 10%, Supplementary file 5), and we identified no cases in which the effects of breeding status on gene expression were significantly mediated by the first principal component of cell composition (p>0.05 for all 171 queen-associated genes at 10% FDR; Supplementary file 6). The majority of breeding status-associated genes were upregulated in queens (151 of 171 genes, 88%). In support of their role in skeletal plasticity, upregulated genes were enriched for bone remodeling (log2[OR]=4.07, p=5.07×10−6), a process that involves the balanced cycle between bone formation by osteoblasts and bone resorption by osteoclasts (Redlich and Smolen, 2012; Figure 2). Surprisingly, however, enriched pathways were specifically related to bone resorption, not formation (Supplementary file 7), including ‘positive regulation of bone resorption’ (Figure 2A, C; log2[OR]=6.51, p=1.55×10−6) and ‘superoxide anion generation,’ which is involved in osteoclast activity and degradation of bone matrix (Figure 2A, C; log2[OR]=5.29, p=1.4×10−5) (Darden et al., 1996; Datta et al., 1996; Key et al., 1990; Key et al., 1994). Differentially expressed genes were also enriched for immune-related processes (e.g., ‘cytokine secretion,’ ‘chemotaxis,’ ‘leukocyte activation involved in immune response’; Supplementary file 7). These observations suggest that transitions to queen status also involve changes in immunoregulatory signaling (osteoclast cells are derived from monocytes). Figure 2 with 3 supplements see all Download asset Open asset Queen status drives increased regulatory activity of bone resorption pathways. (a) Gene Ontology (GO) terms enriched in queen upregulated genes, relative to the background set of all genes tested. Bars represent 95% confidence intervals. Processes highlighted in purple are also depicted in (c). Highest-level (most general) terms are shown; for full GO enrichment results, see Supplementary file 7. (b) Accessible transcription factor binding site motifs enriched near queen upregulated genes, relative to all genes tested. Bars represent 95% confidence intervals. Transcription factors highlighted in purple are also depicted in (c). (c) Schematic of the balance between bone formation and bone resorption, showing key regulators and markers for mesenchymal stem cell differentiation into osteoblasts and hematopoietic stem cell differentiation into osteoclasts (Redlich and Smolen, 2012; Segeletz and Hoflack, 2016). Note that not all genes or proteins in gray were tested for differential expression (e.g., because they were not annotated in the Damaraland mole-rat genome or were too lowly expressed in our sample); see Supplementary file 4 for full set of tested genes. Queen upregulated genes or corresponding proteins (false discovery rate [FDR] < 10%) are highlighted as purple ovals, and transcription factors with binding motifs enriched near queen upregulated genes are highlighted as purple hexagons. Inset for osteoclasts shows the NADPH oxidase system, which generates superoxide radicals (O2-) necessary for bone resorption and is highly enriched for queen upregulated genes (purple ovals). Omni-ATAC-seq profiling of open chromatin regions further supports a central role for bone resorption and osteoclast activity in the queen skeleton (n = 8; Supplementary file 8). Specifically, transcription factor binding motifs (TFBMs) located in accessible chromatin near queen upregulated genes were enriched for PU.1 and MITF, two transcription factors that are essential for osteoclast differentiation (Segeletz and Hoflack, 2016; Figure 2B, C; PU.1 log2[OR]=1.041, p=2.84×10−4; MITF log2[OR]=0.707, p=7.36×10−3; see Supplementary file 8 for a complete list of enriched TFBMs). MITF was also among the 151 genes that were differentially expressed between queens and nonbreeders and upregulated in both queen long bones and LV. Surprisingly, given the role of sex steroid hormones in bone growth and elevated estradiol levels in queen versus helper Damaraland mole-rats (Bennett, 1994), we observed no significant effects of estradiol treatment on gene expression in either bone type (all FDR > 10%). Queen upregulated genes were also not in closer proximity to androgen response elements (AREs) or estrogen response elements (EREs) than expected by chance (ARE log2[OR]=0.207, p=0.627; ERE log2[OR]=0.196, p=0.652). Consistent with this observation, transcription factor footprinting analysis showed no evidence of queen-associated differences in transcription factor activity of the androgen receptor (AR), estrogen receptor 1 (ESR1), or estrogen receptor 2 (ESR2), in either the long bones or LV (all paired t-tests: p>0.05; Figure 2—figure supplement 3). Thus, our data point to the involvement of non-sex steroid-mediated signaling pathways in remodeling queen mole-rat bones, at least after 1 year post-transition. Extensive skeletal remodeling in queen mole-rats The gene expression data suggest that queen status-driven changes to the skeleton extend beyond the LV to the long bones. Further, they suggest that bone resorption—an important counterpoint to bone formation that is required for normal skeletal maintenance—also distinguishes breeding and nonbreeding females. To investigate this possibility, we performed high-resolution micro-computed tomography (μCT) scanning to generate 3D reconstructions of LV6, LV7, right femur, and right tibia of queens and female nonbreeders (n = 140 bones from 36 animals; Figure 3A, Figure 3—figure supplement 1). This approach substantially increases the level of resolution for investigating breeding status-linked differences in skeletal morphology, as previous studies relied on x-ray data alone (O'Riain et al., 2000; Thorley et al., 2018). Figure 3 with 2 supplements see all Download asset Open asset Queen status leads to reduced growth potential in the tibia and reduced cortical area at the femoral midshaft. (a) Micro-computed tomography (μCT) scans of Damaraland mole-rat tibias. Boxes indicate the location of the proximal growth plate, which varies between unfused (left) to fully fused (right). (b) Example Safranin O-stained histological sections of the proximal tibia, in which the growth plate is unfused (top), partially fused (middle), or fully fused (bottom). Values indicate percent growth plate fusion across the width of the bone. The cartilaginous growth plate is stained deep pink, and calcified bone is stained green. (c) Queens, and specifically queens that gave birth to more offspring, show increased growth plate fusion (β = 0.050, p=4.51×10−3, n = 12, controlling for age) and (d) decreased number of chondrocyte columns within the remaining growth plate (β = −0.132, p=0.020, n = 12, controlling for age). Each box represents the interquartile range, with the median value depicted as a horizontal bar. Whiskers extend to the most extreme values within 1.5× of the interquartile range. In (c) and (d), dots represent individual animals, and shading indicates each animal’s total offspring number. Ages of queens and nonbreeders do not significantly differ (unpaired t-test, t = 0.489, n = 12, p=0.644). (e–g) Femoral cross-sections with area highlighted in gray show the measures represented in the corresponding plots below. Each line represents an age-matched, nonbreeder and queen littermate pair. (e) Queens have less cortical bone (relative to the total area of the femoral midshaft cross-section) compared to their paired nonbreeding littermates (paired t-test, t = −4.07, df = 8, p=3.60×10−3). (f) Queens also have enlarged marrow cavities (paired t-test, t = 5.36, df = 8, p=6.82×10−4) but (g) show no difference in overall periosteal area (paired t-test, t = 1.54, df = 8, p=0.162). We first asked whether breeding status could be predicted from morphological differences in the 3D reconstructions. We found that it could for the LV, but not for the femur: by applying the smooth Euler characteristic transform (Crawford et al., 2016), we were able to predict queen versus nonbreeder status in LV6 (77.8% accuracy, p=0.01, n = 36), but not the femur (52.8% accuracy, p=0.53, n = 36). Including only highly fecund queens (≥6 total offspring) improved predictive accuracy in the femur (70% accuracy, p=0.12, n = 30). Although these predictions did not reach statistical significance, they raised the possibility that morphological changes in femurs become enhanced with increasing reproductive effort. We next tested whether the transition to queen status affects the ability to continue bone lengthening. Lengthening requires the presence of a growth plate, a region of cartilage in the bone where longitudinal growth occurs through proliferation of cartilage cells (chondrocytes) (Figure 3A, B, Figure 3—figure supplement 1). Closure of the growth plate, which indicates that bone lengthening potential has terminated, typically occurs in mammals after reaching sexual maturation, when energy begins to be invested in reproduction instead of growth (Kilborn et al., 2002). To test whether the transition to queen status alters bone lengthening potential, we performed Safranin O staining on sections of the right tibia and LV7 to visualize growth plates (Figure 3B). In the proximal tibia but not LV7, queens were less likely to have open growth plates (Figure 3C, Figure 3—figure supplement 1, and Supplementary file 9; tibia: two-sided binomial test, p=0.019; LV7: two-sided binomial test, p=0.422). The increased probability of growth plate closure in the tibia of queens is linked to the number of offspring a female has produced: females with more offspring showed a higher expanse of closure across the growth plate (β = 0.050, p=4.51×10−3, n = 12, controlling for age). This pattern may be due in part to reduced chondrocyte proliferation, as females that produced more offspring had fewer chondrocyte columns in the remaining growth plate (Figure 3D; β = −0.132, p=0.020, n = 12, controlling for age). Thus, offspring production in queens is associated with loss of the ability to lengthen the long bones, but not the LV, consistent with the importance of abdominal lengthening for supporting larger litters. A major demand on reproductively active female mammals is a high requirement for calcium, particularly during lactation when mothers support rapid offspring bone growth. Maternal skeletons are remodeled to meet this demand, although in most mammals, these changes are not permanent (reviewed in Kovacs, 2016). Because of the particularly intense reproductive investment made by cooperatively breeding mole-rat queens, we therefore also evaluated the effect of queen status on trabecular and cortical bone volumes, which are thought to be important in satisfying short-term and long-term calcium demands, respectively. We found no effect of queen status on the amount of trabecular bone in the femur, tibia, LV6, or LV7 (all p>0.05 for bone volume/total volume). However, we found that cortical bone was significantly reduced at the femoral midshaft, but not in the LV, in queens compared to their nonbreeding sisters (Figure 3E, Figure 3—figure supplement 2; femur: paired t-test of cortical area (CA)/total area, t = −4.067, df = 8, p=3.60×10−3; LV6: paired t-test of CA/total area, t = −0.741, df = 6, p=0.487). Relative to nonbreeders, the femoral midshafts of queens showed significantly lower apparent density (paired t-test, t = −3.734, df = 8, p=5.75×10−3), but no difference in material density (paired t-test, t = −0.074, df = 8, p=0.943). Thus, reduced bone mass in queens is due to reduced bone volume, and not to reduced mass per unit volume (e.g., due to increased porosity). The reduction of apparent density in queens could be due to slowed bone growth, which typically occurs on the outer, periosteal bone surface, or to increased bone resorption, which typically affects the inner endosteal surface and increases the marrow cavity. Our analysis indicates that cortical bone loss in queens is due to the latter explanation: queens had a larger marrow cavity (paired t-test, t = 5.355, df = 8, p=6.82×10−4; Figure 3F) but showed no difference in periosteal area compared to their nonbreeding sisters (paired t-test, t = 1.539, df = 8, p=0.162; Figure 3G). Because changes in cortical bone are thought to reflect accumulated demands over long time frames, we hypothesized that cortical thinning in queens is a consequence of repeated cycles of pregnancy and lactation over time, which can occur simultaneously in Damaraland mole-rat queens. In support of this idea, we found that, within queens, the relative amount of cortical bone is not predicted by the number of pups in a queen’s re
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