Morphological and genomic shifts in mole-rat 'queens' increase fecundity but reduce skeletal integrity.
Morphological and genomic shifts in mole-rat 'queens' increase fecundity but reduce skeletal integrity.
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作者：
Johnston RA;Vullioud P;Thorley J;Kirveslahti H;Shen L;Mukherjee S;Karner CM;Clutton-Brock T;Tung J
在一些哺乳动物和许多群居昆虫中，高度合作的社会以生殖分工为特征，繁殖者和非繁殖者在行为和形态上都是不同的。虽然繁殖者和非繁殖者之间的行为和生长差异已经被广泛描述，但对其分子基础知之甚少。在这里，我们研究了繁殖对高度合作的达马拉兰鼹鼠骨骼形态和基因调控的影响。通过实验将繁殖“蚁后”地位与非繁殖者地位分配给年龄匹配的幼崽，我们证实蚁后经历椎体生长，可能赋予繁殖力优势。然而，它们也会上调骨吸收途径，并显示出股骨质量的减少，这预示着骨折的易损性增加。总之，我们的研究结果表明，就像在群居昆虫中一样，鼹鼠的生殖分工导致了基因调控的重新布线和广泛的形态可塑性。然而，在鼹鼠身上，集中繁殖也伴随着骨骼强度的降低。一些群居动物是高度合作的生物，生活在紧密的群体中。蜜蜂和蚂蚁可能是群居昆虫中最著名的例子，而在非洲南部和东部发现的两种啮齿类动物达马拉兰鼹鼠和裸鼹鼠是最具合作精神的哺乳动物。在这些形成群体的动物中，只有一只或几只雌性繁殖，这些有生育能力的雌性通常被称为“女王”。当动物成为蚁后时，它的体型会发生巨大的变化，以满足高繁殖力和频繁繁殖的需求。这种变化的分子基础已经在群居昆虫中得到了很好的描述。然而，在哺乳动物中，人们对它们知之甚少。为了解决这一知识缺口，Johnston等人研究了向鼠后地位的过渡如何影响达马拉兰鼹鼠的骨骼生长和结构完整性，以及体型和大小。实验将无法繁殖的雌性鼹鼠与其他成年雌性鼹鼠进行比较，这些成年雌性鼹鼠最近与一只雄性鼹鼠配对，成为一个新群体的唯一繁殖者。Johnston等人也使用实验室培养的骨源性细胞来评估新生鼠后的潜在基因调控变化。Johnston等人的研究表明，向女王角色的转变会导致一系列骨骼变化，并伴随着与骨骼生长相关的遗传通路调节的变化。鼹鼠后显示出下背部脊柱的加速生长。这些骨头被称为腰椎，这可能使它们有更大的产仔。然而，鼹鼠王鼠的腿骨也会失去骨骼生长潜力，大腿骨会变薄，这可能会增加骨折的风险。因此，与高度群居的昆虫不同，鼹鼠似乎并没有逃脱密集繁殖的物理代价。这项工作增加了我们对基因和身体特征的理解，这些特征已经进化到支持群居动物的合作行为，包括昆虫和哺乳动物之间的差异。它还以一个引人注目的例子表明，动物的基因组如何对社会线索作出反应，从而产生一系列反映其指定社会角色的特征。
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. 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.