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Book ChapterDOI

Social Behavior in Naked Mole-Rats: Individual Differences in Phenotype and Proximate Mechanisms of Mammalian Eusociality.

TL;DR: Naked mole-rats (Heterocephalus glaber) are small rodents native to east Africa, living in subterranean colonies of up to 300 individuals, and reproduction is restricted to a single breeding female and 1-3 breeding males; all other colony members are reproductively suppressed and socially subordinate unless removed from the suppressive cues of the colony.
Abstract: Naked mole-rats (Heterocephalus glaber) are small rodents native to east Africa, living in subterranean colonies of up to 300 individuals. Within each colony, reproduction is restricted to a single breeding female and 1-3 breeding males; all other colony members are reproductively suppressed and socially subordinate unless removed from the suppressive cues of the colony. Due to their striking reproductive skew, naked mole-rats are often considered eusocial mammals. Consistent with this idea, there are behavioral specializations and at least some evidence for morphological distinctions within and between the breeding and non-breeding members of the colony. Importantly, naked mole-rats show plasticity in their behavioral phenotype whereby changes in the social environment influence expression of both type and amount of social behavior. Thus, naked mole-rats provide the opportunity to examine the proximate mechanisms controlling individual differences in social behavior, shedding light on how mammals live in complex social groups.
Citations
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Journal ArticleDOI
TL;DR: The naked mole-rat (Heterocephalus glaber) has attracted considerable biomedical interest not only because of its extraordinary longevity, but also because of unusual protective features (e.g. its tolerance of variable oxygen availability), which may be pertinent to several human disease states, including ischemia/reperfusion injury and neurodegeneration.
Abstract: The naked mole-rat (Heterocephalus glaber) has fascinated zoologists for at least half a century. It has also generated considerable biomedical interest not only because of its extraordinary longevity, but also because of unusual protective features (e.g. its tolerance of variable oxygen availability), which may be pertinent to several human disease states, including ischemia/reperfusion injury and neurodegeneration. A recent article entitled 'Surprisingly long survival of premature conclusions about naked mole-rat biology' described 28 'myths' which, those authors claimed, are a 'perpetuation of beautiful, but falsified, hypotheses' and impede our understanding of this enigmatic mammal. Here, we re-examine each of these 'myths' based on evidence published in the scientific literature. Following Braude et al., we argue that these 'myths' fall into four main categories: (i) 'myths' that would be better described as oversimplifications, some of which persist solely in the popular press; (ii) 'myths' that are based on incomplete understanding, where more evidence is clearly needed; (iii) 'myths' where the accumulation of evidence over the years has led to a revision in interpretation, but where there is no significant disagreement among scientists currently working in the field; (iv) 'myths' where there is a genuine difference in opinion among active researchers, based on alternative interpretations of the available evidence. The term 'myth' is particularly inappropriate when applied to competing, evidence-based hypotheses, which form part of the normal evolution of scientific knowledge. Here, we provide a comprehensive critical review of naked mole-rat biology and attempt to clarify some of these misconceptions.

47 citations

Book ChapterDOI
TL;DR: The African mole-rat superfamily as discussed by the authors is a unique group of underground rodents that are remarkable for their adaptations to a subterranean lifestyle and their range in sociality, spanning strictly solitary species to the most social of all rodents.
Abstract: The African mole-rat superfamily are a unique group of subterranean rodents that are remarkable for their adaptations to a subterranean lifestyle and their range in sociality, spanning strictly solitary species to the naked mole-rat, the most social of all rodents. Widely distributed through sub-Saharan Africa their occurrence is associated with the presence of food resources in the form of underground roots, bulbs and tubers, which form their staple diet. African mole-rats have an ancient Oligocene/Eocene origin, with the naked mole-rat, the extant species with the earliest divergence from the common ancestor of the clade. As a consequence of its early evolution the naked mole-rat appears to have acquired many extraordinary biological features, even when compared with other mole-rats. Molecular phylogenies indicate that complex sociality and cooperative breeding has been convergently gained and/or lost more than once among African mole-rats, making them a fascinating group for comparative studies of social evolution. Ultimately, ecological constraints on digging and finding food have played a role in increasing cooperative behavior and social complexity, from what was most likely a monogamous ancestor living in family groups. Phylogenetically controlled comparisons suggest that proximate control of their lifestyle shows both conservation and divergence in the underlying mechanisms.

16 citations

Book ChapterDOI
TL;DR: The African mole-rat family (Bathyergidae) includes the first mammalian species identified as eusocial: naked mole-rats as mentioned in this paper, which are found in the oxytocin, vasopressin and corticotrophin-releasing factor (CRF) systems within the nucleus accumbens, amygdala, bed nucleus of the stria terminalis and lateral septal nucleus.
Abstract: The African mole-rat family (Bathyergidae) includes the first mammalian species identified as eusocial: naked mole-rats. Comparative studies of eusocial and solitary mole-rat species have identified differences in neuropeptidergic systems that may underlie the phenomenon of eusociality. These differences are found in the oxytocin, vasopressin and corticotrophin-releasing factor (CRF) systems within the nucleus accumbens, amygdala, bed nucleus of the stria terminalis and lateral septal nucleus. As a corollary of their eusociality, most naked mole-rats remain pre-pubertal throughout life because of the presence of the colony’s only reproductive female, the queen. To elucidate the neuroendocrine mechanisms that mediate this social regulation of reproduction, research on the hypothalamo-pituitary-gonadal axis in naked mole-rats has identified differences between the many individuals that are reproductively suppressed and the few that are reproductively mature: the queen and her male consorts. These differences involve gonadal steroids, gonadotrophin-releasing hormone-1 (GnRH-1), kisspeptin, gonadotrophin-inhibitory hormone/RFamide-related peptide-3 (GnIH/RFRP-3) and prolactin. The comparative findings in eusocial and solitary mole-rat species are assessed with reference to a broad range of studies on other mammals.

12 citations

Book ChapterDOI
TL;DR: In this article, the authors outline the captive care and unusual housing needs of these animals and provide information and examples from their own experiences while working with naked mole-rats for many decades.
Abstract: Naked mole-rats are a burgeoning model species in the field of biomedical research and are also housed at many zoos throughout the world. These mammals possess many traits that have a large impact on the way that they are kept in captivity such as their eusociality, thermolability and lack of need for drinking water. This chapter outlines the captive care and unusual housing needs of these animals. Providing information and examples from our own experiences while working with naked mole-rats for many decades. While this chapter serves as a good framework for the captive care of this mammal species, it is in no way all-encompassing but simply reflects the way in which we have managed over many years to successfully sustain our colony of thousands of animals.

12 citations

Book ChapterDOI
TL;DR: In this article, the authors highlight recent progress in understanding how and what Heterocephalus glaber hears and which vocalizations it uses, which is essential for a complete understanding of naked mole-rat cooperation, society and even culture.
Abstract: Since their discovery, naked mole-rats have been speaking to us. Early field studies noted their extensive vocalizations, and scientists who are fortunate enough to spend time with these creatures in the laboratory setting cannot help but notice their constant peeping, chirruping and grunting (Hill et al., Proc Zool Soc Lond 128:455–514, 1957). Yet, few dwell on the function of these chirps and peeps, being instead drawn to the many other extraordinary aspects of naked mole-rat physiology detailed throughout this book. Still, no biology is complete without a description of how an organism communicates. While the field of naked mole-rat bioacoustics and acoustic communication has been largely silent for many years, we highlight recent progress in understanding how and what Heterocephalus glaber hears and which vocalizations it uses. These efforts are essential for a complete understanding of naked mole-rat cooperation, society and even culture.

6 citations

References
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Journal ArticleDOI
TL;DR: The models to date have advanced understanding by suggesting possible mechanisms for division of labor and by revealing how individual and colony-level behavior may be related, and so may lead to the development of more powerful and integrative explanatory models.
Abstract: ▪ Abstract Division of labor is one of the most basic and widely studied aspects of colony behavior in social insects. Studies of division of labor are concerned with the integration of individual worker behavior into colony level task organization and with the question of how regulation of division of labor may contribute to colony efficiency. Here we describe and critique the current models concerned with the proximate causes of division of labor in social insects. The models have identified various proximate mechanisms to explain division of labor, based on both internal and external factors. On the basis of these factors, we suggest a classification of the models. We first describe the different types of models and then review the empirical evidence supporting them. The models to date may be considered preliminary and exploratory; they have advanced our understanding by suggesting possible mechanisms for division of labor and by revealing how individual and colony-level behavior may be related. They s...

767 citations

Journal ArticleDOI
01 May 1981-Science
TL;DR: Laboratory observations on a field-collected colony of 40 Heterocephalus have shown that only a single female breeds, which together with long life-spans, overlap of generations, cooperative brood care, and possible age polyethism provide parallels with the eusocial insects.
Abstract: Laboratory observations on a field-collected colony of 40 Heterocephalus have shown that only a single female breeds. The remaining individuals constitute two or three castes, each containing both sexes and distinguishable by size differences and the tasks they perform. These features, together with long life-spans, overlap of generations, cooperative brood care, and possible age polyethism provide parallels with the eusocial insects.

603 citations

Journal ArticleDOI
18 Apr 1996-Nature
TL;DR: The discovery of a dispersal phenotype that may occasionally promote outbreeding in naked mole-rats is reported, suggesting that, although rare, a dispersive morph exists within Naked mole-rat colonies.
Abstract: CLOSE inbreeding is known for a variety of small mammal species1–4 for which a high probability of mortality during dispersal makes helping and delayed maturation a relatively secure fitness option5. Prolonged inbreeding, however, is usually associated with lowered fitness6,7, and it has been shown that most highly inbred small mammals8 and social insects9 have inbreeding-avoidance mechanisms that promote some degree of outbreeding. However, previous field and laboratory research on the naked mole-rat (Heterocephalm glaber) suggested that this cooperatively breeding rodent is highly inbred10–12, with new colonies forming by fission13. Here we report the discovery of a dispersal phenotype that may occasionally promote outbreeding in naked mole-rats. These dispersers are morphologically, physiologically and behaviourally distinct from other colony members. They are laden with fat, exhibit elevated levels of luteinizing hormone, have a strong urge to disperse, and only solicit matings with non-colony members. These findings suggest that, although rare, a dispersive morph exists within naked mole-rat colonies.

301 citations

Journal ArticleDOI
TL;DR: Differences in colony cohesion, ethology and the hormonal profiles of non-reproductive animals suggests that eusociality evolved along different pathways in these two phylogenetically divergent genera of the Bathyergidae.
Abstract: Extensive field and laboratory studies show that Damaraland mole-rats, like naked mole-rats, have an extreme form of vertebrate sociality. Colonies usually contain 2 reproductives and up to 39 non-breeding siblings, 90% of whom live a socially-induced lifetime of sterility; they remain in the natal colony, forage for food, defend the colony and care for successive litters. Although there is heightened dispersal following good rainfall, the majority of adult non-reproductives remain in their natal colony and failure to disperse is not directly attributable to habitat saturation or unfavourable soil conditions. A major dispersal event follows the death of a reproductive. Differences in colony cohesion, ethology and the hormonal profiles of non-reproductive animals suggests that eusociality evolved along different pathways in these two phylogenetically divergent genera of the Bathyergidae.

269 citations