The 'hairless' gerbil: a new mutant
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1 Laboratory Animals (1980) 14, The 'hairless' gerbil: a new mutant HEIDI H. SWANSON Department of Anatomy, Medical School, University of Birmingham, Vincent Drive, Birmingham, B15 2TJ, United Kingdom Summary Although the animal looks bald, the smooth, warm skin is covered by fine stubble. The vibrissae also appear broken off short. The nails appear normal and the ventral scent gland and nipples are well developed. This female is fertile and has had several litters, but none of her offspring show the mutation. Her parents produced 2 other hairless gerbils in subsequent litters, but these did not survive past S weeks. Histological examination revealed marked pathology of hair development, although the number of follicles seemed normal. The thymus was disorganized and sparsely populated with lymphocytes. 'Hairless' mutants have been known in various species of mammals for many years. Examples are found in cattle, goats and dogs (Mohr & Wriedt, 1928), mice (Crew & Mirskaia, 1931) rats (Robinson, 1965) and rabbits (Castle, 1932). The character 'hairless' is usually distinguished from 'nude' in that the latter mutation refers to a congenital absence of thymus as well as hair. The nude mouse has been extensively used in immunological research (Fogh & Giovanella, 1978). The Mongolian gerbil (Meriones unguiculatus) was introduced as a laboratory animal some 15 years ago (Marston, 1972), and has been bred extensively both for the pet trade and for research, primarily in the behavioural sciences. 4 mutations have recently been described (Robinson, 1973, 1980), the nonagouti (a), acromelanic albino (c h ), pink-eyed (p) and white spot (sp). The colony of the Department of Anatomy of the University of Birmingham was bred exclusively from about 50 gerbils imported from the USA by Dr John Marston in The colony now contains animals. About 50 animals are kept in pairs as breeding stock, and experimental subjects are selected from their offspring. An attempt is being made to breed more hairless gerbils. Anyone interested in obtaining the homozygous individuals (when available) or heterozygous stock animals should contact the author. Present address: NetherlandsInstitutefor BrainResearch, Ijdijk28, Amsterdam,the Netherlands. Received 29 August Accepted 13 December Emergence of hairless gerbils in the Birmingham colony 8 family groups, established from young adult pairs, have been living in indoor enclosures since March One of these pairs produced 7 litters of which 2 males and 7 females survived to maturity. It has been our general experience that when gerbils are left with their parents beyond the usual age of weaning, sexual development in the daughters is greatly delayed and breeding is suppressed (Swanson & Lockley, 1978). In the colony under study, none of the daughters bred and from behavioural observations it seems likely that the founding father sired all the young born to the founding mother. Hairlessfemale 1 A litter was born in this enclosure on 6 July Some weeks later it was observed that one of the females was completely bald. Her 2 sisters had normal hair. The hairless animal (Fig. I), although smaller than her siblings, seemed to be healthy. Gerbils possess a ventral scent gland controlled by sex hormones (Owen & Thiessen, 1973), the first appearance of which at puberty is a convenient index of sexual maturation (Swanson & Payman, 1978). The hairless female developed an active scent gland at the usual age for females of this colony, indicating normal ovarian endocrine function. At the age of 12 months, this animal weighed 80 g, which is within the normal range of females in our colony, although she looked much smaller because of the absence of hair. Her skin was a grey-purplish colour, but she had a number of black spots over the rump (Fig. 1A). The ears, feet, tail, and around the eyes and snout, were black. These areas also appear to be dark in normal gerbils, although this is not obvious because they are covered by light tan hair (Robinson, 1973). The skin of the hairless animal was smooth and very warm to the touch. It was covered by a fine stubble, the 'goose-bump' appearance on close-up (Fig. 1B) suggesting that the arrector pili muscles were normal. The vibrissae were also only short stubble. The nails appeared normal. The ventral scent gland was well developed and nipples were prominent (Fig. 1B). The behaviour of the animal was unremarkable and she seemed to be accepted in the colony. At the age of 3 months, she was removed to a cage and paired with her littermate brother. She produced a litter of 8 young on 1 January 1979, indicating that her sexual
2 144 Swanson gerbils are all naked at birth. Another litter was born on 15 February and suffered a similar fate. It was obvious that the father had not interfered with the infants. When it appeared that the female was again pregnant, it was decided that the young should be fostered as it seemed possible that her mammary glands were deficient. The hairless mice described by Crew & Mirskaia (1931), although fertile, had atrophic mammary glands and could not rear their litters. A 3rd litter was born to the hairless female on 15 March 1979 and fostered the same day. The only foster parents available had a litter already a week old, but they accepted the newborn without difficulty. The week-old litter was given to the hairless female and, to our surprise, she suckled these successfully. Perhaps she needed the stronger sucking stimulus supplied by the older pups to initiate lactation. About a week later, the offspring of the hairless female were examined, but all seemed to be growing hair. HairlessJemale 2 On 6 October 1978, another hairless femaie was born to the same parents, with 2 normal female littermates. This animal lived for 5 weeks, but on 9 November was found dead. The cause of death was not obvious, although she had always been rather small and delicate. Samples of thymus, spleen, and skin from various parts of the body, were fixed in Bouin's fluid and prepared for histology. Specimens from a normal gerbil of the same age were taken for comparison. Skin samples were stained with Masson's trichrome, using celestin blue as nuclear stain, so that pigment granules would not be masked by the usual brown or black haematoxylin. Longitudinal sections of the 'hairless' follicles were, of course, difficult to obtain. A few were found in many sections, but critical orientation of blocks proved impossible, even for the 'hairless' vibrissa pads. Fig. J. 'Hairless' gerbil. Adult female hairless gerbil. Ventral view of same animal showing scent gland and mammary glands. behaviour was normal and that she was accepted by her brother as a mate. It has been reported that in a strain of hairless mice, the hairless females are rejected by normal males but are mated by hairless males, although normal females will accept hairless males (Crew & Mirskaia, 1931). Although our hairless female built a nest and gathered the young into it, they were all found dead the next day. It was not possible to ascertain whether any would have been hairless, as Fig. 2. Hair follicles. A longitudinal section of hair shaft from the skin of the back of a normal gerbil, showing well-organized medulla and hair shaft. B similar follicle of 16 day old hairless gerbil. The medulla is disorganized and the hair shaft varies in diameter. Pigmem granules are irregularly dispersed. C sections of hair follicles in a transverse section of the tail of a J 6 day old hairless gerbil. There are few bulbar mitoses, hair shafts are of varying diameter, and one plug can be seen in the centre top follicle. D section of the whisker pad of a normal 16 day old gerbil, showing an accessory vibrissa follicle in telogen/early anagen. The variation in fibre diameter is due to section-plane artefact. E similar section of an accessory vibrissa follicle (at the edge of a sample) from whisker pad of a 16 day old hairless gerbil. Note the plug and the variation in fibre diameter. F Quasi-sagittal section of a normal vibrissa follicle from a 16 day old gerbil. Note the flame-shaped dermal papilla. Mitoses are present in the matrix and external root sheath. G largest diameter section of a vibrissa follicle bulb from a 16 day old hairless gerbil. The bulbs are twisted and irregular, and the distortion of dermal papilla shape is obvious. Stained with Masson's trichrome and celestine blue.
3 F
4 146 Swanson Hairless male 1 On 19 December 1978, a hairless male was discovered in a litter born to another breeding pair in the colony. This animal, which also seemed small and weak, survived for only 2 weeks, and tissues were taken for histology. Pedigree There was a common ancestor on both the maternal and paternal sides of the family of the hairless females. This same ancestor also appeared on both sides of the family of the hairless male. Although the evidence is scanty, one could surmise that this is a simple recessive mutation, which was present in the homozygous condition in the hairless individuals. It is possible that hairless individuals had been born previously, but were not recognized because they died before the age at which they would have been expected to grow hair. The early death of 2 of 3 hairless individuals identified suggests that the condition is associated with impaired vigour, although the surviving female is healthy and fertile. Attempts are presently being made to produce additional homozygous animals by breeding the parents and siblings of the hairless animals. The absence of hairless individuals in the present litter of the hairless female (comprising 6 young) suggests that the brother with whom she is mated does not carry the recessive mutant gene. It is of course possible that as the gene spreads through the population, more hairless individuals will appear. Histology Skin Skin samples of a 16 day old hairless gerbil were compared to those of a normal animal of the same age. Hair follicles with sections of shaft could be seen in all skin areas, but comparison of Fig. 2A (normal) and 2B (hairles's) illustrates the extent of disorganization in the mutant. Hyperkeratinization of the skin surface is obvious (Fig. 2C) and pieces of hair shaft, outer root sheath and other follicle debris are engaged in the thick epidermal keratin. The abnormalities are particularly obvious in the vibrissae: comparison of Fig. 2D (normal) and Fig. 2E (hairless) illustrates the irregularity in shaft diameter and the presence of plugs of 'keratin pearls' which occlude the follicles. Even the 1st generation of fibres are affected and the pathological change is still continuing at the dermal papilla/matrix--<:ompare Fig. 2F (normal) and Fig. 2G (hairless) whisker follicles. There did not seem to be any difference in the histological appearance of the skin between hairless animals at 2 and 5 weeks of age. Thymus Since the lack of hair is associated with congenital absence of the thymus in the mouse and other 'nude' mammals, the appearance of the thymus and other lymphatic tissue was of special interest. Both the hairless gerbils that died possessed a thymus (Fig. 3), although it had a distinctly abnormal histological appearance (Fig. 3A, B). While the normal thymus consists of a cortical area heavily infiltrated with lymphocytes and a less dense medulla, no differentiation into regions is apparent in the hairless animals. The whole organ is sparsely populated with lymphocytes, so that many epithelial elements are visible. Since thymus involution may follow stress, the abnormal appearance of this organ in hairless animals may reflect the fact that they had died of unknown causes before being autopsied. On the other hand, an abnormality in the immune mechanism may have contributed to the death of the animals. Fig. 3. Thymus. A thymus of 16 day old normal gerbil. B thymus of 16 day old hairless gerbil. Stained with haematoxylin and eosin. Spleen The spleen of the hairless animals also seems to show a scarcity of lymphocytes, so that the typical white pulp nodules are not obvious. This suggests that the aminals do indeed have a lymphoid deficiency and that the appearance of the thymus does not merely represent a response to the stress of their terminal illness.
5 The 'hairless' gerbil: a new mutant 147 Discussion It has been suggested that the symbol hr (hairless) should be used to designate this mutation, to conform with similar symbols in other rodents (Robinson, 1973 and personal communication). The hairless (hr) mutation is distinguished from the nude (nu) in that the latter is associated with athymy (Fogh & Giovanella, 1978). The hairless mutation which has appeared in the Birmingham gerbil colony differs from that described in the mouse (Crew & Mirskaia, 1931; Fogh & Giovanella, 1978) and the rat (Robinson, 1973). In those species hair starts to grow normally, but is replaced less and less successfully at each subsequent moult. The gerbil fails to grow the 1st coat of hair. The scarcity of emergent hair and the broken-off stubble of both body hair and whiskers is confirmed by the histological study. Shafts of varying diameters, and frequent 'pearls' of keratin can be seen in foliicle sections. The number of follicles seems normal but no count was made. Even in the 1st generation (16 days) this disorganization appears not to permit the emergence of continuous fibres. However dermal papiliae are present, and of normal cell number, even if distorted in shape. Attribution of the fault in fibre integrity to epidermal, dermal or dermal papillary components is not possible from the histological appearance, transplants between animals would be necessary (Robinson, 1965). While dermal papillae seem fairly normal, directing suspicion to ectodermal reactivity, the presence of normal nails, sebaceous, mammary and scent glands makes a general ectodermal deficiency unlikely. Although some hyperkeratinization is seen in histological sections, the gross appearance of the skin is fairly smooth. The hairless mutation in most animals is usually associated with some debility resulting in early mortality, impairment of fertility and deficient lactation (Crew & Mirskaia, 1931; Robinson, 1965). Since athymy associated with hairlessness in the mouse-the nude (nu) mutation-was not discovered until 1966 (Fogh & Giovanella, 1978), some of the mutants described in the early literature may also have suffered from thymic deficiency, which may have accounted for their early death. The fitness and long survival (now over a year) of the hairless female gerbil under conventional laboratory conditions suggests that it must have a normal immune mechanism. However, the death in infancy of the other mutants, as well as the histological appearance of the thymus and spleen, suggests that there may be a variable degree of abnormality in the lymphomyeloid system. Acknowledgements The author would like to thank Dr Jack Cohen, Department of Zoology, University of Birmingham, for his help in the preparation and interpretation of the histological sections of the skin. References Castle, W. E. (1932). The furless rabbit. Journal of Heredity 24, Crew, F. A. E. & Mirskaia, L. (1931). The character 'hairless' in the mouse. Journal of Genetics 25, Fogh, J. & Giovanella, B. C. (eds) (1978). The nude mouse in experimental and clinical research. New York: Academic Press. Marston, J. H. (1972). The Mongolian gerbil. In The UFAW handbook on the care and management of laboratory animals, 4th ed., pp Edinburgh: Churchill Livingstone. Mohr, O. L. & Wriedt, C. (1928), Hairless, a new recessive lethal in cattle. Journal of Genetics 19, Owen, K. & Thiessen, D. D. (1973). Regulation of scent marking in the female Mongolian gerbil (Meriones unguiculatus). Physiology and Behaviour 11, Robinson, R. (1965). Genetics of the Norway rat, pp New York: Pergamon. Robinson, R. (1973). Acromilanic albinism in mammals. Genetica 44, Robinson, R. (1980). Handbook of mammalian genetics. New York: Garland. Swanson, H. H. & Lockley, M. R. (1978). Population growth and social structure of confined colonies of Mongolian gerbils: scent gland size and marking behaviour as indices of social status. Aggressive Behavior 4, Swanson, H. H. & Payman, B. C. (1978). Social and spatial influences on puberty in the female Mongolian gerbil. In Hormones and brain development (ed. G. Dorner & M. Kawakami), pp Amsterdam: Elsevier. Die haarlose Rennmaus--eine neue Mutante H. H. SWANSON Zusammenfassung Obgleich das Tier haarlos aussieht, ist die glatte, warme Haut von feinen Haarstoppeln bedectk. Auch die Schnurrhaare sehen abgebrochen und kurz aus. Die Nagel sehen normal aus und die ventrale Duftdriise und die Zitzen sind gut entwickelt. Dieses Weibchen ist fertil und hat mehrere Wiirfe geboren, aber keines der Nachkommen zeigte diese Mutation. Von den Eltern dieses Weibchens wurden noch 2 weitere haarlose Rennmause in Folgewiirfen geboren, doch iiberlebten diese nicht langer als 5 Wochen. Obgleich die Anzahl der Haar-Follikel normal zu sein schien, zeigte die histologische Untersuchung deutliche pathologische Veranderungen der Haarentwicklung.
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