of the assay a fte r day 26, and this female did not develop a p erfo rate vagina during this initial period o f ovarian activity. In contrast, female 100 appeared to immediately take on the role o f the new breeding queen, with vaginal perforation occurring within 12 days. This female underwent two ovarian cycles between days 16 and 76 (Figure 5.6), then conceived a t the following oestrus and gave birth on day 143. The seven pups th a t were born in this fir s t litte r were all successfully reared. Conception occurred again at the following post-partum oestrus period, and female 100 gave birth to a second litte r o f approximately eight pups, four o f which were successfully reared. A fte r these pups were weaned, female 100 developed an abscess on the jaw, which may have resulted from a bite wound. A fte r fully recovering from this, female 100's position as queen was challenged by female 97, who killed her in a fight on day 291 and subsequently became the new breeding female (Figure 5.6).
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FIGLff?E 5.6 - U r i n a r y p r o g e s t e r o n e p r o f i l e s ( • ) f o r f e m a l e s 100 , 9 7 & 102 f r o m C o l o n y N . D a y 0 c o r r e s p o n d s t o t h e d a y w hen t h e p r e v i o u s q u e e n , b r e e d i n g m a le a n d o t h e r c o l o n y m e m b e rs d ie d t o l e a v e t h e s e t h r e e f e m a l e s , a n d f o u r m a le s . B = b i r t h o f l i t t e r . B o d y m a s s e s a t v a r i o u s t i m e s a r e i n d i c a t e d by t h e f i g u r e s in p a r e n t h e s e s , a = V a g i n a i m p e r f o r a t e . A = V a g i n a p e r f o r a t e . j 9 1 0 0 71# 423 0 -
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Prior to the death o f female 100, there appears to have been some loss of suppression among the non-breeding adult females. Female 102 had elevated urinary progesterone on days 101 and 124, and had a p erfo rate vagina on days 124 and 194, indicating that this animal was also becoming reproductively active. A fte r her initial small peak in urinary progesterone, female 97 was imperforate and acyclic until day 248, when progesterone was detected in a urine sample. In addition, this female had gained considerable mass, such that on day 193, her body mass had increased from 3 0.8g on day 0, (the average adult body mass), to reach a maximum o f 55g, an increase o f 178%. Although no further urine samples were obtained from this female a fte r day 248, her vagina was p erfo rate by day 265, implying that she was reproductively active, and 26 days later she became the new queen a fte r killing female 100. By this time the signs o f reproductive activation in female 102 had ceased, and her vagina became imperforate again (Figure 5.6).
5.4 DISCUSSION
The results o f this study show that in non-breeding female naked mole- rats, the socially-induced block to reproduction is due to a failure o f these females to ovulate, and th at this physiological state is also a characteristic o f non-breeding females in wild populations o f naked mole-rats. Histological examination o f the reproductive tra c t o f wild and captive females confirmed this hypothesis, because the ovaries o f non-breeding females tacked both pre ovulatory follicles and corpora lutea, in contrast to those o f breeding queens (see Chapter 4; Jarvis, 1990 a). The low plasma LH concentrations measured in non-breeding females, in comparison to those in breeding females, provides circumstantial evidence that the failure o f ovulation may be due to insufficient secretion o f LH from the anterior pituitary. This latte r point is further investigated in Chapter 7. Although single plasma samples do not give information regarding pulse frequency and amplitude o f LH secretion, the consistency o f low LH levels found in non-breeding females suggested that either LH pulse frequency or amplitude, or both were reduced in these females. In the common marmoset monkey, suppressed pituitary LH secretion due to an inhibition of hypothalamic GnRH release has been shown to be the central mediating fa c to r responsible fo r the suppression o f ovulation in socially-induced in fe rtility found in subordinate females (Abbott et al., 1988).
While these and other studies (B rett, 1986, 1990 b; Lacey & Sherman, 1990) show that reproduction is normally restricted to one breeding female, rare exceptions may occur. Jarvis (1990 a) has recorded instances o f captive colonies that have contained two queens at some time in their history, and that these females have co-existed fo r a period o f time. In one case a colony had two breeding females fo r a period o f five years, and although many litters were born (15 to one female, and 16 to the other), pup survival was low, and only 16 out o f an estimated 540 pups were reared (Jarvis, 1990 a). The significance o f these observations in captivity is not clear, but it is interesting to speculate that in the wild, this type o f phenomenon may trigger colonies to split into new colonies.
The ovarian cycle o f the naked mole-rat with its long luteal phase o f approximately 28 days, is similar to that reported fo r other hystricomorph rodents. In guinea-pigs, the corpus luteum o f an un-mated, non-pregnant female secretes progesterone fo r 15-17 days (Weir & Rowlands, 1974). Total cycle lengths are relatively long in hystricomorph rodents e.g. the cuis, Galea musteloides (22 days), chinchilla, Chinchilla laniger (40 days), and acouchi, Myoprocta p r a tti (3 0 -5 5 days) (Tam, 1974), in contrast to the short 4-day ovarian cycles o f myomorphs like the mouse and ra t (Short, 1984).
The presence o f large quantities o f luteal tissue during pregancy in the naked m ole-rat (see Plates 4.2 & 4.3, Chapter 4), is consistent with the detection o f sustained high levels o f urinary progesterone over the 72-day gestational period (Figure 5.4). Other hystricomorphs also show structural and functional modifications o f the ovary in the form o f accessory corpora lutea, which may enhance progesterone secretion fo r the maintenance o f pregnancy during the relatively long gestational periods (Tam, 1974; see Chapter 4). Concentrations o f progesterone during gestation d iffe r greatly between species. In rats, plasma progesterone levels rise to reach a maximum during the second half o f pregnancy, then drop prior to parturition (Heap & Flint,
1984). This is similar to the naked mole-rat (Figure 5.4). A completely differen t picture is seen in guinea pigs, however, where a large increase in plasma progesterone over th at in the non-pregnant state, reaches a maximum mid-term. The circulating progesterone levels then decline and rise again prior to parturition (Heap & Flint, 1984). In naked mole-rats, prolonged high levels o f urinary progesterone (in excess o f 40 days, Figure 5.4) normally distinguish the pregnant female from the regular oscillations found in non-pregnant, cycling females (Figure 5.5), and the constantly undetectable levels found in
non-breeding females (Table 5.1, Figure 5.1). The one exception to this was female 38 (Figure 5.3), who, unaccountably, had elevated urinary progesterone fo r at least 80 days while not being pregnant.
Although fe rtility is normally completely inhibited in non-breeding female naked m ole-rats whilst they remain in their colony, results from this study show that if the social environment is manipulated, fo r example by separating females from their parent colonies, then ovarian cyclicity may commence in as little as 7 days. As the follicular phase o f the cycle was calculated as 6.0 + 0.6 days (Figure 5.2), then this implies that the process o f ovarian activation is occurring within the fir s t one or two days o f separation. Pregnancy can also occur rapidly in previously non-breeding individuals, as shown by three o f the females separated which underwent one cycle a fte r being paired with a male, then at the following period o f oestrus became pregnant (e.g. females 4 and 29, Figure 5.5). The observation that four out o f the five singly housed females underwent what appeared to be normal cycles, together with the fa c t that breeding queens always solicit mating behaviour (Jarvis, 1990 a) suggests that the naked mole-rat may be a spontaneous ovulator. Among other hystricomorphs, both the guinea-pig and the chinchilla are known to be spontaneous ovulators (Weir &t Rowlands, 1974).
The age and body mass o f the females a t the time o f separation had no apparent e ffe c t on the onset o f cyclicity, with comparatively young (5 months), small (23g) females giving similar results to older animals (up to 28 months age). This illustrates that reproductive activation in female naked mole-rats may occur over a wide range o f ages and body sizes, an observation that has also been noted by Jarvis (1990 a).
Reproductive activation o f a non-breeding female was also rapid in the converse situation to separation, that is, when the queen o f a colony died, exemplified by female 100 in Colony N. In this case, vaginal perforation occurred between 7 and 14 days a fte r the death o f the previous queen, and two ovarian cycles followed before conception (Figure 5.6). An initial 'switch on' o f ovarian function in female 97 appears to have been suppressed, presumably by female 100, once the la tte r female commenced ovarian cyclicity. At this time females 97 and 100 had a similar body mass. Over the days that followed, however a fascinating sequence o f events unfolded. Both non breeding females 97 and 102 increased dramatically in body mass, and exhibited signs o f ovarian activity, reflected in elevations o f urinary progesterone concentrations, and developed p erfo rate vaginas. However, female
97 emerged as the more dominant individual, reaching a maximum body mass o f 55g, while in female 100, the non-pregnant body mass had only increased slightly from 30.8 to 3 4 .5g. Female 102 was still comparatively small and had reverted back to being imperforate and acyclic. Female 97 then killed female
100 and took over as the new breeding queen.
Although only a single example, it is interesting to compare this activation and take over by a non-breeding female in a colony with reproductive activation in separated females. While ovarian cyclicity and pregnancy commenced within similar time periods in both situations, large increases in body mass were not observed in females separated from their colonies. For example, in the cases where females were housed singly, then paired with a male, body masses increased by approximately 10% a fte r 12 weeks o f separation (84 days). In a similar time period in Colony N, female 97 body mass rose from 35 to 55g, an impressive increase of 57%. These results suggest that in the colony situation, it is fast-growing individuals that are possible contenders fo r the position o f queen. This phenomenon has also been reported by Jarvis (1981), Jarvis et at. (1990), and Lacey and Sherman (1990).
The rapid onset o f reproduction in non-breeding female naked m ole-rats removed from their colonies is remarkable, given the complete suppression imposed on non-breeders th a t remain in their colonies, which apparently continues fo r their entire lifespan (Jarvis, 1990 a). Naked m ole-rat colonies have been kept in excess o f 15 years in captivity (Jarvis, 1990 a), yet some still retain the original breeding queen. Therefore, although most m ole-rats may never breed, it is important th a t new breeding females can be recruited quickly if required, fo r example if the queen dies, or if a group is separated from the parent colony. In the la tte r case, fa s t recruitment o f young may be crucial to the survival o f the colony, because below a certain group size the energy expended by the animals in digging and foraging, will exceed the food resources that a small group can exploit (B rett, 1986). This situation arises because the habitat o f the naked mole-rat is characterised by hard, dry soil, and the large geophytes (roots and tubers) upon which they feed often tend to be widely dispersed (Jarvis, 1971, 1985; B rett, 1986; Lovegrove & Wissel, 1988). In such habitats where geophyte densities are low, Lovegrove and Wissel (1988) have developed a mathematical model which quantifies the relative risks o f foraging. They calculate that the risk o f one burrowing naked mole-rat not encountering a geophyte a fte r digging a distance o f 3 m
is 41 times greater than when 10 animals are digging and foraging. Therefore,