Can pseudo entrainment explain the synchrony of estrous cycles among golden hamsters (Mesocricetus auratus)?

Synchrony among golden hamsters is often cited in the menstrual-cycle synchrony literature and has recently become a paradigm for explaining menstrual synchrony in humans (L. Weller, A. Weller, and S. Roizman (1999), J. Comp. Psychol. 113, 261-268). It has also stimulated further research on synchrony in Djungarian hamsters, for which no evidence of synchrony was found (G. E. Erb, H. E. Edwards, K. L. Jenkins, L. C. Mucklow, and K. E. Wynne-Edwards (1993), Physiol. Behav. 54, 955-959). The case for synchrony in the golden hamster is reexamined in this paper. It is demonstrated, with the help of computer simulation experiments, that the experimental method used by G. Handelmann, R. Ravizza, and W. J. Ray (1980, Horm. Behav. 14, 107-115) for detecting synchrony has a critical flaw. It does not distinguish synchrony that can occur by chance (pseudo entrainment) from synchrony due to a process of entrainment. It is suggested that the apparent entrainment of estrous cycles in hamsters and the role of social dominance may be due to the stress caused by moving animals to different rooms or grouping them. Thus, because we cannot reject the possibility of pseudo entrainment as an explanation for these results, it must be concluded that there is no evidence that golden hamsters synchronize their estrous cycles. Finally, an approach is briefly outlined for testing synchrony in golden hamsters.     

Estrous synchrony in a group of African elephants (Loxodonta africana) under human care

Synchrony of estrous, and consequently of conception and birth of young, may be of adaptive significance for certain mammals. Among the species in which estrous synchrony has been suspected several times are elephants, but clear evidence is still missing. We determined estrous cycles of African elephants (Loxodonta africana) (n=4) at the Vienna Zoo, Austria, between June 2003 and January 2006 by measuring serum progesterone levels from weekly blood samples. Except for the dominant female when she was intensively lactating, all animals showed clear cycles or progesterone release with a mean period of 105.3+/-15.37 days. For most of the study period, estrous cycles were asynchronous between females. However, after re-occurrence of the progesterone cycle in the dominant female following the first period of lactation, all four females showed high synchrony of progesterone release over the two subsequent cycles. Large changes in individual period lengths indicated that synchronization was due to the adjustment of cycle length in subdominants to that of the dominant female. We used a bootstrap procedure, based on resampling measured times of progesterone peaks, to determine if this apparent synchrony could have been caused by chance alone. This statistical analysis indicated that between-individual variances of the timing of progesterone peaks were much smaller that to be expected by chance (P=0.009). This finding represents the first evidence for estrous synchrony between elephants. We discuss various hypotheses to explain the biological function of cycle synchrony in elephants.     

Influences of the adrenal gland and photoperiod on the hamster oestrus cycle

The influence of the adrenal gland and photoperiod on the adult female hamster estrous cycle was investigated. Hamsters were exposed to 14 hours of light per day and estrous cycles were monitored. Normal cycles were characterized by a copious discharge every 4th day. Hamsters were then adrenalectomized, adrenalectomized and blinded, or blinded only. Adrenalectomized/blinded hamsters were given a .2% sodium saccharine-1%(w/v) sodium chloride solution to drink which promotes long-term survival in most adrenalectomized hamsters. With blinding alone, it took from 18 to 62 days for cessation of estrous cycles. Cycles ceased in a mean of 36.2 days in blinded/adrenalectomized hamsters. After adrenalectomy only, 3 hamsters continued to show 4-day estrous cycles for at least 9 weeks in response to the long days. 6 adrenalectomized animals died due to adrenal insufficiency but displayed several 4-day estrous cycles. It is suggested that in the hamster, adrenal hormones are nonessential for the long-term expression of estrous cyclicity. However, further research is needed to determine whether adrenal hormones are capable of modulating photoperiodic time measurement or ovarian regression.     

The peripubertal golden hamster and the transition between daily and estrous cycle hormone rhythms

Transitional patterns of LH, FSH, and progesterone (P4) in the circulation were studied in peripubertal female golden hamsters. A daily rhythm, with afternoon surges of these hormones, is typical of the immature female, whereas 4-day rhythms characterize the estrous cycle of the adult. Blood samples were collected repeatedly from maturing individuals at either 1400 or 1700 h. Each animal was examined daily for the appearance of regular vaginal estrous cycles as indicated by a mucous exudate on the morning of ovulation. Between Days -10 and -5 relative to first vaginal estrus (FVE), afternoon surges of LH, FSH, and P4 were often observed. From Days -5 to -1 relative to FVE, afternoon surges of LH and FSH were less frequent, but P4 retained the daily rhythmicity until Day -2. A 4-day pattern of LH secretion, but not of FSH or P4, was established prior to FVE. To determine whether or not ovulations were occurring prior to the appearance of external vaginal estrous cycles, reproductive tracts were collected from 26-34 days of age and examined for evidence of ovulation. Of 124 females, concordance between the record of daily vaginal examinations and the examinations of the ovaries and oviducts was found in 103 cases (83%). The development of ovarian follicles was correlated with FVE in peripubertal hamsters by unilateral ovariectomy. Antral follicles were found only in the last 3 days prior to vaginal estrus.     

Glucoprivic regulation of estrous cycles in the rat

Previous research has shown that glucoprivation induced by chronic 2-deoxy-D-glucose (2DG) treatment extends estrous cycle length and disrupts reproductive behaviors in female hamsters, similar to food deprivation. Such treatment also suppresses food intake, which is reversed in male rats by reducing brain histamine levels prior to 2DG treatment. We, therefore, determined if 2DG extends estrous cycles in the female rat and if this is due to elevated brain histamine levels. We measured estrous cycle length during 2DG-induced glucoprivation, in the presence and absence of alpha-fluoromethylhistidine (FMH), a treatment that reduces brain histamine levels. Adult female rats were treated for 72 h with either saline (n = 8), 2DG (200 mg/kg S.C. every 6 h; n = 9), or FMH (100 mg/kg i.p. daily) + 2DG (200 mg/kg; n = 7). An additional group was treated with FMH (100 mg/kg i.p.; n = 5) alone. To determine if 2DG extends estrous cycles due to glucoprivation or to decreased caloric intake, a group of rats (n = 7) received a reduced diet equal to the mean daily food intake of rats receiving 2DG alone. 2DG induced more long estrous cycles compared to rats receiving saline, FMH + 2DG, or FMH alone. In rats treated with FMH + 2DG, the percentage of 4-5-day cycles was similar to that of saline-treated rats, and a high percentage of 4-5-day cycles was also observed in rats receiving a reduced diet. These data suggest that 2DG does not suppress estrous cycles through a decrease in total calorie intake, but rather by inducing glucoprivation. In addition, during 2DG-induced glucoprivation, elevated brain histamine levels contribute to the mechanism that suppresses reproductive function.     

Nonphotic phase shifting in female Syrian hamsters: interactions with the estrous cycle

Nonphotic phase shifting of circadian rhythms was examined in female Syrian hamsters. Animals were stimulated at zeitgeber time 4.5 by either placing them in a novel running wheel or by transferring them to a clean home cage. Placement in a clean home cage was more effective than novel wheel treatment in stimulating large (> 1.5 h) phase shifts. Peak phase shifts (ca. 3.5 h) and the percentage of females showing large phase shifts were comparable to those found in male hamsters stimulated with novel wheels. The amount of activity induced by nonphotic stimulation and the amount of phase shifting varied slightly with respect to the 4-day estrous cycle. Animals tended to run less and shift less on the day of estrus. Nonphotic stimulation on proestrus often resulted in a 1-day delay of the estrous cycle reflected in animals' postovulatory vaginal discharge and the expression of sexual receptivity (lordosis). This delay of the estrous cycle was associated with large phase advances and high activity. These results extend the generality of nonphotic phase shifting to females for the first time and raise the possibility that resetting of circadian rhythms can induce changes in the estrous cycle.     

Production of piglets from in vitro-produced embryos following non-surgical transfer

The objective of this study was to enhance procedures for producing piglets derived from in vitro-produced (IVP) pig embryos by non-surgical embryo transfer (ET). The effects of insertion length for the catheter, asynchrony between the age of donor IVP blastocysts and the recipient estrous cycle, and volume of transfer medium were investigated. The IVP blastocysts at 5 days after in vitro fertilization were placed into porcine zygote medium (PZM)-5 supplemented with 10% (v/v) fetal bovine serum (PZM+FBS) in a 0.25 mL plastic straw (21-40 blastocysts per straw) and then transferred into one uterine horn of recipients using the Takumi(?) catheter for deep intrauterine insertion. Successful production of piglets derived from IVP embryos was achieved following non-surgical ET when the catheter was inserted at more than 30 cm anterior to the spiral guide spirette. The efficiency of piglet production (percentage number of piglet(s) born based on the number of embryos transferred) was greater (P<0.05) in recipients whose estrous cycle was asynchronous to that of donors with a 1-day delay (8.3%) than in those with a 2-day (1.5%) or 3-day (0.9%) delay, while pregnancy and farrowing rates (10-40%) did not differ among treatments. When blastocysts were transferred into recipients with 1.0 or 2.5 mL PZM+FBS, there were no significant differences in farrowing rate (30-40%) or average litter size (4.5-6.7) between treatments. The results of the present study indicate that the insertion length of the deep intrauterine catheter and the degree of asynchrony between donor embryos and recipient estrous cycle influenced on pregnancy and birth outcome following non-surgical transfer of IVP blastocysts.     

Synchronization of ovarian cycles within and between social groups in golden lion tamarins (Leontopithecus rosalia)

Synchronization of ovarian events has been reported in a number of primate species, with the temporal resolution of synchrony ranging from the occurrence of seasonal breeding within the annual cycle to a close matching of ovarian events within a single ovarian cycle. However, ovarian synchrony has not been reported in a New World primate. The temporal association of ovarian events was examined in female golden lion tamarins (Leontopithecus rosalia) living in the same or different social groups. Ovarian cyclicity was monitored by measuring the excretion of urinary estrogen metabolites. There was a high degree of synchronization in the occurrence of urinary estrogen peaks for females in different social groups (mean peak discrepancy = 2.1 days) and in females housed in the same social group (mean peak discrepancy = 1.3 days). Contrary to previous reports on callitrichid primates, daughters housed in their natal family group exhibited cyclic patterns of urinary estrogen excretion. These findings represent the first explicit demonstration of ovarian synchrony in a New World primate, and the tight coupling of ovarian cycles in female tamarins resembles the nature of menstrual synchrony in human females.     

Depressed pituitary prolactin mRNA, prolactin synthesis, and prolactin storage after light-deprivation in female hamsters is not due to loss of estrous cyclicity alone

Pituitary prolactin (PRL) cell activity (i.e. PRL messenger ribonucleic acid [mRNA] levels, PRL synthesis, and radioimmunoassayable [RIA]-PRL), and serum RIA-PRL were measured in female golden Syrian hamsters that were (1) light-deprived and then ovariectomized before loss of estrous cyclicity, (2) light-deprived but not yet acyclic, and (3) light-deprived and ovariectomized simultaneously. The results indicate that light-deprivation can decrease PRL cell activity in ovariectomized hamsters but not in animals that continue to cycle. Thus, estrous cyclicity can be said to largely protect PRL cell activity from depressions due to light deprivation. After acyclicity/ovariectomy, however, PRL cell activity is no longer protected and light-deprivation leads to large depressions in PRL mRNA levels, PRL synthesis, and RIA-PRL beyond that caused by acyclicity/ovariectomy alone. As seen in previous studies of total light-deprivation in nonovariectomized female hamsters, we found that removing the pineal gland in conjunction with light-deprivation in ovariectomized hamsters can completely, partially, or fail to restore various measures of PRL cell activity.     

Dynamics of Estrous Synchrony in Captive Gray Mouse Lemurs (Microcebus murinus)

Estrous synchrony in seasonal breeders can in principle be based on and shaped by environmental, internal, and/or social cues. We analyzed the dynamics of estrous synchrony for the first time in a seasonal, nocturnal primate species, the gray mouse lemur (Microcebus murinus). We compared successive estrous cycles and different levels of spatial proximity over two reproductive seasons in a captive population in order to identify possible social influences on estrous synchrony. The females exhibited a marked estrous synchrony at the beginning of each reproductive season, but we found no indication of a process of socially induced synchronization among them. Females housed in the same cage/room were not more strongly synchronized than females housed in different cages/rooms. Moreover, cycles desynchronized from the first to the second estrus of the season. Estrous cycle length did not depend on age, parity, or social housing conditions, but instead mainly on the individuality of the lemurs. This individuality, shown for the first time in a nocturnal primate species, is likely to be based on an endogenous rhythm with a genetic basis. We discuss possible social advantages, e.g., communal rearing, and disadvantages, e.g., mate choice and female-female competition, of estrous synchrony for nocturnal primates living in a dispersed individualized social network, and propose that a moderate flexibility within the individual cycle lengths probably enables the females to compromise between the different socioecological pressures.     

Socially stimulated androgen surges in male hamsters: the roles of vaginal secretions, behavioral interactions, and housing conditions.

The sources of cues necessary for elicitation of androgen surges and sexual behavior in male golden hamsters (Mesocricetus auratus) were investigated. Circulating androgen levels were measured in males after interactions with other males or several types of estrous females: intact females, vaginectomized females, or vaginectomized females scented with vaginal secretions. All groups of males that interacted with estrous females demonstrated significant elevations in androgens whereas those that interacted with other males did not. Thus, the presence of vaginal secretions is not necessary for the elicitation of androgen surges in sexually experienced male hamsters. Individual differences in sexual performance were not correlated with the degree of change in androgen levels, suggesting that such hormonal responses are not graded but are all-or-none. Housing males in isolation from females did not alter either baseline androgen levels or the magnitude of androgen responses caused by interactions with females.     

Divergent reproductive endocrinology of the estrous cycle and pregnancy in dwarf hamsters (phodopus)

Progesterone (P4) and prolactin (PRL) in peripheral circulation of Siberian hamsters (Phodopus sungorus) throughout an estrous cycle and pregnancy were determined by repeated, small volume sampling from individuals housed in modified home cages. As predicted, the endocrinology of P. sungorus reproduction is similar to the rat, mouse and golden hamster and shows none of the eight distinctive features known for Djungarian hamsters (Phodopus campbelli). Specifically, in P. sungorus there is no evidence for resumption of pituitary PRL surges in late pregnancy, P4 concentrations during the differentiation of the corpus luteum on day 2 of pregnancy are higher (as opposed to lower) than concentrations on the comparable day of an unmated estrous cycle (diestrus 1), P4 concentrations increase throughout pregnancy, PRL surges are common during the estrous cycle, including a reliable surge on proestrus, and P4 plays an important role in facilitating the expression of behavioral receptivity. We conclude that 'novel' P. campbelli reproductive endocrinology has evolved since a common ancestor was shared with P. sungorus. With a time frame (the available time since the divergence of the two species) and an ecological context (known niches and behavior in the wild) these species offer the opportunity to study endocrinological evolution in progress.     

Inhibition of estrous cyclicity in golden hamsters by melatonin administration on the day of proestrus

Single injections of melatonin (25 micrograms) were administered to female hamsters, 15 minutes before lights-out (14L:10D), during either the early diestrous (day 1) or proestrous (day 4) phase of the estrous cycle. Hamsters which received melatonin only on the evening of proestrus became anovulatory by three weeks of treatment, while those that were injected with melatonin during diestrus, or administered oil on either day 1 or 4, continued to exhibit normal estrous cycles. These results indicate that quartan injections of melatonin can suppress reproductive function in female hamsters, and that the effectiveness of the injections may be dependent upon the stage of the estrous cycle at which they are administered.     

Ovarian matrix metalloproteinases are differentially regulated during the estrous cycle but not during short photoperiod induced regression in Siberian hamsters (<Emphasis Type="Italic">Phodopus sungorus</Emphasis>)

Background  

Matrix metalloproteinases (MMPs) are implicated as mediators for ovarian remodeling events, and are involved with ovarian recrudescence during seasonal breeding cycles in Siberian hamsters. However, involvement of these proteases as the photoinhibited ovary undergoes atrophy and regression had not been assessed. We hypothesized that 1) MMPs and their tissue inhibitors, the TIMPs would be present and differentially regulated during the normal estrous cycle in Siberian hamsters, and that 2) MMP/TIMP mRNA and protein levels would increase as inhibitory photoperiod induced ovarian degeneration.     

Short estrous cycles and associated serum progesterone levels in beef cows

Short estrous cycles in beef cows were investigated in two experiments. In trial 1, breeding dates from 2,854 fall-calving Angus cows were used to determine the incidence of short estrous cycles. Of 198 cycles of less than 17 days, 170 were between the first and second detected estrus. Estrous cycles of 7 to 10 days occurred more frequently (P<.005) than other short estrous cycles. Eight-day estrous cycles were most frequent. In the second experiment, calves were weaned from 25 of 33 anestrous spring-calving, crossbred Simmental cows. Compared to herdmates still nursing calves, an increased percentage of cows which had calves weaned were observed in estrus within 10 and 25 days after the date of weaning (P<.005) and a higher percentage had 7- to 10-day estrous cycles. Cows that were observed in estrus within 10 days after weaning were inseminated with Angus semen at their first estrus and with Simmental semen at their second estrus. No cows conceived on the first estrus of 7- to 10-day estrous cycles; 61.5% conceived on the second estrus. Serum progesterone was higher (P<.01) before the second estrus than the first.     

Variation of food hoarding with the estrous cycle of Syrian golden hamsters (Mesocricetus auratus)

Food hoarding was assessed in 16 adult female Syrian golden hamsters (Mesocricetus auratus) across the stages of the estrous cycle. Results show that food hoarding is depressed on the day of behavioral estrus but does not vary among the other days of the cycle. Decreases in food hoarding appear to be correlated with high levels of estrogen and progesterone. The data are consistent with the hypothesis that food hoarding, food intake, and weight gain are controlled either by the same mechanism or by similar mechanisms in some female rodents.     

Effect of bromocriptine and progesterone on the length of the ovarian cycle in 4- and 5-day estrous cyclic rats

To study the effect of prolactin and progesterone on the length of the reproductive cycle in the rat, rats of different estrous cycle length (four and five days, respectively) were injected daily (09.00 h) with either bromocriptine (1 mg/rat) or 70% ethanol vehicle (0.25 ml) from the day of estrus onward, up to the appearance of the next ovulation. Each group of rats was then (16.00, metestrus) also injected with either progesterone (4 mg/rat) or 0.2 ml of olive oil. The effects of these treatments on the length of the estrous cycle was studied by both the recording of vaginal smears daily and by direct visualization of oocyte-cumulus complexes on the ensuing day of estrus (10.00 h-12.00 h). Bromocriptine treatment shortened the length of the cycle by one day in 5-day but not in 4-day cyclic rats, while progesterone treatment lengthened estrous cycles by one day in both groups of rats. Treatment with both bromocriptine and progesterone had no effect on the estrous cycle length of 5-day cyclic rats, but did prolong in one day the cycle of 4-day cyclic rats. These facts suggest that prolactin regulates the length of the ovarian reproductive cycle in the rat through its action on the secretion of progesterone by the corpus luteum.     

Decreases in vaginal acyclicity of rats when housed with female hamsters

The effect of the presence of female hamsters on female rat reproductive cycles was assessed. This was accomplished by maintaining two colony rooms, one of which contained only female rats, whereas the other contained both female rats and female hamsters; the estrous cycles of female rats in these rooms were compared. Rats in the rat-hamster room displayed fewer periods of acyclicity than did rats in the rat-alone room. These data indicate that there can be interspecific effects on the periodicity of the rat reproductive cycle.     

Repeat breeding in dairy heifers: follicular dynamics and estrous cycle characteristics in relation to sexual hormone patterns

Repeat breeding occurs at an incidence of 10% in the Swedish dairy cow population.Evidence is available for a hormonal asynchrony around estrus in repeat-breeder heifers (RBH). This asynchrony seems to be the underlying cause for a series of dysfunctions such as prolonged standing estrus and delayed ovulation, leading to fertilization failure. For further determinations of repeat-breeder estrous cycle characteristics, seven strictly selected RBH and six virgin heifers (VH) were studied during 3-7 consecutive cycles, with particular attention paid to the estrous period. Follicular dynamics were studied by ultrasonography and related to estrous behavior and pattern of sexual hormones (progesterone, estradiol-17beta, and LH) in peripheral circulation. Mean group data were compared and a classification model was designed. The most prominent findings for RBH were prolonged duration of estrus, delayed LH peak, prolonged lifespan of the preovulatory follicle, and a late postovulatory rise in plasma progesterone. There was also a strong tendency for peri-ovulatory suprabasal progesterone levels in RBH. It is suspected that these deviations cause changes in the microenvironment of the preovulatory follicle, negatively affecting the final maturation of the oocyte. The heterogeneity of the RBH group underlines the multifactorial cause of the repeat-breeder syndrome. The VH formed a homogenous group with data varying within physiological limits. A classification model based on three characteristic variables managed to identify 81% of the VH and 79% of the RBH correctly. Results from this study propose that some heifers have general, consistent problems in synchronizing estrous events, displayed as varying symptoms in the course of consecutive estrous cycles. These subfertile animals could be classified as repeat-breeders.     

Aggression in the female golden hamster: effects of reproductive state and social isolation

To gain information on possible hormonal correlates, the aggressive behavior of intact female hamsters towards males was observed at various times during the estrous cycle, pseudopregnancy, pregnancy, and lactation. For methodological information, estrous cycle females also were tested after varying periods of social isolation. It was found that pregnant and especially lactating hamsters were more aggressive than pseudopregnant or estrous cycling females. Comparisons of days within each reproductive condition showed that aggression tended to be higher on certain days: the day preceding behavioral estrus of the estrous cycle, Day 10 of pregnancy, and the first 5 days of lactation. Except for pseudopregnancy, sexual behavior unaccompanied by aggression occurred at some time during all reproductive conditions, and both sexual behavior and aggression were found to occur together on Day 10 of pregnancy and Day 1 of lactation. The changes in aggressive behavior associated with reproductive states were attributed to increased male interest, inhibition by ovarian hormones, and facilitation by prolactin. Increasing periods of social isolation also were found to be associated with increased aggression. It was suggested that this effect, too. might have been due to increased prolactin levels.