Effects of age lactation and repeated cycles on rhesus monkey copulatory intervals.код для вставкиСкачать
American Journal of Primatology 721-26 (1984) Effects of Age, Lactation, and Repeated Cycles on Rhesus Monkey Copulatory Intervals MARK E. WILSON, MARGARET L. WALKER, AND THOMAS P. GORDON Yerkes Regaonal Pramate Research Center, Emory Unauersrty,Atlanta Young, sexually mature female rhesus monkeys copulate on more days prior to conception than do older females, and this prolonged discrete mating period is associated with a n earlier rise in serum estradiol prior to the first ovulation of the breeding season. The influence of repeated ovulatory cycles and the presence of a suckling infant on the copulatory patterns were examined in two separate analyses. Extending previous work, young, nulliparous females copulated on more days at the first ovulation of the breeding season than did older, multiparous females. However, the duration of the copulatory period a t the second ovulation of the breeding season was similar and significantly shorter for both age groups. Furthermore, the presence of a suckling infant did not influence the duration of the mating periods in adult, multiparous females. The onset of copulatory behavior for all females was associated with serum estradiol concentrations of approximately 90 pg/ ml, indicating that the age and cycle differences in the duration of the copulatory periods are due to the time course of serum' estradiol prior to ovulation. A separate, longitudinal analysis of the duration of the mating period associated with the first ovulation of three successive breeding seasons indicated that females copulated on more days during their first ovulatory cycle of their first breeding season. These data indicate that the copulatory interval is longer for females during the first ovulation of the breeding season, and this pattern is accentuated in young, sexually mature animals. Key words: copulation, age, repeated cycles, rhesus monkey INTRODUCTION Female rhesus monkeys living in outdoor environments exhibit discrete periods of copulatory behavior associated with conceptions during the annual mating season [Lindburg, 1971; Carpenter, 19421. This behavior is related to the hormonal condition of the female [Gordon, 19811, as copulations begin during the follicular phase, when serum estradiol (Ez) levels rise, and then cease abruptly following ovulation, when concentrations of serum progesterone increase [Wilson et al, 1982aI. The duration of this mating period is age-dependent, since young females, a t their first ovulation, copulate on more days prior to conception than older females [Wilson and Gordon, 19801, and this longer period of copulation is related to a n earlier rise in serum Ez [Wilson et al, 1982131. These data indicate that the first ovulation of the Received December 24, 1983; accepted March 20, 1984 Address reprint requests t o Mark E. Wilson, Yerkes Regional Primate Research Center of Emory University, Field Station, 2409 Collins Hill Road, Laurenceville, GA 30245. (Q 1984 Alan R. Liss. Inc. 22 Wilson, Walker, and Gordon breeding season is both behaviorally and physiologically different for young, sexually mature females. Since these age differences were observed at the first ovulation for young females in their first breeding season, it is not known how the mating pattern changes with subsequent ovulations within the same breeding season or during the first ovulation of successive breeding seasons. Further, in the original study, the older female group comprised animals resuming ovulation following parturition and lactation. Since the events of lactation may have antigonadotropic effects [Plant et al, 1980; Schallenberger et al, 19811, the observed age differences in serum E2 and copulatory patterns could be accounted for by lactation in adult females and not by some characteristic of young females. In order to understand better the influence of age on the hormonal induction of female sexual behavior, the present study examined the duration of female copulatory periods during the first and second ovulatory cycles of the breeding season for young, nulliparous females and older, multiparous females who were either lactating or nonlactating. Furthermore, a longitudinal analysis of a separate group of females examined the changes in the duration of the discrete copulatory periods a t the first ovulation of successive breeding seasons. METHODS Female rhesus monkeys (Macaca m ulatta) housed in outdoor compounds served as subjects. Females lived in social groups containing many adult males, females, and juveniles. Each outdoor- compound, with a n enclosed area of either 30 m x 30 m or 38 m x 38 m, had attached indoor quarters. Animals were given commercial monkey feed twice daily and received a daily supplement of fresh fruit, Effects of Repeated Cycles and Lactation The influence of repeated ovulatory cycles and lactation on the duration of female copulatory periods was examined in 16 animals: five females 3.5 years of age who had not ovulated previously and 11 multiparous females 5.5-10.5 years of age. Females were housed with vasectomized males so that pregnancy was prevented. Collection began in September 1981 prior to the beginning of the breeding season. At that time, the 11multiparous females were lactating, as evidenced by the presence of suckling infants born the previous spring. The average age of the infants at the outset was 4.2 & 0.2 months (n = 11;X 5 SE). Behavioral observations were made 2 hr per day, 6 days per week through the first two ovulatory cycles of the breeding season. Observations were begun each day at 0900 hr following feeding. In the present environment, this sampling protocol provided data on female copulatory patterns identical to that obtained from all-day, 9-hr sampling (unpublished observations). The 11 multiparous females were observed again the following breeding season, beginning in September 1982 when they were not lactating. Behavioral data were collected through the first two ovulatory cycles of this breeding season. During observational sessions, all occurrences of male-female copulations resulting in ejaculations were recorded. Vaginal swabs were obtained 6 days per week to monitor menstruation. Blood samples (5 mlj were obtained from unanesthetized animals 2 days per week as described earlier [Walker et al, 19831. Harvested serum was analyzed by radioimmunoassay for Ez and progesterone [Wilson et al, 1982aI. Ovulation was inferred from sustained elevations in serum levels of progesterone > 2 ng/ml. Longitudinal Changes in Copulatory Periods Copulatory behavior of 13 female rhesus monkeys housed with intact males was examined in three successive breeding seasons, from their first ovulation at 3.5 Copulatory Periods in Female Rhesus 23 years of age to 5.5 years of age. During the second breeding season at 4.5 years of age, 11of 13 females were lactating; during the third breeding season at 5.5 years of age, four of the 13 females were lactating. Lactation was again inferred from the presence of suckling infants born the previous spring. Behavioral observations of male-female copulatory behavior were collected 2-3 hr per day, 6 days per week from September through December each year. Only data from the first ovulation of each breeding season for each female were used. Ovulations were confirmed on the basis of elevations in serum progesterone > 2 ng/ml, if available, or by backdating 168 days from parturition [van Wagenen, 19721. Analyses The duration of the discrete copulatory period, defined by the number of consecutive days a female engaged in copulations, was obtained for each female. All grouped data were expressed as X 2 SE. DiDTerences in the duration of copulatoiy behavior or serum Ez levels at the initiation of behavior between age groups and across ovulatory cycles were evaluated by analysis of variance with repeated measures. Serum E2 concentrations associated with the onsct of copulatory behavior were determined from the first hormone value following the initiation of behavior. Since previous data had demonstrated that young females exhibit a longer discrete period of copulations, specific differences between age groups were evaluated with planned comparisons [Keppel, 19731. All statistical values having a P < 0.05 were considered significant. RESULTS Effect of Repeated Cycles Age differences in the duration of copulatory periods were only evident at the first ovulation of the breeding season. As illustrated in Figure 1, young females 4 I -20 . -15 I -10 -5 2nd Ovulation Menses 1st Ovulation 4 4 1 1 0 5 . 10&5 -10 -5 I m 0 5 Days from Copulatory Offset Cx Fig. 1. Duration of the copulatory periods ? SE)for both age classes of females at the first and second ovulation of the breeding season. Data are aligncd to the last day of copulatory behavior (Day 0 ) a1 each ovulation. Also shown arc thc intcrvcning mcnstruation interval. 24 Wilson, Walker, and Gordon copulated on more days at the first ovulation (F1,14 = 5.73; P < 0.05). In contrast, all females copulated for a similar number of days at the second ovulation ( F I J ~< 1.0; P > 0.05). The finding of no age differences during the second ovulation resulted from a significant reduction in the length of the copulatory period for young females (F1,4 = 12.4; P < 0.05). In addition, multiparous females showed a significant reduction in the number of days on which they copulated at the second ovulation of the breeding season (Fl,lo = 11.4; P < 0.05). Thus, young females were observed to copulate on more days only during the first ovulatory cycle of the breeding season, with the duration of the copulatory period a t the second ovulation similar and significantly reduced for both age groups. All females began copulatory activity when serum EZ levels reached approximately 90 pgiml. Serum E2 associated with the onset of copulatory behavior was similar a t the first and second ovulation for both young (1st: 93.4 8.4 and 2nd: 99.9 4.2 pgiml) and multiparous females (1st: 85.4 k 4.8 and 2nd: 92.9 +_ 4.2 pgf ml). No age (F1,14< 1.0) or repeated cycle ( F 1 , ~ 4 = 1.17) differences in serum E2 concentrations following the onset of copulatory behavior were evident. Effects of Recent Lactation A recent lactational period did not influence the duration of the copulatory intervals for multiparous females. The length of the copulatory period during the first (12.9 k 1.2 days) and second ovulatory cycles (9.7 5 0.8 days) of the breeding season for nonlactating females was similar to that observed the previous year following a recent lactation (Fig. 1; 1st: 12.5 k 1.0 days; 2nd: 8.5 f 1.1days; F1,lo < 1.0). However, as in the previous year, the copulatory period during the second ovulatory cycle was significantly shorter than the period associated with the first ovulation (Fl,lO = 6.52; P < 0.05). Also, serum levels of EZwere similar at the outset of copulatory behavior whether the females were nonlactating (83.4 3.2 pg/ml) or lactating 85.4 k 4.8 pg/ml; t l o = 0.86). Longitudinal Changes in Copulatory Periods When female copulatory periods were examined across successive breeding seasons, the duration was found to be longest a t initial ovulation. As illustrated in Table I, the copulatory period associated with the first ovulation of the first breeding season was significantly longer than the first ovulation of the second or third breeding season (F124 = 13.80; P < 0.05). The duration of the mating periods during TABLE I. Mean(& SE) Number of Days on Which Females Copulated During the First Ovulation of Three Successive Breeding Seasons From 3.5 to 4.5 Years of Age 3.6 A11 females (n = 13) Lactating only Nonlactating only 19.5 a (+ 2.1) Age category years 4.5 5.5 13.3 12.9 (i1.2) (+ .8) 12.9 14.3 (i1.4) (+ 1.1) n=ll 15.5 (+ 2.5) n=4 n=2 "Significantly higher compared to successive years, P < 0.05. 12.3 (* 1.1) n=9 Copulatory Periods in Female Rhesus 25 the second and third breeding seasons was similar (F1,24 < 1.0) and characteristic of that of other adult females (Fig. 1). Further analysis revealed that those females who were lactating copulated on a similar number of days compared to nonlactating females during both the second breeding season a t 4.5 years of age (tll = 0.69) and the third breeding season a t 5.5 years of age (TI1 = 1.03). DISCUSSION The present analysis indicates that previously demonstrated age differences in the duration of female copulatory periods are limited to the first ovulation of the breeding season when young females experience their initial ovulation. The length of subsequent copulatory periods is significantly shorter and does not differ from that of fully adult females. This is true of the second ovulation of this first breeding season as well as the first ovulation of the second and subsequent breeding seasons. Furthermore, although lactation may delay the resumption of ovulations [Walker et al, 1984; Schallenberger et al, 19811, once the ovulatory process is initiated, the recent experience of lactation has no influence on the duration of mating periods in adult females. Thus, the observed differences in the length of copulatory intervals associated with the first ovulation of the breeding season are age-dependent. In addition to this age effect, the copulatory period was significantly reduced a t the second ovulatory cycle of the breeding season for multiparous females as well. Since females copulate on a similar number of days following the Ez peak at ovulation regardless of age [Wilson et al, 1982b1, the age and cycle differences observed in the present study are likely due to a n earlier rise in serum EZprior to first ovulation in both young and older females. These data thus indicate that the hormonal profile associated with the first ovulation of the breeding season is characteristically different from that observed in subsequent cycles for both young, nulliparous females and multiparous females. Following a period of summer and/or lactational anovulation, the first ovulation of the breeding season for adult females is characterized by a gradual increase in basal serum levels of gonadotropins followed by serum Ez, some 20-30 days prior to ovulation [Walker et al, 19841. Progesterone levels do not rise until about two days following the E2 peak. Subsequent ovulations during the breeding season [Walker et al, 19831 are then similar to those observed in regularly cycling, laboratory-housed females. Typically, a relatively fixed follicular phase of 10-12 days is followed by a luteal phase of 15-18 days [Wilks et al, 19791. Since female copulatory behavior [Wilson et a1 1982al or other aspects of female or male sexual behavior [Wallen et al, 19831 are restricted in the present environment to periods when E2 is greater than 80-90 pgiml and progesterone is low, the length of the copulatory period of subsequent ovulations is limited to the 10- to 12-day follicular-periovulatoryphase. On the other hand, copulatory behavior prior to the first ovulation of the breeding season begins whenever serum Ea levels exceed 80-90 pg/ml and are not constrained by the inhibitory influences of progesterone. Superimposed on the time course of hormone levels between the first and second ovulation of the breeding season is a developmental effect. The long period of follicular maturation indicated by elevations in serum E2 is simply enhanced for young females at their initial ovulation [Wilson et al, 1982133. This suggests that increases in basal levels of serum gonadotropins begin even earlier in young females prior to the first ovulation. Furthermore, from analyses done on sheep, i t has been suggested that the neuroendocrine mechanisms that control the seasonal resumption of ovulation in adults are analogous to those that control the occurrence of first ovulation a t the completion of puberty [Karsch & Foster, 19811. The present data would support this hypothesis for rhesus monkeys, since the first ovulation of the 26 Wilson, Walker, and Gordon breeding season for both young and multiparous females is characterized by an extended period of elevated EZ levels that is presumably due to a gradual increase in gonadotropin stimulation. Thus, these data suggest a commonality in the physiological control of puberty onset and the seasonal resumption of ovulation in rhesus monkeys. CONCLUSIONS 1. Age differences in the duration of rhesus female copulatory periods are restricted to the initial ovulation of the first breeding season for young females. 2. Although the copulatory period is longer for young females a t the first ovulation, the period shortens significantly a t the second ovulation of the breeding season for both young and older females. 3. A recent lactational period has no influence on the duration of the copulatory period for adult females. 4. These data suggest a commonality in the physiological control of puberty onset and seasonal resumption of ovulation in rhesus monkeys. ACKNOWLEDGMENTS We thank M.A. Smith for her technical assistance and L. Wright for her editorial assistance. This work was supported by grants from NIH RR00165 and HD16305 and NSF BNS13181. REFERENCES Carpenter, C.R. Sexual behavior of free-ranging rhesus monkeys. JOURNAL OF COMPARATIVE PSYCHOLOGY 33:113-142, 1942. Gordon, T.P. 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