Physiology& Behavior, Vol. 47, pp. 831-835. ©Pergamon Press plc, 1990. Printed in the U.S.A.

0031-9384/90 $3.00 + .00

Prolonged Copulatory Behavior Facilitates Pregnancy Success in the Musk Shrew A N N I E L. C L E N D E N O N A N D E M I L I E F. R I S S M A N 1

Departments o f Biology and Psychology, University of Virginia, Charlottesville, VA 22903 R e c e i v e d 27 N o v e m b e r 1989

CLENDENON, A. L. AND E. F. RISSMAN. Prolonged copulatory behaviorfacilitates pregnancy success in the musk shrew. PHYSIOL BEHAV 47(5) 831-835, 1990.--Female musk shrews (Suncus murinus) are sexually receptive and actively seek contact with males during the first ten days of pregnancy. In the series of experiments reported here we examined the effects of prolonged copulatory behavior on pregnancy success. Females received multiple ejaculations either on the same day or over the course of up to six days. When ejaculations were distributed over an interval of several days, the number of females delivering litters was significantly increased. The same outcome was found regardless of whether the trlrst fertile mating was followed by subsequent copulations with normal or vasectomized males. One ejaculation followed by daily contact with soiled bedding taken from a male's cage did not increase pregnancy rates. Three ejaculations received over a three-day interval caused significantly more females to ovulate than three ejaculations given on the same day. The results demonstrate that prolonged copulatory behavior, which includes vaginocervical stimulation, facilitates ovulation and pregnancy in this species. Pregnancy

Induced ovulation

Musk shrew

Receptivity

FEMALE mammals have been categorized according to whether or not ovulation is induced by vaginocervical stimulation associated with mating. Most female mammals used in the laboratory exhibit spontaneous ovulatory cycles. During the course of the estrous, or menstrual cycle, ova are released, regardless of whether mating has taken place, and around this time females exhibit sexual behavior. Whether or not copulations have occurred, sexual behavior terminates within a few hours after its onset, only persisting for a small portion of the total duration of the cycle. In the event of a successful mating and pregnancy, estrous cycles cease and females remain sexually unreceptive throughout pregnancy. Rats, for example, are receptive for about 15 hours during the 4-5 day estrous cycle if they do not mate, and for a slightly shorter length of time (10-12 hours) if mating occurs (11,12). Likewise, female hamsters allow males to mount for 12 to 20 hours starting on the evening of proestrous (6,7). Sexual receptivity is abbreviated when complete copulation or vaginocervical stimulation occurs (5,19). A few notable exceptions to this rule are seen in primates. Female rhesus monkeys and humans often allow copulations throughout the menstrual cycle as well as during pregnancy (21, 28, 30, 33). In a number of other mammals, intromissions received during mating stimulate the neuroendocrine events associated with ovulation. After a successful mating females exhibiting induced ovulation often remain sexually receptive for a longer period of time than do females that ovulate spontaneously, Cats are receptive for six days after ejaculations that result in ovulation (31). The latency with which female ferrets approach males in a " T " maze

Sexual behavior

Implantation

remains the same until several days after mating, suggesting that proceptivity continues after ovulation has occurred. Likewise the demonstration of receptive behavior does not begin to decline for three days after mating in pseudopregnant ferrets (29). Prairie voles (34), New Zealand white and California rabbits (2,3) continue to mate for 24-30 hours after ejaculations that cause either pregnancy or pseudopregnancy. The musk shrew (Suncus murinus) is an induced ovulator (10). Nonpregnant females allow males to mount daily for at least two weeks. Once females have mated successfully, they continue to exhibit sexual behavior (including allowing males to mount and ejaculate) for at least the first third of their 30-day pregnancy (26). Even after this, up to 40% of females tested on any given day of pregnancy will allow males to mount. This pattern of behavior is also demonstrated under testing conditions where nonpregnant and pregnant females are able to choose whether or not they interact with a male (Clendenon and Rissman, unpublished data). The experiments presented here were designed to examine the possible function of this extensive copulatory behavior in the female musk shrew. METHOD

Animals Musk shrews used in these studies were born and raised in our colony at the University of Virginia. The colony founders were provided in 1985 by Dr. G. L. Dryden and were descended from

1Requests for reprints should be addressed to Dr. E. F. Rissman, Department of Psychology, Gilmer Hall, University of Virginia, Charlottesville, VA 22903.

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animals trapped on Guam Island in the early 1960s. The colony is maintained on a light cycle of 14 L: 10 D (lights on at 0600 EST) at a temperature of 23-4-Ioc. Animals are provided with food (Purina Cat Chow and Complete Mink Pellets, from Mink Specialty Products, New Holstein, WI) and water ad lib. Female musk shrews in these studies were individually housed (cage dimensions: 28 × 17x 12 cm) after weaning (18-20 days of age) with pine wood shavings and paper towels for bedding. Between the ages of 40-50 days virgin females were randomly assigned to groups for use in these experiments. Stimulus males used in these studies were proven breeder males (vasectomized males were former breeders). Males were housed individually (cage dimensions: 44 × 24 x 14 cm) and were not used for testing during the 48 hours prior to a test session that included an ejaculation to ensure adequate sperm counts. In all experiments, pairing occurred in the male's cage. Females receiving multiple ejaculations were mated to different males on each occasion. Starting 28 days after their first mating females were checked once daily in the morning (0800-1200) for the presence of litters. Pregnancy lasts for 30-32 days in this species (the day of mating is designatcd as day 0).

Experimental Designs In Experiment 1, females (N = 58) received ejaculations based on one of the five different mating schedules. Females in group I received one ejaculation ( N = 11). Females in group 2 received two ejaculations on the same day within a 4-hour period (N = 11). Animals in group 3 received three ejaculations on one day (N = 12). Females in group 4 received two ejaculations over the course of two days, each ejaculation was separated by 48 hours (N = 13). Finally, females in group 5 received three ejaculations over the course of four days, again each was separated by 48 hours (N---11). All mating occurred between 2000 and 2400 hr. Red lights (two 25-watt bulbs) were on at all times to facilitate behavioral tests conducted in the dark. Females in Experiment 2 (N = 47) received ejaculations according to one of four different mating schedules. Females in group 1 received one ejaculation ( N = 11). Females in group 2 received one ejaculation daily for six consecutive days (N = 12). Animals in group 3 received one ejaculation on the first day, and one ejaculation daily for the subsequent five days from vasectomized males (N = 12). Females in the final group received one ejaculation with a vasectomized male on the first day, an additional ejaculation the next day from a normal male, followed by daily ejaculations with vasectomized males for the next four days (N = 12). All mating occurred between 0800 and 1200 hr. In Experiment 3, females (N = 46) received ejaculations and other types of contact with a male according to one of four different schedules. Females in the first group received one ejaculation (N = 13). Females in group 2 received one ejaculation on the first day of the experiment, followed by a daily ejaculation, with a vasectomized male, for five days (N= 12). Females in group 3 ( N = 11) received an ejaculation: next they were paired with a male daily for five days but only received mounts. The length of the pairing period was based on the amount of time it typically takes a female to receive an ejaculation on the days subsequent to the first mating. Mounts were provided by males fitted with a gauze "apron" which covered their ano-genital region. Mounting behavior was observed and appeared normal in its timing and frequency. Females in the final group ( N = 10) received one ejaculation on the first day of the study and were subsequently placed in a cage containing male-soiled bedding daily for the next five days. These females resided in test cages for the same length of time as an average behavior test. Contact with a male or his bedding occurred between 0800 and 1200 hr.

CLENDENON AND RISSMAN

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(N

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Same Night

Different Nights

FIG. 1, Female musk shrews in Experiment t were mated either during a single time period or over the coarse of 3-5 days. Females that received 3 ejaculations on three different nights separated by 48 hours were more likely to deliver litters than females receiving 3 ejaculations on the same night (*p