Advances in
THE STUDY OF BEHAVIOR VOLUME 14
Contributors to This Volume JAMES R. ANDERSON MARTHA K. MCCLINTOCK
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Advances in
THE STUDY OF BEHAVIOR VOLUME 14
Contributors to This Volume JAMES R. ANDERSON MARTHA K. MCCLINTOCK
HANUS PAPOUSEK MECHTHILD PAPOUSEK HOWARD TOPOFF MICHEL VANCASSEL
Advances in
THE STUDY OF BEHAVIOR Edited by
JAY S. ROSENBLATT Institute of Animal Behavior Rutgers University Newark, New Jersey
COLINBEER Institute of Animal Behavior Rutgers University Newark, New Jersey MARIE-CLAIRE BUSNEL Laboratoire de Physiologie Acoustique Institut National de la Recherche Agronomique Jouy en Josas (78350), France PETER J. B. SLATEU Ethology and Neurophysiology Group School of Biological Sciences The University of Sussex Brighton, England
VOLUME 14 1984
ACADEMIC PRESS, INC. (Harcourt Brace Jovanovich, Publishers)
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ISBN 0-12-004514-1 PRINTED IN THE UNITED STATES OF AMERICA 84 85 86 87
9 8 7 6 5 4 3 2 I
Contents
Contributors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Announcement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
vii ix xi
Group Mating in the Domestic Rat as a Context for Sexual Selection: Consequences for the Analysis of Sexual Behavior and Neuroendocrine Responses MARTHA K. MCCLINTOCK
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
.. ..... . .. .. . 111. Behavioral Units of Analysis: Robustness and Redefinitions . . . . . IV. New Individual Behaviors . . . . . , . . . . . . . . . . . . . . . . . . . . . . . . . . 11. The Social Pattern of Mating in Groups and Pairs
V. The Social Structure of Mating: Selection within and of Groups. . VI. Classic Mating Behaviors in a Social Context. . . . . . . . . . . . . , . . . VII. Panogamy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2 3 8 13 20 32 39 42
Plasticity and Adaptive Radiation of Dermapteran Parental Behavior: Results and Perspectives MICHEL VANCASSEL
I. II. 111. IV. V.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The Development of Parental Behavior. . . . . . . . . . . . . . . . . . . . . . The Adaptive Radiation of Parental Behavior. . . . . . . . . . . . . . . . . Relationship between Development and Adaptive Radiation . . . . . The Study of Parental Behavior: Illustration of Which Theories? . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . V
51 52 58 63 74 78
vi
CONTENTS
Social Organization of Raiding and Emigrations in Army Ants HOWARD TOPOFF I. 11. I11 . IV . V. VI .
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Phylogeny and Systematics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nomadic Behavior and Brood-Stimulation Theory . . . . . . . . . . . . . Behavioral Ecology of Chemical Communication . . . . . . . . . . . . . . Empirical Tests of Brood-Stimulation Theory . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
81 83 85 88 99 120 123
Learning and Cognition in the Everyday Life of Human Infants HANUS PAPOUSEK AND MECHTHILD PAPOUSEK
I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11. Some Fundamental Principles of Cognitive Integration . . . . . . . . . 111. The Relevance of Dyadic Interactions: Concluding Remarks . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
127 130 157 159
Ethology and Ecology of Sleep in Monkeys and Apes JAMES R . ANDERSON
I. 11. I11. IV . V. Vl . VII . VII1 . IX . X.
/tidf..r .
introduction . . . . . . . . . . . ....................... Where Do Primates Sleep'. . . . . . . . . . . . . . . . ........... Sleeping Sites as a Limiting Resource . . . . . . . . . . . . . . . . . . . . . . . Sharing and Competition for Sleeping Sites . . . . . . . . . . . . . . . . . . Characteristics of Sleeping Sites . . . . . . . . . . . . . . . . . . . . . . . . . . . Traditional Sleeping Sites and Security . . . . . . . . . . . . . . . . . . . . . . Arrival, Sleeping Postures, and Nighttime Activity . . . . . . . . . . . . Social Aspects of Sleeping . . . . . . . . . . . . . . . . . . . . . . . . . . . . Awakening and Leaving the Sleeping Site . . Concluding Comments . . . . . . . . ..... References . . . . . . . . . . . . .......................
.................................................................... Cot7icwr.r of Previous Vnl~rmes ..................................................
166 166 170 174 177 188 194 201 208 215 216
231 235
Contributors Numbers in parentheses indicate the pages on which the authors' contributions begin.
JAMES R. ANDERSON, Department of Psychology, University of Stirling, Stirling FK9 4LA, Scotland (165) MARTHA K. MCCLINTOCK, Department of Behavioral Sciences, University of Chicago, Chicago, Illinois 60637 ( I ) HANUS PAPOUSEK, Developmental Psychobiology, Max-Planck Institute for Research in Psychiatry, 0-8000 Munich-40, Federal Republic of Germany (127) MECHTHILD PAPOUSEK, Developmental Psychobiology, Max-Planck Institute for Research in Psychiatry, 0-8000 Munich-40, Federal Republic of Germany (127) HOWARD TOPOFF, Department of Psychology, Hunter College of the City University of New York, New York, New York 10021, and The American Museum of Natural History, New York, New York 10024 (81) MICHEL VANCASSEL, Laboratoire d Ethologie, LA 373 CNRS, Universite'de Rennes I , 35042 Rennes Cedex, France (51)
vii
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Preface The aim of Advances in the Study of Behavior is to serve the increasing number of scientists who are engaged in the study of animal behavior by presenting their theoretical ideas and research to their colleagues and to those in neighboring fields. Since its inception in 1965, this publication has not changed its aim, to serve ". . . as a contribution to the development of cooperation and communication among scientists in our field." We acknowledge that in the interim new vigor has been given to traditional fields of animal behavior by their coalescence with closely related fields and by the closer relationship that now exists between those studying animal and human subjects. Scientists studying animal behavior now range from ecologists to evolutionary biologists, geneticists, endocrinologists, ethologists, comparative and developmental psychobiologists, and those doing research in the neurosciences. As the task of developing cooperation and communication among scientists whose skills and concepts necessarily differ in accordance with the diversity of phenomena that they study has become more difficult, the need to do so has become greater. The Editors and publisher of Advances in the Study of Behavior will continue to provide the means to meet this need by publishing critical reviews, by inviting extended presentations of significant research programs, by encouraging the writing of theoretical syntheses and reformulations of persistent problems, and by highlighting especially penetrating research that introduces important new concepts.
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s Dr. Peter J. B. Slater of England has been invited to be an Editor and we are pleased that he has accepted the position beginning with this volume. With his appointment we continue to have an English representative. We hope, therefore, to maintain the international representation among both our readers and contributors established by earlier volumes.
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ADVANCES IN THE STUDY OF BEHAVIOR, VOL. 14
Group Mating in the Domestic Rat as a Context for Sexual Selection: Consequences for the Analysis of Sexual Behavior and Neuroendocrine Responses MARTHAK. MCCLINTOCK DEPARTMENT OF BEHAVIORAL SCIENCES UNIVERSITY OF CHICAGO CHICAGO. ILLINOIS
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11. The Social Pattern of Mating in Groups and Pairs . . . . . . . . . . . . . . . . . . . . . A. The Sequence of Copulation . . . . . . . . . . . . . . . . . . . . . . . . . 111. Behavioral Units of Analysis: Robustness and Redefinitions A. The Ejaculatory Series . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
A.
B. C.
Male Rece Female So Female Intercep
..........................................
2 3 3 7 8 8 10 13 13 13 19 19
V.
VI.
The Social Structure of Mating: Selection within and of Groups A. Intrasexual Selection: Competition. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Intersexual Selection: Mate Choice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Cooperation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D. Sexual Selection at the Group Level.. . . . . . . . . . . . . . . . . . . . . . . . . , . Classic Mating Behaviors in a Social Context.. . . . . . . . . . . . . . . . . . . . . . . . A. Multiple Intromissions and Multiple Ejaculations. . . . . . . . . . . . . . . . . . B. Male Postejaculatory Quiescence. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Sensory Regulation of Copulation .............
. . . . . . . . . ............................ ..................... References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . , . , 1
20 21 26 28 30 32 32 33 34 38 39 39 40 42
Copyright Q 1984 by Academic Press. Inc. All rights of reproduction in any form reserved ISBN 0-12-0345 14-1
MARTHA K . MCCLINTOCK
I.
INTRODUCTION
In the rat (Rattus nonpegicus), behavior and neuroendocrine function are reciprocally linked in the control of reproduction. Species-typical mating behavior is the product of underlying neuroendocrine mechanisms. In turn, the neuroendocrine events necessary for ovulation, ejaculation, sperm transport, and implantation are triggered or modulated by specific patterns of copulatory behavior. There are many aspects of this reciprocal relationship that are puzzling, if not paradoxical. Some of the confusion may stem from a focus limited to the study of rats mating in pairs. Although domestic rats are sometimes bred in pairs, it is not the social context which most breeders generally use. More commonly, rats have been selected for high reproductive output when they mate in groups (Charles River Breeding Laboratories, Inc., In lirt.). Therefore, the study of rats in groups may resolve some of the seemingly paradoxical aspects of behavior and neuroendocrine function. Domestic rats are clearly adapted to group living. Even when there is room for dispersal in a cage, they often huddle together in a corner (see Fig. 1). They can recognize individuals and establish a variety of social relationships within the group, including dominance (Barnett, 1975). Therefore, given that a group is one of the social contexts in which the mating system of the Sprague-Dawley strain has been selected, it is likely that social relationships are an important factor in determining the individual’s pattern of copulation. Thus, an analysis of the social control of copulation will be an integral part of understanding the reciprocal relationship between individual behavior and neuroendocrine function. The breeding practices of some breeders have inadvertently imposed sexual selection at both the individual and the group level. At the individual level, mating in a group presents the opportunity for two forms of sexual selection: competition and mate choice. Females are subjected only to this level of sexual selection. Although a female conceives in a group along with several other females, she does not remain with these same females throughout her reproductive lifespan. Her reproductive performance can be monitored on an individual basis because the maternity of her litters is obviously always known. Therefore, if a female conceives and delivers a full set of healthy pups, she is eventually returned to the breeding colony and placed with the first available group. Maies. on the other hand, are selected at both the individual and the group level. Sexual selection is imposed at the group level when males are kept together as a group throughout their reproductive lives and remain in the breeding colony or get discarded solely on the basis of their reproductive output as a group. Presumably, discarding the entire group is more cost effective than determining which member, if any, is responsible for a decrease in the number of offspring sired by the group as a whole. Nonetheless, this does have the effect of
GROUP MATING IN THE DOMESTIC RAT
3
FIG. 1. A huddle or pile-up of domestic rats living in a group cage.
group selecting males for reproductive performance (albeit in a weak form; Arnold and Wade, personal communication). It is this sex difference in the breeding practices that represents a form of sexual selection at the group level. The purposes of this article are therefore twofold. The first is to use the social context of group mating to reevaluate the units of behavior that are appropriate for the study of mating behavior and neuroendocrine function in the Norway rat. The second purpose is to evaluate the ways that sexual selection at both the individual and the group level is mediated by copulatory behavior, which in turn triggers the neuroendocrine mechanisms required for successful reproduction in the domestic strain.
11. THE SOCIALPATTERNOF MATINGIN GROUPSAND PAIRS A.
THE SEQUENCE OF COPULATION
When rats mate in pairs, the sequence of copulatory events obviously must be the same for the male and female (see Fig. 2). The male mounts the female many times when she is in estrus, achieving an intromission during most mounts. The male thrusts rapidly during an intromission, then dismounts and immediately grooms his penis. The pair then separates and each rat may briefly explore the environment, eat or drink before coming together again for another mount and
4
MARTHA K . MCCLINTOCK
PAIR
I11
[
Interintromission Interval
’ Ejaculatory Series
1
Postejaculatory Interval PEI
intromission. After several intromissions, the male ejaculates and becomes quiescent. He usually sits or lies on the ground, urinates and emits a 22-kHz ultrasonic call. After a while, the pair resumes mating and begins the next ejaculatory series. The pair may have as many as seven ejaculatory series before the copulatory sessions ends. This pattern of copulation is remarkably stereotyped whether a pair mates in the small enclosure of a standard laboratory testing cage ( I ’ X 2’) or in a larger seminatural environment containing a burrow system. Wild rats also mate in a similar pattern (McClintock and Adler, 1978). The pattern of copulation is strikingly different when rats mate in groups. Females and males change partners repeatedly in the midst of copulation in a
5
GROUP MATING IN THE DOMESTIC RAT
mating system termed panogamy (see Section VI1,A). Therefore, males and females do not experience the same sequence of copulatory events as they must when they mate in a pair (see Fig. 3). Social interactions during copulation create a sex difference in the pattern of copulation. Although these interactions are complex, they result in a pattern of copulation that is elegantly coordinated with the neuroendocrine mechanisms of successful reproduction from both the male and the female perspectives (McClintock and Anisko, 1982; McClintock et al., 1982a,b).
c
9,
111
91
PE I
d*
PEI
* 0
INTROMISSION EJACULATION
FIG. 3. A schematic of the sequence of copulation during group mating at a 2:3 sex ratio. The male and female sharing a copulatory event are connected by a horizontal line. To see the sequence of copulation from the perspective of one of the individuals, follow down that individual’s column. The time line only indicates the order of events, not the intervals between them. (Reprinted from McClintock et al., 1982a.)
6
MARTHA K. MCCLINTOCK
During group mating at sex ratios ranging from 2:l-2:4, males change partners after an intromission. Their intromissions are spread evenly (not randomly) among the estrous females of the group. That is, they are significantly more likely to mate with a different female than would be expected if the sequence of partners were random (see Fig. 3; McClintock er a / . , 1982a). In contrast, females are not likely to change partners between successive intromissions. However. after an ejaculation, they usually do change partners and resume mating with the other male (McClintock er a / . , 1982a,b; Thor and Flannelly, 1979). Males and females both take turns during group mating in a way that is consonant with the pattern of changing partners. They do this at different points in the copulatory sequence. Males take turns between themselves after they have ejaculated (when there are two males in the group). Thercfore, there is only one male mating with the estrous females of the group at a given time (see Fig. 3). After a male has ejaculated and returned to his resting spot, the other male usually approaches him to within one body length. The approaching male ignores solicitations from the females until he has made his approach and only then begins to mate, copulating until he ejaculates, whereupon the first male resumes mating. Therefore, each male has one or two complete ejaculatory series during the postejaculatory quiescent period of the other male. Females also take turns mating more frequently than randomly expected; that is, they are less likely to mate twice in a row than they would in a random sequence (see Fig. 3). However, in contrast to the males, females take turns after receiving an intromission; there is no alternation pattern after receiving an ejaculation. In general, it appears that the social pattern of copulation results more from turn-taking within a sex than it does from active attempts to change mating partners. Female rats tend to solicit and mate with whichever male is available. They seldom approach the male that is “out-of-turn.” Likewise, males tend to follow the closest soliciting female. There are exceptions to this generalization. For example, 78% of all cases in which a male mated out-of-turn resulted from a female soliciting a male that was sitting in his resting place (McClintock er a / . , 1982a). As will be discussed in Section V,B, exceptions such as these provide evidence for mate choice and sexual selection. Nonetheless, turn-taking within a sex is striking, particularly because it is observed at a variety of sex ratios (2: 1 , 2:2, and 2:4; McClintock er al., 1982a). Female turn-taking has also been observed at sex ratios of 1:5 (Tiefer, 1969) and 1:2 (Krames and Mastromatteo, 1973). However, male turn-taking may not be as stable when more than two males are in a group (e.g., 3:4). Furthermore, it is not observed among males that have not been living together prior to mating (Thor and Carr, 1979) and may well not be as striking when there is more space in which to monopolize females.
GROUP MATING IN THE DOMESTIC RAT
7
AND ITS PATTERNOF COPULATION B. TEMPORAL FUNCTIONS NEUROENDOCRINE
Rats must have several intromissions during copulation in order to trigger the males’ ejaculation and the females’ progestational state. Both the male and the female neuroendocrine systems are exquisitely sensitive to the timing of intromissions so that there are optimal intervals for triggering both of these neuroendocrine events. Surprisingly, the optimal intervals for the two sexes are not the same. From the male perspective, a 3-min interval is the most efficient for achieving ejaculation (Larsson, 1956; Bermant, 1964; Bermant et al., 1969). When intervals are either shorter or longer, more intromissions are needed to reach his ejaculatory threshold. From the female perspective, however, the optimal intervals for inducing a progestational state are substantially longer. Females are more likely to enter the progestational state when intromissions are spaced at 10 to 15 min (Edmonds et al., 1972). When intromissions are paced at these long intervals, males may never ejaculate (Larsson, 1956). When rats mate in pairs, intromissions are paced at 1-min intervals (Beach, 1956; Dewsbury, 1967a), a temporal pattern that is not optimal for triggering either ejaculation or the progestational state. Furthermore, it is not even a compromise between the two optimal intervals. When rats mate in groups, copulation is timed in a pattern that does match the optimal patterns for triggering ejaculation and the progestational state (McClintock and Anisko, 1982). This is because males and females can take turns mating and change partners so that the sequence and timing of copulation is no longer the same for males and females (compare Figs. 2 and 3). Intervals between intromissions are significantly shorter for males than they are for the females (see Fig. 4). Furthermore, there is a sex difference in temporal dependence of the rate of copulation. Males pace intromissions at a relatively constant rate that does not change markedly with the passage of time. Females pace intromissions at a slower rate and this rate decreases as time passes since the previous intromission. Furthermore, the intervals that are optimal for triggering neuroendocrine events are slightly more probable than other intervals. This is particularly true when the animals do change partners and the timing of their behavior is not as constrained by the temporal preferences of their original partner (see Fig. 5). A male is more likely to mate at intervals of approximately 3 min and also at 1 to 1.5 min than he is to mate at other intervals (see Fig. 6). The 3-min interval is optimal for reaching ejaculatory threshold. It is also the interval at which spinally transected males have spontaneous erections (Hart,1968), possibly reflecting the temporal pattern of the spinal mechanisms of male sexual behavior. The shorter interval (1- 1.5 min) may reflect the temporal parameters of CNS control of the initiation of copulation in males. It corresponds to the interval between mounts
MARTHA K . MCCLINTOCK
- 99 --- dd
0
10
20
30
40
50
60
70
80
90
100
110
Time t Interintromission I n t e rvals (min )
FIG. 4.Sex differences in the rate of copulation during group mating. In log survivor analysis. a cumulative distribution of intervals is plotted on a log scale. This method is used because the steepness of the slope of the survivor plot at time f is proportional to the probability of a behavioral event at time f since the previous event, and hence to the rate of behavior (Fagen and Young, 1978; Lee, 1982). (Figure redrawn from McClintock and Anisko, 1982.)
when a male mates with a tethered female that is prevented from affecting the pace of copulation (Larsson, 1973). It is also the length of mount bouts when males are prevented from intromitting (Sachs and Barfield, 1970; Lodder and Zeilmaker, 1976). Females, on the other hand, are particularly likely to mate at 10- to 15-min intervals (see arrow in Fig. 5). These intervals were found to be effective in inducing the progestational state necessary for implantation (Edmonds et a/., 1972j. Furthermore, intromissions paced at 6-min intervals were slightly lcss effective for inducing a progestational state; these intervals are relatively less common during group mating. Therefore, the pattern of group mating is well coordinated with both the temporal requirements of the neuroendocrine rellexes that are triggered by copulation and with its neural mechanisms. 111.
BEHAVIORAL UNITS OF ANALYSIS: ROBUSTNESS AND REDEFINITIONS
THEEJACULATORY SERIES The ejaculatory series is one of the fundamental units of analysis for mating behavior in the rat. In the male, the ejaculatory series has been used to quantify sexual motivation and to document its endocrine and neural mechanisms (Beach, A.
9
GROUP MATING IN THE DOMESTIC RAT
1956; Caggiula et al., 1973; Dewsbury, 1968a; Hart, 1968; Sachs and Barfield, 1976). In the female, it has been used as an independent variable to quantify her receptivity and assess the neuroendocrine consequences of copulation (Adler, 1969; Chester and Zucker, 1970; Connor and Davis, 1980; Lanier et al., 1979; Thor and Can, 1979). During group mating, the ejaculatory series is a robust unit of analysis for male sexual behavior. Males begin with an intromission and continue mating, usually without interruption, until they ejaculate. Furthermore, the males take turns mating, alternating at the end of an ejaculatory series, indicating that the behavioral unit is also robust at the social level of analysis. However, from the female perspective, the ejaculatory series has no meaning as a unit of analysis. In startling contrast with the sequence of copulation from the male perspective, females do not experience a regular sequence of mounts, intromissions, and ejaculations. The total number of copulatory events had by females in the group is the same as the males’; it must be. But the sequence from the female perspective is completely different (see Fig. 3 and compare the sequence of events in the male and female columns). The variance in the number of intromissions before ejaculation is five times greater than that of the male’s (McClintock and Anisko, 1982; see Section IV,B for a discussion of female units of analysis that are robust). This suggests that several tacit assumptions underlying the analysis of female
100
d
-different
50
1
I 0
% 10
, 20
30
40
50
60
Time t Interintromission Intervals (min )
FIG.5. The effect of changing partners on the rate of copulation. Note that intervals between intromissions > 3.5 min are not likely when males change partners and mate with a different female. From the female perspective 10- to 15-min intervals are particularly likely when females change partners. (Figure redrawn from McClintock et al., 1982a.)
10
MARTHA K. MCCLINTOCK
10
'
0
1
2
3
1
I
4
5
Time t
interintromission i n t e r v a l s ( m i n )
FIG 6. Distribution of intervals between intromissions of a single male (2BS) during group mating. Notc that 1- and 2.5- to 3-min interval\ are particularly likely. (Figure redrawn from McClintock and Anisko, 1982.)
sexual behavior should be reassessed. For example, it is often assumed that the intromissions must occur prior to ejaculation in order to induce sperm transport. Nonetheless, most females in a group become pregnant even when they do not receive stimulation in the ordered pattern of an ejaculatory series, suggesting that sperm transport may also be triggered during an ejaculation or afterward. Another example is the literature on mechanisms of sperm competition and its role in sexual selection. To date, controlled studies of sperm competition have assessed paternity only when the ejaculations from competing males were separated by complete ejaculatory series (Dewsbury and Hartung, 1980). In order to fully understand sperm competition in a biologically meaningful context, the types of copulatory sequences should be expanded to include those that occur during group mating (e.g., two ejaculations in a row without intervening intromissions). B.
THE OFTIMALPACEFOR TRIGGERING EJACULATION
1 . The Optimul Intervul befiveen Intromissions
Larsson (19.56, 19.59)quantified the optimum copulatory interval for bringing male rats to ejaculation. He enforced different copulatory intervals by using a partition to keep the male and female separate until a predetermined time had elapsed. Several different investigators have used this technique and identified the optimum interval as approximately 3 min. These findings have been used to build a model of the time course of net excitation relative to the ejaculatory threshold (Sachs and Barfield, 1976).
GROUP MATING IN THE DOMESTIC RAT
11
A similar relationship is found between the pacing and number of preejaculatory intromissions even when the pace of mating is not artificially controlled (see Fig. 7A). In our studies, the probability of intervals of different lengths was biased by giving males (both domestic and wild) the opportunity to mate with either a wild or a domestic female. Furthermore, pairs were tested in both standard testing cages and a seminatural environment. Long intervals are more likely when the female is of the wild strain and also when mating takes place in a large seminatural environment. A bias toward short intervals occurs when the male is paired with a domestic or a wild postpartum female (McClintock, unpublished observations) and also by mating in a small standard testing cage. Data from these various conditions demonstrate a relationship between the pacing and number of preejaculatory intromissions that is almost identical to that reported by Larsson (1956). Other investigators have manipulated the interval between intromissions using a variety of techniques and failed to alter the number of preejaculatory intromissions (Beach et al., 1956; Bermant, 1964; Caggiula, 1972; Dewsbury, 1968b; Sachs and Barfield, 1974). If anything, lengthening the interval decreased rather than increased the number of preejaculatory intromissions (Beach et al., 1955; Caggiula and Vlahoulis, 1974; Larsson, 1963). This suggests that some experimental treatments, such as shock, may change more than the interval between intromissions; they undoubtedly alter the ejaculatory threshold as well, obscuring its relationship to the pace of copulation. 2.
The Cost of Ejaculation
During group mating, intromissions are not likely to be paced at intervals greater than 3-3.5 min. In fact, almost every analysis of male sexual behavior, including the effect of dominance and changing partners, indicated that intervals greater than 3.5 min were not likely to occur (McClintock et al., 1982a; see Fig. 5 and 12 for examples of inflection points in a log survivor curve). In other words, intervals that are greater than the optimal value for triggering ejaculation are less likely to occur under almost every social circumstance. This suggests that intervals longer than 3.5 min are particularly costly. The “cost” of a particular interval between intromissions can be measured in terms of the time it takes to reach ejaculation [sometimes called the ejaculatory latency (Dewsbury, 1967b)l. Figure 7B plots the cost (in time to reach ejaculation) as a function of the interval between intromissions and is based on the ejaculatory threshold curve in Fig. 7A. It is immediately obvious that variation in intervals up to the optimum length have little effect on the cost of ejaculation. Up to the optimal interval, an increase in the time between intromissions is compensated by reaching ejaculation after fewer intromissions (see Fig. 7B). However, when intervals are longer than the optimum, the cost climbs exponentially as intervals become longer. It is these longer intervals that are rare from the male’s
12
MARTHA K . MCCLINTOCK
A
L 1.0
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S.0
7.0
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TIME t INTERINTROMISSION INTERVALS (min)
B
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..De-1.. 2, 179- 184. Field, T. M . . Woodson. R.. Greenberg. R.. and Cohen. D. (1982). Discrimination and imitation of facial expression\ by neonates. Scirrice 218, 179- 18 I . Fisher. C B.. Fcrdinandsen. I