ADVANCES IN THE STUDY OF BEHAVIOR V 14

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 Contents

Contributors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . vii
Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ix
Announcement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 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 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
11. The Social Pattern of Mating in Groups and Pairs .. ..... . .. .. . 3
111. Behavioral Units of Analysis: Robustness and Redefinitions . . . . . 8
IV. New Individual Behaviors . . . . . , . . . . . . . . . . . . . . . . . . . . . . . . . . 13
V. The Social Structure of Mating: Selection within and of Groups. . 20
VI. Classic Mating Behaviors in a Social Context. . . . . . . . . . . . . , . . . 32
VII. Panogamy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42

Plasticity and Adaptive Radiation of Dermapteran Parental

Behavior: Results and Perspectives
MICHEL VANCASSEL

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51
II. The Development of Parental Behavior. . . . . . . . . . . . . . . . . . . . . . 52
111. The Adaptive Radiation of Parental Behavior. . . . . . . . . . . . . . . . . 58
IV. Relationship between Development and Adaptive Radiation . . . . . 63
V. The Study of Parental Behavior: Illustration of Which Theories? . 74
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 78

V
vi CONTENTS

Social Organization of Raiding and Emigrations in Army Ants

HOWARD TOPOFF

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81
11. Phylogeny and Systematics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83
I11 . Nomadic Behavior and Brood-Stimulation Theory . . . . . . . . . . . . . 85
IV . Behavioral Ecology of Chemical Communication . . . . . . . . . . . . . . 88
V. Empirical Tests of Brood-Stimulation Theory . . . . . . . . . . . . . . . . . 99
VI . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 120
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123

Learning and Cognition in the Everyday Life of Human Infants

HANUS PAPOUSEK AND MECHTHILD PAPOUSEK

I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127
11. Some Fundamental Principles of Cognitive Integration . . . . . . . . . 130
111. The Relevance of Dyadic Interactions: Concluding Remarks . . . . . 157
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 159

Ethology and Ecology of Sleep in Monkeys and Apes

JAMES R . ANDERSON

I. introduction . . . . . . . . . . . ....................... 166

11. Where Do Primates Sleep'. . . . . . . . . . . . . . . . ........... 166
I11. Sleeping Sites as a Limiting Resource . . . . . . . . . . . . . . . . . . . . . . . 170
IV . Sharing and Competition for Sleeping Sites . . . . . . . . . . . . . . . . . . 174
V. Characteristics of Sleeping Sites . . . . . . . . . . . . . . . . . . . . . . . . . . . 177
Vl . Traditional Sleeping Sites and Security . . . . . . . . . . . . . . . . . . . . . . 188
VII . Arrival, Sleeping Postures, and Nighttime Activity . . . . . . . . . . . . 194
VII1 . Social Aspects of Sleeping . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201
IX . Awakening and Leaving the Sleeping Site . . 208
X. Concluding Comments . . . . . . . . ..... 215
References . . . . . . . . . . . . ....................... 216

/tidf..r .
.................................................................... 231
..................................................
Cot7icwr.r of Previous Vnl~rmes 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 In-

stitute 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 present-
ing their theoretical ideas and research to their colleagues and to those in neigh-
boring 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, geneti-
cists, endocrinologists, ethologists, comparative and developmental psycho-
biologists, and those doing research in the neurosciences. As the task of develop-
ing 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 high-
lighting especially penetrating research that introduces important new concepts.

ix
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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 contribu-
tors 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 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
11. The Social Pattern of Mating in Groups and Pairs . . . . . . . . . . . . . . . . . . . . . 3
A. The Sequence of Copulation . . . . . . . . . . . . . . . . . . . . . . . . . 3
7
111. Behavioral Units of Analysis: Robustness and Redefinitions 8
A. The Ejaculatory Series . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
10
13
A. Male Rece 13
B. Female So .......................................... 13
C. Female Intercep 19
19
V. The Social Structure of Mating: Selection within and of Groups 20
A. Intrasexual Selection: Competition. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
B. Intersexual Selection: Mate Choice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26
C. Cooperation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28
D. Sexual Selection at the Group Level.. . . . . . . . . . . . . . . . . . . . . . . . . , . 30
VI. Classic Mating Behaviors in a Social Context.. . . . . . . . . . . . . . . . . . . . . . . . 32
A. Multiple Intromissions and Multiple Ejaculations. . . . . . . . . . . . . . . . . . 32
B. Male Postejaculatory Quiescence. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33
C. Sensory Regulation of Copulation ............. 34
38
39
. . . . . . . . . ............................ 39
..................... 40
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . , . , 42

1
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 re-
ciprocally linked in the control of reproduction. Species-typical mating behavior
is the product of underlying neuroendocrine mechanisms. In turn, the neuroen-
docrine events necessary for ovulation, ejaculation, sperm transport, and implan-
tation 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 neuroen-
docrine 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 reproduc-
tive 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 to-
gether 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 deter-
mining 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

Postejaculatory
Interval
PEI 1

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
 GROUP MATING IN THE DOMESTIC RAT 5

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).

9,
111 c
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 part-
ners 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). Howev-
er, 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

PATTERNOF COPULATION
B. TEMPORAL AND ITS
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 intro-
missions so that there are optimal intervals for triggering both of these neuroen-
docrine 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 opti-
mal 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 com-
promise 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 (McClin-
tock 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

A. 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,