Group Title: role of repeated copulations in reducing the effects of competitive inseminations among male laboratory rats
Title: The role of repeated copulations in reducing the effects of competitive inseminations among male laboratory rats
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Title: The role of repeated copulations in reducing the effects of competitive inseminations among male laboratory rats
Physical Description: vii, 57 leaves : ; 28 cm.
Language: English
Creator: Lanier, David Louis, 1950-
Copyright Date: 1978
 Subjects
Subject: Rats -- Reproduction   ( lcsh )
Rats -- Behavior   ( lcsh )
Sexual behavior in animals   ( lcsh )
Psychology thesis Ph. D   ( lcsh )
Dissertations, Academic -- Psychology -- UF   ( lcsh )
Genre: bibliography   ( marcgt )
non-fiction   ( marcgt )
 Notes
Statement of Responsibility: by David Louis Lanier.
Thesis: Thesis--University of Florida.
Bibliography: Bibliography: leaves 52-56.
General Note: Typescript.
General Note: Vita.
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Bibliographic ID: UF00098913
Volume ID: VID00001
Source Institution: University of Florida
Holding Location: University of Florida
Rights Management: All rights reserved by the source institution and holding location.
Resource Identifier: alephbibnum - 000066137
oclc - 04394340
notis - AAH1352

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THE ROLE OF REPEATED COPULATIONS IN REDUCING
THE EFFECTS OF COMPETITIVE INSEMINATIONS
AMONG MALE LABORATORY RATS










By

DAVID LOUIS LANIER


A DISSERTATION PRESENTED TO THE GRADUATE COUNCIL OF THE
UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE
REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY


UNIVERSITY OF FLORIDA
1978















ACKNOWLEDGEMENTS


I would like to express my gratitude to Dr. Donald

A. Dewsbury for his continued encouragement, guidance and

support during this research and other academic endeavors

at the University of Florida. For their supervision of

various, diverse aspects of my graduate training and for

their aid in my search for an academic position, I wish to

thank Dr. Marc N. Branch, Dr. William G. Luttge, Dr. John H.

Kaufmann, Dr. Merle E. Meyer, and Dr. Carol J. Van

Hartesveldt.

This research was supported by Grant BMS 75-08658 of

the National Science Foundation.

I would also like to express my appreciation to the

fellow graduate students, especially Harry N. Davis and

Daniel Q. Estep, whose discussions and suggestions have

aided me in my research. Finally, I wish to thank my parents,

Robert E. Lanier and Geraldine Lanier, without whom this

dissertation would not have been possible.
















TABLE OF CONTENTS


ACKNOWLEDGEMENTS. . . . . .

LIST OF TABLES. . . . . .

ABSTRACT. . . . . . . .

INTRODUCTION. . . . . . .

Behavioral Stimuli Influencing


Page


ii

v

vi

1


Successful


Reproduction in Muroid Rodents.
Sexual Selection and Competitive


Inseminations . . . . . .
Evidence of Competitive Inseminations
in Rodents . . . . . ..
The Adaptive Significance of Male Rat
Copulatory Behavior . . . . .
The Hypothesis to be Tested. . . .

EXPERIMENT I. . . . . . . . .

Methods. . . . . . . . .

Subjects. . . . . . .
Procedure . . . . . .

Results and Discussion .... .. ...

EXPERIMENT II . . . . . . . .

Methods. . . . . . . . .

Subjects. . . . . . .
Procedure . . . . . .

Results and Discussion . . . .


. . . . 2











TABLE OF CONTENTS (Continued)


Page

EXPERIMENT III. . . . . . . . . .. 31

Methods. . . . . . . . . . .. 31

Subjects. . . . . . . . .. 31
Procedure . . . . . . . . 32

Results and Discussion . . . . . . 34

GENERAL DISCUSSION. . . . . . . . ... 38

APPENDICES
APPENDIX I . . . . . . . . . 45
APPENDIX II. . . . . . . . . .. 48
APPENDIX III . . . . . . . . . 50

REFERENCE NOTES . . . . . . . . . 52

REFERENCES. . . . . . . . . . .. 52

BIOGRAPHICAL SKETCH . . . . . . . . 57















LIST OF TABLES


Table Page

1 Test Combinations for Experiment I of
Two Males Each Mating for One Ejaculatory
Series with the Same Female . . . . 15

2 The Total Number of Pups of Each Coat
Color and the Per Cent Albino Pups Which
Resulted from Two Successive Matings of
Two Males from Different Strains. .. .. . 20

3 Experiment I, the Frequency of Each of
Three Types of Litters after Successive
Matings of Males of Two Different
Strains . . . . . . . . . 22

4 Strain and Number of Ejaculatory Series
Allowed for Each Male in Experiment II. . 25

5 Litter Composition, Number of Litters,
and Mean Percentage of Pups Sired by
the First Male in Experiment II . . . 28

6 Summary of the Results of Experiment III
in Which an Albino Male Mated for One
Ejaculatory Series, an Intermediate
Treatment Was Given and Then a Hooded
Male Was Allowed to Copulate for Five
Ejaculatory Series. . . . . . .. 35










Abstract of Dissertation Presented to the Graduate Council
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Doctor of Philosophy

THE ROLE OF REPEATED COPULATIONS IN REDUCING
THE EFFECTS OF COMPETITIVE INSEMINATIONS
AMONG MALE LABORATORY RATS

By

David Louis Lanier

June 1978

Chairman: Donald A. Dewsbury
Major Department: Psychology

While male laboratory rats (Rattus norvegicus) typi-

cally display several ejaculatory series when mating with

a female rat, the possible adaptive significance or benefits

of such a behavioral pattern have heretofore been unclear.

The present research investigated the possibility that such

multiple ejaculatory series serve to prevent sperm displace-

ment or sperm dilution by other males. Interpretations of

previous research on sperm displacement in rodents were

rendered tenuous by inadequate observation of behavioral

phenomena or by fertility differences between strains. In

Experiment I, six combinations of four strains were examined

in tests of successive matings of two different strains.

Two strains of nearly equal fertility were chosen for

subsequent experimentation. Moreover, frequent sperm dis-

placement was observed for these males when only one










ejaculatory series was allowed for each male. In Experiment

II, the first male sired most of the offspring (79 per cent

for one strain and 60 per cent for the other), when the

first male was allowed to mate for five ejaculatory series

prior to the copulation of a male of the other strain for

five ejaculatory series with the same female. However, the

first male sired few offspring (12 per cent for one strain

and 17 per cent for the other) when the first male was only

allowed one ejaculatory series. Experiment III examined

whether successive inseminations, vaginal stimulation, or

time alone was responsible for this effect. Neither time

alone nor vaginal stimulation without additional sperm

transfer offered any protection from sperm displacement.

The proposed mechanism for the present effect is sperm

dilution. These data suggest that the behavioral pattern

of multiple ejaculatory series has evolved through the

process of natural selection since males mating for several

ejaculatory series can have a selective advantage over males

mating for one series in species such as rats which have

polygamous mating systems.















INTRODUCTION


Despite the well known stereotypy of the complex,

species-characteristic copulatory patterns of male animals,

very few studies have investigated the adaptive significance

of these patterns. For example, each male mammal of a species

displays only one of a possible sixteen different patterns

based on a classification system devised by Dewsbury (1972).

In this classification system, each species can be readily

categorized on the basis of the following four criteria:

(1) Is there a lock (i.e., mechanical tie between the penis

and vagina)? (2) Does intravaginal thrusting occur? (3)

Are multiple intromissions prerequisite for ejaculation?

and (4) Do multiple ejaculations occur? While a large number

of mammalian species have been classified using this system

(Dewsbury, 1972, 1975), the adaptive functions of the

specific pattern of copulation displayed by a particular

species have rarely been examined. The present thesis will

consider the possible adaptive significance of the diverse

and often complicated patterns of copulation present among

muroid rodents and test a hypothesis regarding one










additional adaptive function of copulatory behavior in male

rats.

Males of most muroid rodent species display copulatory

behavior after the first ejaculation (Dewsbury, 1975). There

are few data indicating that such behavior is necessary for

successful reproduction for females of the same species.

The theoretical proposals and experimental data which could

account for such disparity seem to be inadequate.

The new hypothesis to be tested is that males which

have several ejaculations with a particular female decrease

the probability that another male will sire offspring by

the same female.


Behavioral Stimuli Influencing Successful
Reproduction in Muroid Rodents


Specific quantitative aspects of the male mating pattern

in some muroid rodents have been shown to be important in

(1) initiating pregnancy responses; (2) increasing the

number of ova released by mature follicies; and (3) reducing

the receptivity of females.

In many rodent species initiation of successful pregnancy

may require more than the passing of sperm from male to

female. For example, the critical copulatory stimuli

which initiate the physiological states necessary for










pregnancy vary among these species. While an ejaculatory

reflex by a male is sufficient for the initiation of

pregnancy in female housemice (Land and McGill, 1967),

female laboratory rats require the multiple intromissions

(discrete vaginal insertions) which are normally shown by

male rats prior to an ejaculation (Adler, 1969; Chester and

Zucker, 1970; Wilson, Adler and LeBoeuf, 1965). Copulatory

stimulation which occurs after the first ejaculation increases

the probability of pregnancy in hamsters (Lanier, Estep

and Dewsbury, 1975), cactus mice (Dewsbury and Estep, 1975),

montane voles (Davis, Gray, Zerylnick and Dewsbury, 1974),

and northern grasshopper mice (Lanier and Dewsbury, 1977).

In female rats, which ovulate spontaneously, at least

two factors influence the number of ova released. Rogers

(1971) has noted that the number of ova shed can be increased

if females are mated at particular times in the day-night

cycle. Second, Davis (1974) has demonstrated that more ova

are released after several ejaculatory series than after

only a single ejaculatory series is allowed when a male

mates with an aged,multiparous female.

Copulation and associated stimuli have been shown to be

effective in reducing the receptivity of females of many

rodent species. Hamsters show a decline in receptivity after










vaginal stimulation (Carter, 1972, 1973). A single male

hamster often appears to reduce the receptivity of the

female to a level such that a second male attains very few,

if any, complete ejaculatory series (Estep, Lanier and

Dewsbury, Note 1; Oglesby, Lanier and Dewsbury, Note 2).

Similarly, female laboratory rats show a reduction in

receptivity that is inversely related to the number of

previous intromissions (Hardy and DeBold, 1972).


Sexual Selection and Competitive
Inseminations


The term "sexual selection" was first used by Darwin

(1871) to refer to those advantages which individuals have

over other members of the same species with regard to repro-

duction. While "sexual selection" is now regarded as a type

of natural selection rather than a separate process (Mayr,

1972), Darwin may be properly credited with originating

this term and with making the observation that males compete

for females in many species. Trivers (1972) has suggested

that this type of competition is a logical outcome for species

in which the burdens of reproduction and parental care rest

primarily on the female; ". . where one sex invests con-

siderably more than the other, members of the latter will










compete among themselves to mate with members of the former"

(p. 173). All of the adaptive functions of rodent copulatory

behavior discussed above probably fall into the general

category of sexual selection since these adaptations increase

the probability or efficiency of pregnancy responses evoked

by particular males. However, competition among males is

particularly clear in those situations where two males have

copulated with one female and each have left sperm in her

reproductive tract.

In an article reviewing the literature on similar

competition among insects, Parker (1970) defined "sperm

competition" as ". . the competition within a single female

between the sperm from two or more males for the fertiliza-

tion of ova" (p. 527). Two opposing evolutionary forces

were noted. First, selection would favor those males which

could displace the sperm of a male which had mated previously

with a female. On the other hand, selection would also

favor mechanisms whereby the first male could prevent dis-

placement of his sperm.

The present experiments on competitive inseminations

in rodents will explore an adaptive function of repeated

ejaculations which is probably common to a number of taxa.

While Parker's (1970) examples of sperm mixtures and sperm










displacement in insects illustrate that similar processes

are present in these animals, the term "sperm competition"

has not been presently adopted since this term rhetorically

implies that the individual sperm vie equally in a race

to the ova. What is competitive about most of these

inseminations and behaviors by these males is that one male

may displace or "dilute" the semen of another male.

Males of avian species probably are subject to some

of the same kinds of internal reproductive competition. In

one such study of sperm mixtures among birds, Martin, Reimer,

Lodge and Dzuik (1974) found that the ratio of sperm of each

of two strains of domestic cocks was directly related to

the probability that each would sire the resulting broods.

In short, the pursuit of the general problem of competitive

inseminations may shed new light on the evolutionary

significance of repeated matings.


Evidence of Competitive Inseminations
in Rodents


The present hypothesis is that the repeated ejaculatory

series of male rodents may have the adaptive function of

reducing a second male's ability to compete successfully in

siring offspring. There are indications that more than










one male frequently mates with the same female in the

natural habitat. Competitive inseminations are of obvious

biological significance for at least some rodents since

more than one male frequently mates with a single female

as is documented by the protein analysis of blood samples

of litters born to pregnant, field-caught deermice,

Peromyscus maniculatus (Birdsall and Nash, 1973), and

observations of multiple matings in wild and semi-natural

populations of rats, Rattus norvegicus (Barnett, 1958; Cal-

houn, 1962).

Multiple inseminations frequently occur in laboratory

situations in which two males are housed with a single female

housemouse (Levine, 1958; Levine and Lasher, 1964; Levine and

Krupa, 1966) or rat (King, 1929). These experiments have

used coat color as a convenient genetic marker of which male

has sired the resulting offspring. For example, when a

homozygous albino female is mated with both a homozygous

albino male and a homozygous pigmented male, the coat color

of the offspring will always reflect the strain of the father

since albinism is recessive. Unfortunately, actual copulation

in these experiments was not usually observed.

In two laboratory experiments, one ejaculation by male

rodents of two different strains with the same female was










observed. In housemice, Levine (1967) noted that albino

males mating with albino females sired more of the resulting

offspring than pigmented males, particularly when the albino

male mated first (95 per cent versus 70 per cent). However,

the amount of time between ejaculations by successive males

did not appear to be a critical factor (range = 16-181

minutes). By contrast, Adler and Zoloth (1970) found that a

pigmented male rat which mated with an albino female within

15 minutes after the single ejaculation of an albino male

fathered 66 per cent of the offspring. However, if mating of

the pigmented male was delayed for 30 minutes or longer, less

than 20 per cent of the offspring were pigmented. When

algino males mated second, they sired most of the offspring

regardless of the amount of time between males.

Two additional experiments suggest that prolonged

copulation by male rodents decreases the probability that

another male can compete successfully for paternity of the

offspring. When F344 albino males mated first for only

one ejaculatory series with an albino female, an ACI pig-

mented male that mated second usually sired the offspring.

If five ejaculatory series were allowed for the albino

male, pigmented males were rarely the fathers of the off-

spring. However, regardless of the number of ejaculatory










series allowed for pigmented males mating first, they were

nearly always displaced by albino males (Estep, Lanier and

Dewsbury, Note 1). Somewhat similar data have been

collected in hamsters (Oglesby, Lanier and Dewsbury, Note 2).

Once again there was a fertility difference between strains.

Whereas cream-colored male hamsters of low fertility could

effectively displace the sperm of agouti males allowed only

one ejaculation, displacement rarely occurred if the agouti

males were allowed to mate to satiety before the second male

was introduced.

As with previous studies the interpretations of the

latter two experiments are tenuous due to fertility

differences among strains. These data demonstrate that a

male of low fertility mating second with a female has a

competitive advantage over a male of high fertility which

has mated for one ejaculatory series but does not have an

advantage over a male of high fertility which has mated for

several ejaculatory series. However, since the reciprocal

relationship did not hold, these studies do not necessarily

indicate a normal mechanism by which competitive insemina-

tions occur. For example, the last male rat to mate could

conceivably sire most of the offspring when males of nearly

equal fertility mate sequentially. Nevertheless, since a










male of low fertility can displace the sperm of a more

fertile male under some circumstances, one can safely

assume that another male of high fertility would be effec-

tive at sperm displacement under similar circumstances.


The Adaptive Significance of Male
Rat Copulatory Behavior


Despite the numerous studies of copulatory behavior of

laboratory rats (Rattus norvegicus), the adaptive signifi-

cance of this copulatory pattern is unclear. When a male

laboratory rat is placed with a receptive female, the male

typically displays several mounts with shallow pelvic

thrusting towards the female's vaginal orifice. On some

of these mounts, the male briefly inserts his penis into

her vagina. Approximately ten of these mounts with intromis-

sion occur prior to an insertion on which he ejaculates.

This event concludes the first ejaculatory "series." Sperm

and a seminal coagulate collectively called a "plug," are

deposited in the female's vagina -(Beach and Jordan, 1956).

A male rat typically displays seven ejaculatory series

prior to obtaining a satiety criterion of 30 minutes without

mounting.

The multiple intromissions of male rats have been

shown to aid in successful reproduction in several ways.









Adler (1973) reviewed the available literature and concluded

that multiple intromissions were required to: (1) to

facilitate sperm transport in the female's reproductive

tract (Adler, 1969; Chester and Zucker, 1960); (2) to

initiate a neuroendocrinee reflex" that results in the

necessary hormonal states for a luteal phase of overian

activity; and (3) to initiate a mammary gland development

3-5 days after mating (Dilley and Adler, 1968).

The adaptive or beneficial functions of multiple

ejaculations for female rats are particularly unclear.

Whereas Zucker and Wade (1968) suggested that multiple

ejaculations may have evolved as a "safety factor," this

view seems to be untenable (see Dewsbury, 1971).

Davis (1974) demonstrated that multiple ejaculatory

series greatly increase the probability of pregnancy for

aged (approximately 11-16 mon old) multiparous female rats.

In addition, the number of ova released in these rats was

directly related to the number of ejaculatory series they

received. While these data suggest that multiple ejacula-

tory series may have an important effect on reproduction for

a rather limited period in a female's reproductive life,

one may question how frequently a female rat actually

perseveres to such an age in more natural habitats.










Nevertheless, these data suggest that under some kinds of

"biological stress" multiple ejaculatory series may be

important for success in reproduction. In more recent work,

Davis and Conner (1977) found that multiple ejaculatory

series were more effective than a single series for females

mating in post partum estrus. The "stresses" of recently

bearing a litter and lactating during pregnancy may be respon-

sible for this apparent reduction of sensitivity of repro-

ductive responsiveness. Similarly, Ball (1934) found that

female rats subjected to surgical "stress" to their repro-

ductive tracts were more likely to bear litters if more than

one copulatory plug was present in their vaginae.


The Hypothesis To Be Tested


The present experiments were designed to test the

hypothesis that multiple ejaculatory series can aid in the

successful reproduction of a male mating with a healthy,

young female rat. In particular, an individual male's

probability of siring offspring may be increased by

multiple ejaculatory series in those instances where

another male mates with the same female.

Natural selection of a pattern of multiple ejaculations

would be expected if males showing this pattern had some






13


selective advantage over males displaying only a single

ejaculatory series. Although a female might have maximally

successful reproduction after mating with a male for only a

single series, the results on an individual male's chances

of reproduction could be disastrously affected if another

male subsequently mated with the same female and displaced

or diluted the first male's sperm. In this regard, the

present study differs from most previous work: the relative

reproductive success of males rather than females will be

examined.















EXPERIMENT I


The primary purpose of this experiment was to find

strains of nearly equal fertility for subsequent experimenta-

tion. This selection of strains seemed particularly impor-

tant since fertility differences among populations or

strains have rendered interpretations of most previous

experiments on sperm displacement in rodents somewhat

tenuous.

Replication of the finding that one male rat can dis-

place the sperm of another male rat under laboratory condi-

tions would be expected. This effect, previously observed

by Lanier, Estep, and Dewsbury (Note 3) differs from that

of Adler and Zoloth (1970) in that the displacement of the

first male's sperm occurs even when an interval of 10-15

minutes or more has occurred between matings.

Six combinations of two males of different strains

mating with the same albino female were used (see Table 1).

Males of each of three pigmented strains were allowed to

mate for one ejaculatory series before an albino male was

allowed to mate with the same female for one ejaculatory












Table 1. Test Combinations for Experiment I of Two Males
Each Mating for One Ejaculatory Series with the
Same Female.




First Male Second Male Female

Long-Evans1 F344 F344 Albino

F3442 Long-Evans F344 Albino

Mai3 F344 F344 Albino

F344 MAX F344 Albino

BR4 F344 F344 Albino

F344 BR F344 Albino


1. Long-Evans: hooded, outbred.

2. F344: Fischer albinos, inbred.

3. Mai: Microbiological Associates' hooded, outbred.

4. BR: nonagouti brown, inbred.









series on 30 tests. On an additional 30 tests the strain

of male mating first was reversed.



Methods


Subjects


The four strains of males and their origins are listed

in Table 1. When males in each of these strains were mated

with a homozygous albino female, the resulting offspring

would bear the coat color of the sire since albinism is

recessive. The suppliers of these strains indicated that

it was unlikely that any of the pigmented males carried a

recessive gene for albinism. As described below, the coat

color of the offspring always resembled the coat color of

the sire on these protests.

Males were 4-6 months old and females were approxi-

mately 3 months old at the beginning of the experiment.

All subjects were housed individually in Wahmann stainless

steel cages in an air-conditioned,- windowless room with a

14:10 light-dark cycle with light onset at 1200 hr. Purina

lab chow and water were continuously available.










Procedure


Females were given daily tests for receptivity (Adler,

1968). By applying firm flank stimulation to females and

assessing the degree of lordotic responsiveness receptivity

of females to males could usually be predicted. Tests were

discontinued if the test female was unreceptive.

In protests, batteries of virile males and fertile

females were established. In each of four strains, males

were selected on the basis of three criteria:

1. Each of these males was required to initiate

copulation within 10 minutes after the introduction of a

receptive female on one of four tests. While this procedure

may have eliminated a few sluggish but "normal" copulators,

the males that were selected had reasonably short intro-

mission latencies. Predictable intromission latencies were

important for this and subsequent experiments since the

second male of a test was required to mate with the test

female within a short period of t-ime after the first male

was removed from the female.


2. After the initiation of copulation, each male

was required to mate format least three complete ejaculatory

series. Most males displayed five or six ejaculatory










series. Requiring males to mate for at least three

ejaculatory series helps to eliminate ambiguity in

interpretation caused by including males which mated to

satiety but displayed only one or two ejaculatory series.


3. Males were also excluded if after two tests with

copulation with a receptive female, pregnancy did not

result for at least one female. The resultant litters

verified that albinism was recessive to all of the pig-

mented coat colors and that none of the pigmented sires

carried the recessive gene for albinism.

Tests were conducted in circular plexi-glass arenas

of 18 x 2.54 cm diameter with a floor cover of San-i-cel, a

commercial corncob bedding. Tests were initiated 4-6 hours

after light offset by the introduction into an arena,

approximately 10 minutes after the introduction of the

test female to the arena.

The behavioral events (mounts, intromissions and ejacu-

lations, see Beach and Jordan, 1956) were recorded by the

experimenter on an Esterline-Angus event recorder. Males

were allowed to copulate freely with the female until the

occurrence of the first ejaculation. If the male failed to

copulate with the remale within 5 minutes after the female










was introduced, or if the female failed to show a lordotic

posture in response to vigorous mounting by the male, the

test was disregarded.

After a male achieved one ejaculation with a female,

that male was removed. Ten minutes later, a male of a dif-

ferent strain was introduced and allowed to copulate until

the occurrence of the first ejaculation. If copulation failed

to occur within five minutes after the introduction of the

second male, the test was terminated and disregarded.

In short, every female received one ejaculatory series

from a male of one strain and 10-15 minutes later one

ejaculatory series with a male of another strain was

initiated.


Results and Discussion


As can be seen in Table 2, fertility varies among

these strains. Nearly all albino pups resulted regardless

of strain order after tests of successive matings of Mai-

hooded males and F344 albino males. However, more pigmented

than albino pups were born when Long-Evans males mated

after these albino males. In successive matings of non-

agouti brown males and F344 albino males, the proportion of

albino pups was intermediate between those obtained using

the other two pigmented strains.














Table 2. The Total Number of Pups of Each Coat Color and
the Per Cent Albino Pups Which Resulted from Two
Successive Matings of Two Males from Different
Strains.


Strain of Male
Long-Evans Brown and F344 Mai and F344
and F344
Order Order Order
Long-Evans F344 Brown F344 Mai F344
First First First First First First

Number of
Albino Pups 55 35 53 56 72 34

Number of Pig-
mented Pups 29 37 16 23 0 5

Total 84 72 69 79 72 39

Number of Liters 9 9 9 9 8 6

Per Cent Albino 65.5 48.6 76.8 70.8 100.0 87.2










Application of chi-square tests for each combination

of strains revealed no significant difference in fertility

between the Long-Evans and F344 strains (2 = 3.19, df = 1,

p > .05). However, there were significant differences

between the Brown and F344 strains (X2 = 33.53, df = 1,

p < .001) and between the Mai and F344 strains (X2 = 91.67,

df = 1, p < .001).

A descriptive analysis of the litter composition of

these tests shows a similar trend (See Table 3). Successive

matings of Mai-hooded males and albino males resulted in

thirteen all albino litters and one mixed litter. After

successive matings of Long-Evans and F344 males, about an

equal number of albino, mixed and all pigmented litters

resulted.

Individual data for this experiment are presented

in Appendix I (Table A-l).

On the basis of this experiment, the Long-Evans strain

was chosen for subsequent experiments since males of this

strain appeared to be closer in fertility to the F344 albino

males than any other pigmented strain.

The results also indicate that sperm displacement

frequently occurs when a second male is allowed only one













Table 3. Experiment I,the Frequency of Each of Three Types
of Litters after Successive Matings of Males of
Two Different Strains.


Strains
Long-Evans Mai-Hooded
and F344 Brown and F344 and F344
Order Order Order
Type of Long-Evans F344 Brown F344 Mai F344
Litter First First First First First First

All Albino 3 3 6 3 8 5

Mixed 4 4 1 5 0 1

Pigmented 2 2 2 1 0 0

Total 9 9 9 9 8 6







23


ejaculatory series, 10-15 minutes after the end of a

single ejaculatory series by the first male.















EXPERIMENT II


This experiment critically tested the hypothesis that

some behavioral or physiological aspect of the several

ejaculatory series typically displayed by a male rat is

more effective than a single ejaculatory series in prevent-

ing sperm displacement. The design of this experiment is

represented in Table 4. The first male was allowed to

complete one or five ejaculatory series. The second male

was always allowed to complete five ejaculatory series.

On half of the tests in each condition, an albino male

mated first, while on the other half of the tests, a pig-

mented male mated first.


Methods


Subjects


The 11 Long-Evans males, 12 F344 males and 54 F344

females used in this experiment had served in Experiment I.

Housing conditions and light cycle were as in that experi-

ment. Each of the females was used once and only once in

this experiment. An additional 16 females either failed

24















Table 4. Strain and Number of Ejaculatory Series Allowed
for Each Male in Experiment II.


First Male Second Male
Test Number of Number of
Condition Strain Series Strain Series

1 Pigmented 1 Albino 5

2 Albino 1 Pigmented 5

3 Pigmented 5 Albino 5

4 Albino 5 Pigmented 5










to respond to flank stimulation or vigorous mounting by a

male.

The combination of males, one of each of two strains

was essentially random. No male was used more than twice

in any test condition. Males were allowed two weeks for

recovery between tests.


Procedure


Tests were conducted in the same arenas as in Experi-

ment I. In each test the first male was allowed to mate

until either the completion of the first or the fifth

ejaculatory series, depending on the test condition.

Immediately after the completion of the appropriate ejacula-

tory series, the test male was removed and replaced by a

male of the other strain. Females were left in the test

chamber undisturbed until the end of the test. If the

second male failed to achieve intromission within 5 minutes

after being placed with the test female, that male was

removed and replaced by another male of the same strain.

Tests were terminated whenever a lag of more than 10 minutes

occurred between the last ejaculation of the first male and

the first intromission of a male of the other strain.










The last male on these tests was allowed to mate until

five ejaculatory series were completed or until a satiety

criterion of 30 minutes without an intromission was reached.

However, only those tests in which satiety was reached after

three or more complete ejaculatory series were included in

some of the statistical analyses below.


Results and Discussion


Litter composition, number of litters and mean per-

centage of pups sired by the first male are shown in Table 5.

A Kruskal-Wallis nonparametric analysis of variance (Siegel,

1956) on the mean percentage of pups in each litter sired

by the first male demonstrated there were significant

differences between at least two of the groups (Hc = 23.68,

df = 3, p < .001). Mann-Whitney U-tests (Siegel, 1956)

further revealed that Long-Evans males sired significantly

more pups (U = 11.0, n1 = 12, n2 = 11, p < .001) if five

ejaculatory series rather than one. ejaculatory series were

allowed prior to the introduction of the F344 male.

Similarly, P344 males sired significantly more pups

(U = 11.5, nI = 10, n2 = 10, p <.01) if five ejaculatory

series rather than one ejaculatory series were allowed prior

to the introduction of the Long-Evans male. Thus, regardless














Table 5. Litter Composition, Number of Litters, and Mean
Percentage of Pups Sired by the First Male in
Experiment II.


F344 Long Evans
First First
Measure IE 5E 1E 5E

Mean Percentage of Pups
Sired by 1st Male 12 79 17 60
(74) (56)

Number Sired by 1st Male 7/53 74/98 12/83 39/66
(56/82) (35/66)

Number of Litters 11 12 10 10
(10) (9)


Numbers in parenthesis refer to results when the data from
three tests on which neither of two males of the other
strain mated after the first male.










of the strain of male mating first, the first male had a

high probability (79 or 60%) of siring offspring if 5

ejaculatory series were allowed but a low probability of

siring offspring (12 or 17%) if only one ejaculatory series

was allowed.

Individual data for this experiment are presented in

Appendix II (Table A-2).

While these data give clear evidence that multiple

ejaculatory series can greatly reduce the probability of

sperm displacement or dilution, the mechanism is not clear.

In order to more critically test the hypothesis that the

behavior or physiological changes occurring in the second

through fifth series of the second male were approximately

balanced across groups, three tests, in which the first male

mated for 5 ejaculatory series but in which both a second

and third male of the other strain failed to mate with the

test female, were excluded and the data were reanalyzed.

The apparent reduction in female receptivity which appears

to accompany prolonged copulation may be an interesting

phenomenon. However, these three cases muddle the question

"do multiple ejaculatory series reduce the probability of

sperm competition with another male when a second male has

also mated and deposited viable sperm in the female's repro-

ductive tract."










The results were essentially the same when the three

tests are excluded where only one male mated with the female.

Application of a Krukal-Wallis analysis of variance revealed

that there were significant differences between at least

two of the groups (Hc = 20.71, df = 3, p < .001). Mann-

Whitney U-tests demonstrated that one ejaculatory series was

not as effective as five ejaculatory series in maximizing

the probability that Long-Evans males mating first would

sire the offspring (U = 11, n, = 10, n2 = 11, p < .01) or

that F344 males mating first would sire the offspring

(U = 13.5, ni = 9, n2 = 10, p < .01).

The analysis with the three tests excluded demonstrates

that multiple ejaculatory series reduce the probability

that the second male's sperm will successfully fertilize

the female even when these sperm have been deposited in

the female's reproductive tract. While the first male's

copulatory stimulation may occasionally be sufficient to

terminate receptivity, consideration of these few instances

is not necessary to account for the phenomenon that multiple

ejaculatory series reduce the probability of sperm com-

petition.















EXPERIMENT III


While Experiment II clearly demonstrated that "something"

which occurs during the time interval from the end of the

first to the end of the fifth ejaculatory series of a male

rat's mating sequence reduces the probability that subsequent

males will sire offspring with the same female, the critical

elements of the first male's mating behavior that mediate

this effect are unclear.

In order to test whether successive inseminations,

vaginal stimulation, time alone or other factors were pri-

marily responsible for the effect found in Experiment II,

Experiment III was initiated.


Methods


Subjects


All of the 14 F344 males, 7 vasectomized F344 males

and 10 normal Long-Evans males had served in Experiments I

and II and were vigorous copulators. The 29 F344 females

were virgins approximately 4 months of age. Housing and










general testing conditions were as in Experiments I and

II.

Two ventral incisions were made on each male to be

vasectomized while under Penthrane anesthetic. The vas

deferens was exposed, tied off with surgical thread in two

places near the epididymis and a cut between the ties was

made with surgical scissors.


Procedure


Each test of this experiment followed the same general

format. A single albino female was allowed to mate with

an albino male until the completion of one ejaculatory

series. Next an intermediate treatment was given to each

female. Finally a hooded Long-Evans male was allowed to

mate for five ejaculatory series with this same female.

The three intermediate treatment conditions were as

follows:

1. A normal albino male was allowed to mate with the

test female for four complete ejaculatory series. This male

was introduced one minute after the completion of the first

ejaculation of the first male, at which time the first male

was removed. If the second male failed to initiate copulation

within 10 minutes, the test was terminated.










2. This treatment condition was exactly as above

except that the albino male used for the intermediate con-

dition was vasectomized. Thus, these males were capable of

relatively normal copulatory behavior, but deposited copula-

tory plugs which did not contain sperm. Each of these

vasectomized males had been pretested at least two weeks

prior to the test in order to ascertain that these males

had relatively normal copulatory behavior, and deposited

copulatory plugs but did not deposit sperm.


3. In this intermediate treatment condition, a

restrained albino male was introduced one minute after the

first male's ejaculation. These males were restrained in

wire cages and remained in the test arena for a period of

45 minutes prior to the introduction of the Long-Evans male.

This group was to control for the possibility that time

alone, auditory stimulation or olfactory cues from males of

the albino strain might influence the Long-Evans male's

probability of siring offspring.










Results and Discussion


Table 6 shows the number of litters, the mean per-

centage of pups sired by the first male and the total number

of pups of each type of coat color for each test condition.

An overall chi-square test on the total number of pups of

each coat color for each condition revealed that at least

two groups were statistically different (X32 = 21.28, df = 2,

p < .001). Subsequent pairwise chi-square comparisons

revealed that the restrained male and vasectomized male

groups did not differ (X2 = 0.926, df = 1, p > .05) but that

both the restrained male and vasectomized male groups

differed statistically from the normal male group

(X2 = 12.65, df = 1, p < .001; 72 = 15.82, df = 1, p < .001,

respectively). While the trend of these data appears to

show that the mean percentage of pups sired by the albino

males was highest after a normal male was in the inter-

mediate condition, intermediate when a vasectomized male

was used and least when a restrained male was used, Kruskal-

Wallis nonparametric analysis of variance revealed no signi-

ficant differences between these groups (Hc = 1.95, df = 2,

p > .05).

Individual data for this experiment are presented in

Appendix III (Table A-3).
















Table 6. Summary of the Results of Experiment III in Which
an Albino Male Mated for One Ejaculatory Series,
an Intermediate Treatment Was Given and Then a
Hooded Male Was Allowed to Copulate for Five
Ejaculatory Series.


Intermediate Treatment


Restrained


Vasectomized Normal


Measure Male Male Male

Mean Percentage of
Pups Sired by the
First Male 19.7 31.4 44.1

Pups' Coat Color
Pigmented 56 64 44
Albino 13 13 38

Number of Litters 9 10 10










In short, it appears that vaginal stimulation alone is

not sufficient to account for the present effect. Vasecto-

mized males were not as effective as normal males in pre-

venting sperm displacement. However, these data could be

easily misinterpreted since the vasectomized males were doing

more than adding additional copulatory stimulation. An

analysis of the intromission latencies revealed that all

vasectomized males mated within 300 seconds after their

introduction to the female. As discussed below, these males

effectively removed the copulatory plug of the first male

and replaced the plug with one containing no sperm.

Copulatory behavior and plug dislodgement occurring less

than 4-6 minutes after an ejaculation has been shown to

greatly reduce the number of sperm reaching the female's

uterine horns (Matthews and Adler, 1977). Thus, the present

data indicating that copulatory behavior and plugs of

vasectomized males have no effect greater than time alone

may be misleading, since the group of females in the 45

minute restrained male group did not have the plugs removed.

In the intermediate group with normal males, the plug was

removed by the second albino male's copulation but these

intermediate males deposited additional plugs and sperm

during the course of his four ejaculatory series.







37


While there may be conditions under which copulatory

plugs may serve as a physical barrier to later sperm

deposition and behavioral stimuli may inhibit later sperm

transport, the current data suggest the total number of

sterm from successive ejaculations is the primary factor

in preventing later sperm competition among laboratory rats.















GENERAL DISCUSSION


The three present experiments demonstrate and replicate

a clear effect: while a male rat mating for only one

ejaculatory series with a female rat frequently can have

his sperm displaced by those of another male rat, such dis-

placement is unlikely when the first male has completed

five ejaculatory series. These data suggest that the prob-

able adaptive significance of multiple ejaculations in rats

and closely related species is to reduce the probability of

sperm displacement.

This behavioral pattern, multiple ejaculatory series,

has the necessary concomitant physiological adaptations.

Rats have relatively large testes and complex accessory sex

glands (Arata, 1964). The large testes, seminal vesicles

and coagulating glands of male rats are necessary for

delivering successive ejaculates of appropriate size.

These popularly studied structures of rats probably owe

their large size to this same adaptive function of multiple

ejaculatory series.

There may be other adaptive functions or benefits of

multiple ejaculatory series. In aging, multiparous rats

38










and lactating females mating in post partum estrus, multiple

ejaculatory series increase the probability of pregnancy for

such females when compared to similar females receiving only

one ejaculatory series (Davis, 1974; Davis and Conner, 1977).

However, sperm displacement may well also be an important

factor for males mating with lactating and multiparous females.

Wilson (1975) has outlined the possible types of com-

petition among males including sperm displacement and sperm

plugs. These modes range from infanticide to ". . one

extraordinary species, the certo-pognoid fly Johannseniella

nitida, the body of the male itself serves as the plug . ."

(Wilson, p. 321). Since a single copulatory plug of a male

rat does not provide reliable protection from later insemina-

tions, male rats have evolved a behavior pattern of multiple

ejaculations. One can easily envision a reproductive

battlefield of male rats and their progenitors. As males

evolved more effective physiological mechanisms for pre-

venting sperm displacement (such as the deposition of

copulatory plugs), males within the same population evolved

more effective means of plug dislodgement. While other

adaptive functions have been suggested for the multiple

intromission pattern (as-was discussed above), these pre-

ejaculatory intromissions may serve to dislodge the plugs










of previous matings. If so, this may account for the

reduction of intromission frequency in the second through

fifth ejaculatory series of male rats; selection would not

favor male rats which totally dislodged their own plugs

and displaced their sperm from previous matings. The

ineffectiveness of vasectomized males in preventing subse-

quent inseminations as observed in Experiment III of the

present thesis, suggests that successive copulatory plugs

do not serve as complete physical or chemical barriers but

confer selective advantages on males mating first for several

series.

While Adler and Zoloth (1970), and Matthews and Adler

(1977) have shown that the first 4-6 minutes after an

ejaculation is the critical period in preventing disruption

of "sperm transport" to the uterus which occurs when the

copulatory plug is removed from a female rat, the present

data on the ineffectiveness of restrained males in pre-

venting competitive inseminations suggest that the period of

vulnerability of a female to subsequent inseminations is

longer than 45 minutes. Despite Adler and Zoloth's (1970)

data indicating that roughly a quarter of a million sperm

remain in a female rat's uterus when a plug is not dis-

placed until 45 minutes later, the present data indicate










that a second male can still dilute the first male's sperm

and sire most of the offspring.

Adler and Zoloth rarely found sperm displacement when

an interval of 45 minutes had elapsed between matings. The

strains of rats used by Adler and Zoloth differed from those

presently employed. Nevertheless, there is another critical

factor which could account for the present finding of sperm

displacement when an interval of 45 minutes elapses between

matings. In the present study, the second male was allowed

to mate for five ejaculatory series, while only one ejacula-

tory series was allowed in Adler and Zoloth's study. Thus,

the second male had a much greater opportunity of diluting

the first male's sperm in the present study. While this

speculation can only be substantiated by future research,

comparisons across these two studies suggest that the

current effect is probably the result of sperm dilution

in utero rather than some other mechanism.

Since the major difference between the matings of

intermediate normal males and intermediate vasectomized

males in Experiment III was that the former deposited

additional sperm, these data also suggest that sperm

dilution is the mechanism by which the last test male can

sire offspring.










Three other plausible mechanisms which could mediate

the present effect have little support. The accumulated

material from copulatory plugs does not make an effective

barrier since vasectomized males do not prevent later

inseminations.

It is also unlikely that total or partial plug displace-

ment alone can account for this phenomenon. First, sperm

displacement frequently occurred in Experiment III when 45

minutes occurred between mating of successive males. More-

over, males mating for several series in Experiments II and

III dislodged their own plugs from previous ejaculations in

their own successive ejaculations in their own successive

matings.

Finally, there does not appear to be any evidence that

active sperm transport by the reproductive system of the

female was inhibited by behavioral, mechanical or temporal

factors. Females generally bore litters of normal size sired

by the last male despite the previous matings of vasectomized

males or the imposition of a 45 minute time interval between

successive matings.

In short, the present data suggest an extremely important

adaptive function of multiple ejaculatory series for male

rats. This behavioral pattern appears to reduce the






43


probability of sperm dilution by other males which subse-

quently mate with the same female. Since analogous mechanisms

are known to exist in insects and birds, it appears likely

that multiple ejaculatory series may have similar adaptive

functions in a number of mammalian species where more than

one male mates with a given female.



































APPENDICES











APPENDIX I


Table 1-A.


Individual Data from Experiment I; Each of
Two Males Mated for One Ejaculatory Series


with the Same Female.

Strains
MAX F344 Offspring
First Second
Male Male Female Pigmented Albino
Condition Number Number Number

Pigmented 8 64 46 0 5
male first 2 54 16 0 10
3 42 27 0 10
4 37 66 0 10
6 46 40 0 10
1 46 55 0 10
9 52 49 0 5
10 47 21 0 2
7 61 24 0 10


Strains
F344 MAX Offspring
First Second
Male Male Female Pigmented Albino
Condition Number Number Number

Albino male 39 4 32 0 6
first 44 3 15 0 4
45 6 23 0 9
38 8 28 0 4
47 10 4 5 1
48 9 5 0 10










Table 1-A (Extended)


Strains
Long-Evans F344 Offspring
First Second
Male Male Female Pigmented Albino
Condition Number Number Number

Pigmented 13 48 36 0 11
male first 14 52 22 1 9
15 61 11 0 7
16 64 47 0 10
17 56 2 8 0
18 57 6 6 0
20 47 41 3 7
21 65 1 3 8
22 39 59 8 3




Strains
F344 Long-Evans Offspring
First Second
Male Male Female Pigmented Albino
Condition Number Number Number

Albino male 56 13 48 4 7
first 54 15 64 8 3
55 16 45 0 6
46 17 50 3 7
47 18 53 0 4
61 19 13 5 2
64 20 29 0 6
38 21 56 9 0
66 22 3 8 0










Table 1-A (Extended)


Strain
Brown F344
First Second
Male Male
Number Number


Female
Number


Offspring

Pigmented Albino


26 47 114
28 39 67
29 48 57
30 42 42
31 43 20
32 44 18
33 45 33
34 46 119
22 61 34


Strains
F344 Brown Offspring
First Second
Male Male Female Pigmented Albino
Condition Number Number Number


Albino
male first


Condition


Pigmented
male first










APPENDIX II


Table 2-A. Individual Data
Subject Numbers
Each Coat Color


for Experiment II, listing
and Number of Offspring of
for Each Condition.


First Second Offspring
Male Male Female Pigmented Albino
Condition Number Number Number

Pigmented male 17 52 4 1 8
mating first 18 54 30 0 1
for five 19 58 8 1 4
ejaculatory 20 56 6 0 10
series 21 64 66 0 2
24 61 40 2 7
21 61 21 0 6
24 64 46 3 1
13 44 44 0 2
14 48 54 0 3
15 47 58 0 2


Pigmented male 13 14 26 7 1
mating first 15 46 3 0 8
for one ejacu- 13 48 13 7 0
latory series 14 44 18 5 7
16 46 52 7 0
17 54 14 5 0
18 52 22 3 0
20 56 38 9 0
13 46 10 9 1
14 47 11 7 3
15 48 16 10 2
16 44 27 5 2










Table 2-A (Extended)


First Second Offspring
Male Male Female Pigmented Albino
Condition Number Number Number

Albino male 59 21 19 11 0
mating first 61 22 31 10 0
for one 64 24 36 10 0
ejaculatory 52 18 33 3 1
series 56 19 34 7 0
58 20 49 1 5
47 13 15 11 0
46 14 24 4 6
44 15 59 8 0
45 16 65 6 0



Albino male 45 13 42 5 0
mating first 46 14 32 1 6
for five 44 15 56 6 2
ejaculatory 59 21 28 5 4
series 61 24 48 1 2
58 18 27 3 5
56 18 50 2 7
52 19 51 1 5
54 20 62 0 4
58 17 41 3 4










APPENDIX III


Table 3-A.


Contains Individual Subject Numbers and
Number of Pups of Each Coat Color for Each
Condition in Experiment III.


First Second Third
Male Male Male Female Offspring
Condition Number Number Number Number Pigmented Albino

Restrained 64 19 80 9 0
male 59 21 92 7 2
61 24 81 8 4
46 14 87 4 3
66 15 78 1 0
55 14 99 2 1
56 16 94 4 2
65 19 118 6 0
66 15 97 6 1



Vasecto- 59 38 18 97 0 5
mized male 54 44 15 102 13 0
58 36 24 72 13 0
55 49 14 95 0 3
59 38 13 86 12 3
58 44 14 116 10 0
52 41 13 111 7 0
48 38 15 77 6 1
47 49 14 101 0 4
52 36 19 99 3 0










Table 3-A (Extended)


First Second Third
Male Male Male Female Offspring
Condition Number Number Number Number Pigmented Albino

Normal 59 52 18 98 7 3
male 45 61 2 90 8 0
52 46 21 91 5 5
45 66 19 93 1 9
56 59 13 101 3 0
45 46 19 77 1 6
59 66 18 107 9 1
56 46 20 88 4 3
54 61 21 82 6 3
55 52 16 96 0 8
















REFERENCE NOTES


1. Estep, P. Q., Lanier, D. L., and Dewsbury, D. A.
Unpublished observations, 1975.

2. Oglesby, J., Lanier, D. L., and Dewsbury, D. A.
Unpublished observations, 1976.

3. Lanier, D. L., Estep, D. Q., and Dewsbury, D. A.
Unpublished observations, 1976.




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and the Descent of Man 1871-1971. Chicago, Aldine,
136-179.

Wilson, E. 0. (1975). Sociobiology. Cambridge, Mass.,
Belknap Press.

Wilson, J. P., Adler, N. T., and LeBoeuf, B. (1965).
The effects of intromission frequency on successful
pregnancy in the female rat. Proceedings of the
National Academy of Sciences, 53, 1392-1395.















BIOGRAPHICAL SKETCH


David Louis Lanier was born on September 4, 1950, in

Mount Vernon, Illinois. In June, 1968, he graduated from

Springfield High School in Springfield, Illinois. He

received a Bachelor of Science degree with a major in

psychology from Western Illinois University in June, 1972.

From January, 1972 until September, 1975, and from September,

1977 until June, 1978, he held a graduate research assistant-

ship under the supervision of Dr. Donald A. Dewsbury. He

received a Master of Science degree with a psychology major

from the University of Florida in December, 1973.









I certify that I have read this scudy and that in my
opinion it conforms to acceptable standards of scholarly
presentation and is fully adequate, in scope and quality,
as a dissertation for the degree of Doctor ogfPhilosophy.




Donald A. Dewsbury, Chairm n
Professor of Psychology


I certify that I have read this study and that in my
opinion it conforms to acceptable standards of scholarly
presentation and is fully adequate, in scope and quality,
as a dissertation for the degree of Doctor of Philosophy.




Marc N. Branch
Associate Professor of Psychology


I certify that I have read this study and that in my
opinion it conforms to acceptable standards of scholarly
presentation and is fully adequate, in scope and quality,
as a dissertation for the degree of Doctor of Philosophy.

/ . 'L A

Carol J. Van Hartesveldt
Associate Professor of Psychology


I certify that I have read this study and that in my
opinion it conforms to acceptable standards of scholarly
presentation and is fully adequate, in scope and quality,
as a dissertation for the degree of Doctor of Philosophy.




William G. lut eo
Associate Prdofessor of
Neuroscience









I certify that I have read this study and that in my
opinion it conforms to acceptable standards of scholarly
presentation and is fully adequate, in scope and quality,
as a dissertation for the degree of Doctor of Philosophy.




Jhn H. Kaufmann I
ofessor of Zoology


I certify that I have read this study and that in my
opinion it conforms to acceptable standards of scholarly
presentation and is fully adequate, in scope and quality,
as a dissertation for the degree of Doctor of Philosophy.




Merle E. Meyer
Professor and Chairman of Psychology


This dissertation was submitted to the Graduate Faculty
of the Department of Psychology in the College of Arts and
Sciences and to the Graduate Council, and was accepted as
partial fulfillment of the requirements for the degree of
Doctor of Philosophy.

June 1978


Dean, Graduate School




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