An Experimental Study of Group Selection
Author(s): Michael J. Wade
Source: Evolution, Vol. 31, No. 1 (Mar., 1977), pp. 134-153
Published by: Society for the Study of Evolution
Stable URL: http://www.jstor.org/stable/2407552
Accessed: 02/10/2008 20:16
Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at
http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless
you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you
may use content in the JSTOR archive only for your personal, non-commercial use.
Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at
http://www.jstor.org/action/showPublisher?publisherCode=ssevol.
Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed
page of such transmission.
JSTOR is a not-for-profit organization founded in 1995 to build trusted digital archives for scholarship. We work with the
scholarly community to preserve their work and the materials they rely upon, and to build a common research platform that
promotes the discovery and use of these resources. For more information about JSTOR, please contact [email protected].
Society for the Study of Evolution is collaborating with JSTOR to digitize, preserve and extend access to
Evolution.
http://www.jstor.org
AN EXPERIMENTAL
STUDY
OF GROUP SELECTION
MICHAEL J. WADE
Department of Biology, University of Chicago, Chicago, Illinois 60637
Received November 17, 1975. Revised March 25, 1976.
Darwin (1878) suggested in The Origin
of Species (p. 230-233) that selection between families or communities had given
rise to sterile castes in the social insects.
He argued that sterility could not be
favored directly by selection among individuals but that parents or communities
might benefit, in terms of reproductive
success, from the presence of sterile individuals. It is clear from his arguments
that Darwin believed that selection among
groups could result in a change in the
types of individuals within a species.
It was much later that Wright (1931)
perceived intergroup selection as one of
the primary forces controlling evolutionary
change. He stated that the only practicable
method of bringing about a rapid and
non-self-terminating evolutionary advance
would be through the subdivision of populations into isolated and differentiating
groups, among which selection could be
practiced.
Haldane (1932) and Wright (1945)
both considered the case of the evolution
of altruistic behavior where individual
selection acts against the altruist, but the
altruist is favored by group selection.
Group selection became a more controversial subject with the publication of
Wynne-Edwards' book Animal Dispersion
in Relation to Social Behavior (1962).
It was Wynne-Edwards' thesis that
group selection was a general phenomenon
and was responsible for the evolution of
mechanisms which regulated population
size. Wynne-Edwards believed that population size was limited at some level below
the "carrying capacity" (Errington, 1934)
of the environment by means of individuals within the population withholding
reproduction. To the extent that an individual withholds reproduction that indiEVOLUTION
31:134-153.
March 1977
134
vidual suffers a loss of fitness, where
fitness is measured by reproductive success. It was for this reason that WynneEdwards thought individual selection could
not be responsible for the evolution of the
mechanisms for withholding reproduction
and therefore, some form of group selection
was required. Territoriality, ritualized
aggression, the establishment of hierarchies
and other social orderings, the onset of senility, and the optimum reproductiveeffort
were some of the regulatory mechanisms of
populations that Wynne-Edwardsproposed
had evolved by means of group selection.
The regulation of population size has
been and continues to be an interesting
and central problem in the field of population ecology and several authors, among
them Andrewartha and Birch (1954),
Williams (1964), Hamilton (1966), and
Amadon (1964) have cogently discussed
the evolution of the above mentioned
regulatory mechanisms by means of individual selection.
The focus of much of the controversy
has been the question of whether or not
group selection is required to explain the
evolution of a particular character. In
general, the viewpoint of most ecologists
and theorists has been that individual
selection is a faster and more efficient
form of natural selection than is group
selection for the following reasons:
1. In iteroparous species the generation
time of the individual is short relative to
the turnover time of the population and
therefore selection proceeds faster when
the unit of selection is the individual.
2. The numbers of individuals greatly
exceed the numbers of populations. If the
units of selection are numerous it is less
likely that chance events will significantly
influence the outcome of selection. There-
GROUP SELECTION
fore selection is more efficient when the
unit of selection is the individual.
3. Just as individual selection requires
that there be differences between individuals, group selection requires that there be
differences between populations; however,
the origin of variation between populations
and the maintenance of that variation in
the face of even low levels of migration
has heretofore been considered a major
obstacle to the operation of group selection
(Maynard-Smith, 1964).
Reasoning such as the above led Williams
(1966) to formulate a principle of
parsimony which appears to be generally
adopted at the present time. This principle
states that if the evolution of a trait can
adequately be explained by means of individual selection, there is no need to
invoke group selection. The principle of
parsimony clearly restricts the use of group
selection to those cases in which it operates
in a direction opposite to individual selection.
Serious theoretical inquiry into the
process of group selection was stimulated
in part by MacArthurand Wilson's Theory
of Island Biogeography, published in 1967.
One of the concepts espoused by MacArthur and Wilson was that a species
could be viewed as an array of populations
which are formally equivalent to islands.
When populations are viewed in this way,
the processes of extinction, dispersion, and
recolonization assume a role of central importance in the investigation of many
ecological problems.
During the last five years, several
authors, among them Levins (1970), Boorman and Levitt (1973), E. 0. Wilson
(1973), Levin and Kilmer (1974), D. S.
Wilson (1975), Gadgil (1975), and Gilpin
(1975), have directly addressed the genetic
problems of group selection. All of these
authors implicity or explicity consider the
case of individual selection acting in one
direction and group selection acting in the
opposite direction to be the one of major
importance.
The general conclusion has been that
135
group selection will be a significant force
in natural populations only under a very
restrictive set of conditions.
The purpose of this paper is not to
criticize the aforementioned theoretical
works but to present the results of an
experimental investigation of the process
of group selection.
The basic questions which underlie the
research to be presented here are: Can
the differential extinction and/or differential proliferation of populations cause
genetic change? And if so, what are the
parameters which determine the rate and
the extent of the changes?
Groupselection is defined as that process
of genetic change brought about or maintained by the differential extinction and/or
proliferation of populations (Wright, 1945,
1956; Wynne-Edwards, 1962; MaynardSmith, 1964; Williams, 1966; Lewontin,
1970). (In keeping with this definition,
I will not consider selection between
species [Van Valen, 1975] or between
ecosystems [Dunbar, 1960], both of
which have been called "group"selection.)
The gene frequency changes caused by
group selection, as is also true for individual selection, will consist of changes in the
genetic makeup of individuals within populations. Any trait which significantly increases the probability of survival or
proliferation of the population and at the
same time increases the relative probability
of survival or reproductionof the individuals within populations will be selected for
by both group and individual selection. In
such a case the rate of change of gene
frequency is expected to be significantly
greater than the rate of change when
either group selection or individual selection is acting alone. These two different
processes may or may not result in the
same genetic equilibrium and it is their
interaction which will determine the rate
of approach to, and the position of, the
equilibrium.
EXPERIMENT
I
The purpose of this experiment was to
investigate the genetic effects of a process
136
MICHAEL J. WADE
of differential extinction and recolonization
of populations of the flour beetle,
Tribolium castaneum, and the trait chosen
for selection was the number of adult
beetles in a population. The ecology of
Tribolium has been well studied and much
is known about the factors governing
changes in its population size (King and
Dawson, 1972; Mertz, 1972; and Sokoloff, 1974). It was believed that this large
body of information would facilitate the
interpretation of any changes in population size which might occur during the
course of the experiment.
The developmental time is an important
factor in determining both the turnover
time of the population and the rate of
increase of population numbers. T. castaneum is a holometabolousinsect, passing
through egg, larval, and pupal stages before becoming an adult. The total duration
of the developmental period, from egg to
mature adult, is approximately 33 days
under the conditions of 29 C and 70%
relative humidity (Park and Frank, 1948;
Young, 1970). These life stages are
generally spent in and around flour or
other stored products. Although the
intrinsic rate of natural increase, r,
(Mertz, 1970) varies with the climatic
conditions, an r of approximately .10
beetles per day can be achieved under the
standard conditions mentioned above, and
this represents a doubling in population
size once every seven days (Leslie and
Park, 1949).
In an experimental study of interspecies
competition over a wide range of climatic
conditions, Park (1954) found that a
significant correlation existed between a
species proportion of adults in the early
months of husbandry and the time to
elimination of that species from mixed
species populations. The more T. castaneum adults relative to the total present
in the second and third months of competition the longer the time to extinction
of the T. castaneumpopulation.
In a study of single species populations
of T. confusum on an unrenewed resource,
McDonald and Stoner (1968) established
several replicate populations from each of
several genetic strains. Within genotypes,
large numbers of adults in the early
months implied a long time to extinction.
The opposite correlationheld in a between
genotypes comparison, i.e., large numbers
of adults implied a short time to extinction.
Nathanson (1975) has shown that the
number of T. castaneum adults at 60 days
is a good indicator of the time to extinction
of the T. castaneum population when in
competition with T. confusum on an unrenewed medium. In this case low numbers
of adults at day 60 predict a long time to
extinction, while high numbers at day 60
indicate a relatively early extinction.
These experiments suggest that population size may be associated in a causative
way with the probability of extinction and
that the likelihood of extinction and the
time to extinction can be evaluated at a
relatively early stage in the population's
history. In addition, Ziegler (1972) discovered that 80 to 90% of T. castaneum
adults if allowed to emigrate would do so
six or seven days after eclosion. This result implies that T. castaneum individuals
are prone to dispersion at an age of approximately 3 7 days.
Materials and Methods
Adult numbers in a population at 3 7
days was the criterion chosen in studying
selection on the basis of earlier empirical
studies. In this study a population is a
founding propagule of 16 adults, whose
sex ratio is determined by chance, in an 8
dr shell vial containing 8 g of a flouryeast medium (95% by weight Elam's
stoneground whole wheat flour and 5% by
weight Fleischman'syeast type #7B).
The standard techniques used in the
laboratory of Dr. Thomas Park were
rigorously followed in the handling and
censusing of the experimental populations
(Park, 1948).
A stock culture of high genetic variability was created by mass mating 12
adult males and 12 adult females from
GROUP SELECTION
each of four "inbred" strains of T.
castaneum (for more information on the
"inbred" strains see Park et al., 1961; 2
sexes X 12 adults per sex X 4 strains = 96
adults total). The F3 generation of this
mass mating was the source of the founding propagules for generation 1 for all
treatments.
The propagule size of 16 adults was
chosen to minimize the effects of inbreeding (Crow and Kimura, 1970) and to
produce a manageable number of adults
per population. The effect of inbreeding
upon numbers of adults will be discussed
briefly in ExperimentII below.
The experiment consisted of four treatments with 48 populations per treatment
(4 treatments X 48 populations per treatment = 192 populations total). One
hundred and ninety-two groups of 16
adults were chosen at random from the
common stock described above and one
population was founded with each group
of 16. Each population was assigned a
position in one of six racks in such a way
that the populations were evenly distributed by treatment among the racks but
randomly positioned within the racks. The
racks were placed on one shelf in a dark
incubator and systematically rotated, as
racks and by position, once a day to avoid
the effects of temperature stratification.
The incubator was successfully maintained
at essentially 29 C and 70% relative
humidity throughout the course of the
experiment. After 37 days the populations
were removed from the incubator and a
census of adult beetles was taken for every
population. Immediately following the
census, selection was imposed upon the
populations accordingto treatment.
The four selection treatmentsare labelled
for convenience:
Treatment A: Selection by differential
extinction and recolonization of populations, i.e., group selection, for higher
numbersof adults per population.
Treatment B: Selection by differential
extinction and recolonization of populations, i.e., group selection, for lower numbers of adults per population.
13 7
Treatment C: No group selection; individual selection within the populations
was allowed to determine the numbers of
adults.
Treatment D: Selection and recolonization of populations by means of a table of
random numbers,i.e., a random extinctions
process.
In Treatment A, that population with
the largest number of adults at the 37-day
census was selected and divided into as
many groups of 16 adults as possible.
(Remainders less than 16 were discarded
along with any individuals who appeared
"unhealthy," e.g., missing a limb or having a split elytra. The number of "unhealthy" individuals never exceeded three
of four per population of size 160, and
some of these individuals appeared in all
treatments. Many of these "unhealthy"
individuals are the result of unsuccessful
cannibalistic attack during the pupal or
teneral stage. For these reasons, the effect
of this kind of selection against manifestly
"unhealthy" individuals is of little or no
consequence to the interpretation of the
experimentalresults.) One new population
was founded with each group of 16. The
population with the second highest number
of adults was then chosen and likewise
divided into propagulesof 16 adults. Group
selection for high number of adults was
continued in this manner until 48 new
populations had been established. In Treatment B, the procedure was identical to
that described for A except that the populations with the lowest numbers of adults
were selected and divided. More populations from Treatment B are required to
found 48 new populations than are
populations from A. (Throughout the
course of the experiment, the B founding
populations were approximately three to
five times the number of the A founding
populations.) Treatment D was similar to
A and B, but in this case a table of random
numberswas used to select the populations.
Treatment C was designed to be a control treatment which would determine the
effect of individual selection upon adult
numbers at 37 days. In this treatment one
MICHAEL J. WADE
138
EXPERIMENTAL DESIGN
COMMONSTOCK-
e
B = LOWGROUP
C =NO GROUP
SELECTION
SELECTION
SELECTION
SELECTION
48 POPULATIONS
48 POPULATIONS
48 POPULATIONS
48 POPULATIONS
16ADULTS/POP
16ADULTS/POP
16ADULTS/POP
16ADULTS/POP
A= HIGHGROUP
D=RANDOM
TREATMENTS.
I
I
37-DAYINTERVAL
DATA GATHERED
NUMBER
OF
ADULTS
IN
EACH
POPULATION
/RANDOM
|
SELECTION
K
16
16
C
16
16
48 POPULATIONS
16ADULTS/POP
REPEATED
8 TIMES
|
16
16
V
0
X
16
16
16
T
16
16
16
48 POPULATIONS
48 POPULATIONS
48 POPULATIONS
16ADULTS/POP
16ADULTS/POP
16ADULTS/POP
I
FIG. 1. Schematic outline of the design of Experiment I. See text for further explanation.
group of 16 adults was chosen at random
from each of the 48 C populations and a
new population was founded with each
group of 16. In this manner, each population in one generation gave rise to exactly
one population in the succeeding generation for C. There could be no group
selection in treatment C because there
was no differential extinction or proliferation of the populations. Any changes in
the mean numbers of adults at 37 days in
C could be attributed to individual selection operating within the populations. A
schematic diagram of the selection program is presented in Figure 1.
Conclusions were drawn from the experimental data by a between-treatments
statistical comparison of the distributions
of adult numbers. In deriving these conclusions it is reasonable to assume that
individual selection is operating in the
same direction within the populations of
A, B, and D, as it is within the populations
of C, at least in the initial stages of the
experiment.
Results
The censusing and selection procedures
were continued as described for nine 37day intervals, hereafter called generations.
The experiment was terminated at generation nine because the mean number of
adults in treatment B, the low group
selection populations, had declined to
nearly the lower limit of 16 set by the
experimentaldesign.
The census data indicated an obvious
departure from normality and for this
reason the non-parametric Kruskal-Wallis
rank sum test was employed in all betweentreatmentscomparisons.
The mean, standard deviation, and co-
GROUP SELECTION
139
and the mean of treatment B was less
than that of either C or D. However, the
differences were not statistically signifi<00
cant (see Table 1 and Fig. 2).
LL
~~~~~~~~~~~~~~~~~A
After two generations of selection, there
ot150
were highly significant differences between
0 00
treatments. In generation 3, the mean
Z
number of adults in the A populations exceeded the mean of the control (C) popu0
lations by more than 40 adult beetles. A
4
2
5
6
3
7
8
9
GENERATIONS
test of the means using the non-parametric
FIG. 2. The mean numbers of adults for the
Kruskal-Wallis rank sum statistic gave a
High (A) and Low (B) group selected populaP < .0001. Similarly, the mean number
tions and the Control (C) populations of Experiof adults for treatment B was significantly
ment I for all generations. Each point is the
less than the mean for C (P < .0005).
mean of 48 observations.
Treatments A and B differed at this time
by an average of over 70 adults per popuefficient of variability (%) for all generalation.
tions of all treatments are given in Table
These differences persisted and became
1. Figure 2 depicts the actual mean
more extreme during the course of the
population size for treatments A, B, and
experiment. At generation 9, after 8
C through generation time. Treatment D
generations of selection, the mean differis not presented here for treatment D was
ence between the A and B treatments had
statistically identical to treatment C until
increased to 158 adults per population
generation 7.
The A populations in
There were no statistical differences (see Table 1).
9
recruiting an average of
were
generation
between treatments in generation 1. This
40
times
the
number of adults reover
was expected because the founding propain the same
the
B
populations
cruited
by
gules had been chosen at random from the
common stock and selection had not yet period of time!
The means of the B and C treatments
been imposed. In generation 2, after one
generation of selection, the mean of treat- tend to decline through generation time
ment A was greater than that of C or D while the mean of the A treatment fluctu300
00
250
0
-
HIGHSELECTION"
-
NO
Z
LOW SELECTION
l]
'
SELECTION
50'
"
-
C
'.
TABLE 1. The mean, standard deviation, and coefficient of variability (%) for all treatments of Experiment I.
Rf
Ab
S.D.g
C.V.
x
Bc
S.D.
C.V.
x
Cd
S.D.
C.V.
x
De
S.D.
C.V.
G2
256
223
57
67
22
30
271
211
57
77
21
37
278
215
53
68
19
32
284
214
49
58
17
27
G3
G4
G5
196
178
279
58
60
66
30
34
23
122
88
108
52
42
25
43
48
23
152
137
170
46
58
61
31
42
36
137
121
168
46
52
70
34
43
42
G6
228
69
30
76
27
35
155
68
44
158
59
37
G7
219
64
29
48
29
60
106
59
56
122
53
43
G8
129
55
42
26
7
28
68
27
39
102
46
45
G9
178
57
32
a G = generation.
b A - high selected lines.
B = low selected lines.
20
4
18
49
41
85
69
44
64
Gla
C = control lines.
e D = randomly selected lines.
f=
mean of 48 vials.
d
e S.D. = standard deviation of 48 vials.
h C.V. = coefficient
of variation
in %.
As of G3 the following relationship is true at the 0.005 significance level: A > C = D > B.
140
MICHAEL J. WADE
ates but does not change substantially (Fig.
2). (One should not conclude from this
result that treatment A has remained
genetically similar to the initial stock, for
large differences between A and the maintained stock culture in fecundity, percent
larval survivorship to adulthood, body
weight, and female development time have
been found and will be presented in a later
paper.) It can be inferred from these data
that individual selection (C) operated, in
a way that is yet unknown, to decrease the
mean number of adults per population at
37 days. Possible mechanisms responsible
for this decline will be mentioned in the
Discussion section, but a similar decline
in productivity has been found by Dr.
David McCauley (pers. comm.) for T.
castaneum husbanded in much greater
numbersand in discrete generations.
The upsurge in mean numbersat generation 5 and the precipitous decline at
generation 8 remained unexplained. None
of the important climatic variables, temperature, relative humidity, or age of the
medium, are unusual in any respect for
the intervals of time preceding these
generations. Fortunately, the fluctuations
in mean population size occur in all treatments and therefore it can safely be
assumed that these fluctuations do not
affect the between-treatmentscomparisons
within any given generation.
In any generation, the deviations of the
A, B, and D treatments from the control
mean (C) are an explicit measure of the
effect of group selection (A, B, D) relative
to individual selection (C) (Fig. 3). Group
selection (A) acting in the opposite direction to individual selection (C) rapidly
achieved a difference in mean population
size of over 100 adult beetles. Group
selection (B) acting in the same direction
as individual selection (C) was so able to
accelerate the rate of change of population
size that a mean difference in excess of 60
adults per population was produced. The
apparent convergence of the mean population sizes of the B and C treatments, seen
in the final generations of Figure 3, should
K
140
A
0100
60
0
0-20
D
20
ir0
z
o
60
Q10
w 40
LDI4O
-
HIGH SELECTION
LOW SELECTION
--
RANDOM SELECTION
2
E
3
--
4
5
6
-
E
7
E
8
,
9
GENERATIONS
FIG. 3. The deviations of the mean numbers
of adults of the High (A), Low (B), and Random (D) selection treatments from the mean of
the Control (C) treatment for all generations of
Experiment I.
not be construed to imply a genetic convergence. It will be shown in a later paper
that the B and C treatments differ in their
respective life history parameters, and
probably achieve low population numbers
by different mechanisms.
In generation 4, the populations of
treatment D began a gradual increase in
mean adult numbers relative to the control
populations. This increase continued and
resulted in the mean of D becoming significantly different from that of C in generations seven through nine (P < .0001). An
analysis of variance of the randomly
selected populations reveals the cause of
this increase in the mean population size
of the D treatment. The explication of
this analysis is the topic of the following
subsection.
The Origin of Variation Between Populations.-For any generation the D treatment populations can be partitioned into
"lines" on the basis of the "parent"population in the previous generation. A "line"
is defined to be all the populations in a
given generation that were founded by
choosing propagules from the same
"parent"population in the previous generation. Since each population in a given
generation must be descended from some
population in the previous generation,
every population can be assigned to a
"line."
Because the entire array of 48 populations can be partitioned in this fashion,
the variance in the population size of the
GROUP SELECTION
141
lines variance is a measure of the variation
that is available for group selection.
In the D treatment, the "parent" populations for one generation are a random
sample of the populations from the precedo
ing generation. Therefore, it is possible to
generalize the information obtained from
D~~~~~~~~~~~~~~~~L
the analysis of variance and make a reliable statement concerning the betweenand within-populations variation of the
entire preceding generation.
A similar partitioning can be made for
any generation of the A or B treatments.
However, in these cases, the "parent"
populations are a deliberately biased
FIG. 4. Analysis of variance based upon the
sample of the total array of populations
square-root transformation of the data for each
generation of the Random (D) selection treatand one is not permitted to draw a general
ment.
inference from the analysis of variance.
The analyses of variance for the D
treatment for generations two through nine
array members can also be partitioned. were performed after square root transSpecifically, the total variance for a genera- formation of the data due to the sensitivity
tion can be partitioned into two com- of the F statistic to deviations from the
ponents: A between lines component and normal (Fig. 4). (A logarithmic transa within lines component. These com- formation was also investigated and similar
ponents have an important biological results obtained.) The between-lines variinterpretation which bears a direct rele- ance for the random treatment increases
vance to the comparison of group and in- relative to the total variance through
dividual selection. The within lines com- generation time. In generation two, the
ponent of the variance is a measure of the between-lines component of the variance
amount of genetic variability affecting represents less than 2% of the total varipopulation size which exists within a ance but by generation seven it accounts
population in the previous generation. This for over 70% of the total variance. This
is not an exact measure of the genetic increase in the between-populations comvariance but external environmental fluc- ponent of the variance is highly favorable
tuations have been stringently controlled to the operationof group selection.
by the experimental design and, as is inIt was noted above that the random
dicated below, a large part of this variation extinctions treatment (D) began a slow
is heritable. It is Fisher's Fundamental but steady increase in mean population
Theorem of Natural Selection (1930) that size relative to the control treatment (C)
the intensity of individual selection is in generation four (Fig. 3). The initiation
proportional to the genetic variance within
of this increase in mean numbers coincides
a population. The between lines comwith the large increment in the betweenponent of the variance is a measure of the
populations
variance in generation four
variation between populations in the pre(Fig.
4).
The
random extinctions treatvious generation and, as was stated in the
introduction, group selection requires that ment becomes group selection for large
there be differences between populations. population size once the between-populaThus, the within lines variance is a mea- tions variation reaches 35% of the total
sure of the variation that is available for variance. This group selection is the reindividual selection. while the between sult of a differential proliferation of the
ANALYSIS OF VARIANCE
RANDOM LINES
T
7
WL
4
W
2
5
4
6
GENERATIONS
VARIANCET
TOTAL *
WITHINLINES . WL
BETWEEN LINES . BL
3
7
8
9
MICHAEL J. WADE
142
TABLE 2. Analysis of variance for D = randomly selected lines (square-root transformation of data).
Generation
Total
sum of
squares
Within
lines
sum of
squares
186
158
243
216
279
291
237
311
184
127
159
129
138
89
91
162
G2
G3
G4
G5
G6
G7
G8
G9
Between
lines
sum of
squares
randomly selected populations. That is,
large parent populations will found more
new populations than will small parent
populations and this tendency becomes
heritable when the between-populations
variance reaches a certain, unspecified,
level. The total and component sums of
squares, the F statistic, and the level of
significance for each generation of treatment D are compiledin Table 2.
It is of interest to determine whether or
not an increase in the between-populations
variance also occurredin the control treatment where there was no extinction and
recolonization.In the case of neutral alleles,
population genetics theory predicts that
dividing a large population into several
smaller isolated populations will result in
an increase in the between-populations
variance and a decrease in the within-populations variance. It is not known whether
such a phenomenon would be observed if
the trait in question were undergoing
strong directional selection as was the
case for the adult population size in the
control (C) treatment. It was not possible to perform an analysis of variance
of the C populations during the experiment
because the one-to-one mapping of one
2
31
84
87
141
202
146
149
F
Statistic
Probability
level
0.25
3.57
5.68
4.60
10.98
23.83
11.00
3.67
>
<
<
<
<
<
<
<
.05
.025
.005
.005
.005
.005
.005
.005
Degrees
of freedom
2,45
3,44
4,43
6,41
4,43
4,42
6,41
9,36
generation onto the next prohibited measuring the within-populations variance.
However, at the time Experiment I was
terminated, eight C populations were
chosen by using a table of randomnumbers
and each population was divided into as
many propagules of 16 adults as possible.
One new population was then founded with
each group of 16. This procedure, which
was identical to the handling of the D
populations, permitted an anaylsis of the
within- and between-populations variance
in adult numbers. The results of this
analysis of variance are illustrated in Table
3. There was no significant betweenpopulations variance in adult numbers for
the control populations. This result implies that, when there is strong unidirectional selection within populations, the
isolation of populations in and of itself
will not result in an increase in the
between-populationsvariance for the character undergoing selection. However, a
process of random extinctions with recolonization will cause an increase in the
between-populations variance of a character despite directional selection against
that character within the populations. It
is likely that the rate of extinction and
3. Analysis of variance for the control treatment of Experiment I (square-root transformation
of the data).
TABLE
Total
Variance
Between Lines
Sum of Squares
Within Lines
Sum of Squares
F
Statistic
Degrees
of
Freedom
Probability
21.1
9.01
12.09
1.81
7,17
> 0.25
GROUP SELECTION
recolonization will determine the rate of
increase in the between-populationsvariation. That is, a high rate of random extinction would be expected to produce a
more rapid partitioning of the variance
than would a low rate of extinction. The
intensity of individual selection within
populations must also be consideredin this
hypothesis.
The rate of extinctions in the D treatment of this experimentvaried from 93.7%
to 79.2% with a mean of 88.0%, certainly
a high extinction rate. (The rate of extinctions in the A treatment was similar
to that in the D treatment whereas the
rate of extinctions in the B treatment
averaged 62.2%.) However, the individual selection within populations was of
sufficient intensity to change the mean
population size from 215 adults at generation two to 49 adults at generation nine in
treatment C. Thus it can reasonably be
assumed that a similar phenomenon could
occur when both the rate of extinctions
and the intensity of the individual selection
were operating at the lower levels
hypothesized in natural populations.
It can be inferred from the analysis of
variance of the randomly selected populations (D) that a process of random extinctions and recolonization will establish
the ideal and favorable conditions for
group selection to occur. In this way
group selection need only be a sporadic
event in nature and still accomplish large
genetic change.
143
about that expectation, which is important
for the operation of group selection.
On the other hand, one would expect
that any organism whose persistence depended heavily upon dispersal and recolonization would experience significant
levels of migration between populations.
In order to approximate more closely the
conditions expected in natural populations,
a second experiment was conducted to examine empirically the effects of migration
upon the process of group selection. By
"migration" in this experiment, I specifically mean that new populations are
founded by propagules composed of adults
from more thanaone parent population.
Materials and Methods
In Experiment II, three levels of migration were examined for each of the treatments A, B, C, and D of the previous
experiment.
1) 0% migration; propagules from
selected populations exchanged no migrants
(identical to Experiment I).
2) 25% migration; pairs of populations
were selected according to treatment and
one member of a pair contributed 12
adults and the other 4 adults to a founding propagule of 16 adults. For example,
in treatment A, the two populations with
the highest numbers of adults were
selected. The largest population then contributed 12 adults to as many propagules
as possible and the second largest population added 4 more adults to each group
of
12, for a total of 16 adults per
II
EXPERIMENT
propagule. When the largest population
Wright (1931) and, more recently, was exhausted, the remainderof the second
Maruyama (1970) have shown, on theo- largest population was divided into
retical grounds, that populations which propagules of 12 adults and the third
exchange on the average one migrant every largest population contributed groups of 4
two generationswill be genetically identical adults to these propagules, and so on. An
at equilibrium. For this reason, the identical procedure was followed in treatcomplete isolation of populations has pre- ments B and D except that in B, the parent
viously been considered necessary for populations were selected for low numbers
group selection to occur (Williams, 1966). of adults and in D, the parent populations
However, it is not the expected value of were chosen at random.
Treatment C was designed to be a conthe mean gene frequency but the variance
144
MICHAEL J. WADE
trol which would determine the effect of
individual selection upon the numbers of
adults at 37 days in populations exchanging migrants in a manner comparable to
the other treatments. Thus, in treatment
C pairs of populations were chosen at
random each generation and 12 adults
were taken from the first population of a
pair and 4 from the second population
and combined to form a new propagule
of 16 adults. From this same pair of
populations, another propagule was formed
by drawing 4 adults from the first population and 12 from the second. One new
population was founded with each of the
two propagules.
For each generation every population
in treatment C was a member of exactly
one pair of populations. For this reason,
there was no differential extinction or
proliferation of populations and there
could be no group selection. Any change
in the distribution of adult numbers in
treatment C could be attributed to individual selection operating within the
populations.
3) 50% migration; pairs of populations
were selected according to treatment and
each member of a pair contributed 8
adults to the founding propagule. The
exact procedure in this case was similar
in every respect to that outlined in (2)
above.
There are several other ways in which
migration among populations could have
been added to the process of differential
extinction and recolonization but this was
considered to be the simplest. The case
examined here is analogous to an ecological
situation in which only those populations
with a particular characteristic persist and
send out migrants but migrants from more
than one of the surviving populations can
recolonize vacant habitats. The case in
which even the populations destined for
extinction contribute some migrants is currently under study in this laboratory.
There were 18 populations in each of the
four treatments (A, B, C, and D) for
each of the three levels, of migration (18
populations X 4 selection treatments X 3
levels of migration = 216 populations
total). The number of populations per
treatment in Experiment II was thus, approximately one-third the number of
populations per treatment in Experiment
I (18 vs. 48). Because fewer parent populations were required to found 18 populations than were required to found 48
populations, the variance between populations in any treatment of Experiment II
would be less than that in Experiment I.
For this reason, the intensity of group
selection in Experiment II was not as
great as in ExperimentI.
It is likely that the random sex ratio
of the propagules exerted a proportionately
greater influence upon the progress of
group selection in Experiment II relative
to Experiment I as a result of the reduced
number of treatment populations. A
smaller proportion of the total adult population is required in the A and D treatments to form 18 propagules than is
required to form 48 propagules. Hence,
both random effects and the intensity of
individual selection are increased in ExperimentII relative to ExperimentI.
With regard to Experiment II, 18
propagules of 16 adults comprise a greater
proportion of a population than 18
propagules of 4, 8, or 12 adults. Thus, in
the A treatments of Experiment II (and
to a lesser extent in the D treatments) the
intensity of individual selection will increase with the level of migration as a
consequenceof the experimentaldesign.
In order to ask whether or not the differences obtained in Experiment I would
persist despite migration and because of
the considerable effort involved in the
monthly censusing of 408 populations
(192 + 216 = 408 total populations), it
was decided that Experiment II should
be made ancillary to Experiment I. It was
believed that some information concerning
the problem of migration vis a vis Experiment I could thus be obtained while postponing a thorough study of migration to
a later experiment.
The starting stocks for the migration
GROUP SELECTION
140
120
0MGATIN0
80f
60-
-
.200
_
0
'-
120
40,
6080+
loof
I20
A
B-B
+
40
z
1202
X8
O0-
~60?
40~
25%MIGRATION
A
D-
D
140
-.200
'_
_
-
__ ___
L
'-
r-~~
.__
?_
_
_
_
_
_
60
o 204008
10-
0140
LL_
140i
0
640
Z
G20T
100H-8060
> 1201
40~
LLJ.20-
40-
'
-
-
50%MIGRATION
A
14 5
initial generation of Experiment I. Similarly, C, "control" and D, "random",
stocks were set up from six C and seven
D populations, respectively. The D stock
was composed of descendents from two
original populations and the C stock from
six. Each of the four stocks contained
approximately 1,000 adult beetles. The
A, B, C, and D stocks, respectively, were
the source of the founding propagules for
the A, B, C, and D treatments in generation 1 of the migration experiment. Thus,
the treatment means in the initial generation of the migration experiment were not
identical across the board, and, for this
reason, all comparisonsbetween treatments
in Experiment II must be made with
referenceto generation 1.
D-
~
B,
I
2
~
--
~~
3
~~4 5
GENERATIONS
6
7
FIG. 5. The deviations of the mean numbers of
adults of the High (A), Low (B), and Random
(D) selection treatments from the mean of the
Control (C) treatment for all generations of Experiment II. The data for the three levels of
migration are presented in the following order:
5a 0% migration, 5b 25% migration, and 5c 50%
migration.
experiment were composed of adult beetles
collected from excess populations of the
fourth generation of Experiment I. A
"high-selected" stock was created by
combining all the adult beetles of four
excess populations from treatment A.
These four populations were descended
from two separate populations in generation 1. The adults were allowed to mingle
in a stock jar for approximately40 minutes
at which time groups of 16 adults were
chosen at random and used as founding
propagules for the A treatments of all
three levels of migration in generation 1
of Experiment II. The B or "low-selected"
stock was established by combining the
adults of 12 B populations in one stock
jar; these 12 populations were descended
from three separate populations of the
Results
migration experiment
the
of
The results
are summarized in Figures 5a, b, and c
and Figures 6a, b, c, and d. (Figure 5 is
analogous to Figure 3 of Experiment I
above.) This form of presentation (Fig.
6) was chosen to facilitate the examination
and interpretation of the effect of migration upon the process of group selection.
In Generation-1 for the case of 0%
migration the means of the A, C, and D
treatments were statistically identical (.10
< P < .25) although the B treatment
mean was significantly less than the mean
for the C or control treatment (P < .005).
After one generation of selection the mean
of the A treatment exceeded that of the
control by more than 90 adult beetles per
population (P < .005) and after three
generations of selection the difference was
in excess of 130 adults per population.
The mean of the D or random treatment
became statistically greater than the mean
of the control at Generation-5 (D - C =
41 adult beetles, P < .005) and remained
so for the duration of the experiment.
There was a difference between the means
of B and C treatments in Generation-1 of
95 adults and this difference increased to
122 adults by Generation-3. After that
time there was a convergencein mean pop-
MICHAEL J. WADE
146
s
300
300
HIGH
A
"
250.
-
200'
200-
10--
D
"
150 -
'
150
Cl)
LOW
250-
,
0O%MIGRATION
-25%MIGRATION
---50%MIGRATION
\
/
/
50
50
(A)
6712(B)67
m~~~~~~~~~~~~~~
LL
CD
Z
CONTROL
C
2501
LUI200
_
250t
1001
100t
50
50
(2
\
200-
'-
)
(C)
5
6
7
~GENERATIONS
RANDOM
0--'
N
2
3(D)4
5
6
7
FIG. 6. The mean numbers of adults for the High (A), Low (B), and Random (D) populations
and the Control (C) populations for all generations of Experiment II. Each graph contains the observations for three levels of migration, 0%0,25%,Xand 50%0for one selection treatment. Each point
is the mean of 18 observations.
ulation size between the B and C treatments similar to that previously observed
in Experiment I, although the B treatment
mean remained significantly lower than
the control mean (P < .005) for all
generations.
The magnitude of the deviations from
the controls for all treatments is essentially
the same in both Figures 5a and 3. Thus
the smaller number of populations per
treatment in Experiment II relative to
Experiment I did not significantly affect
the process of group selection.
Although both the A and D means for
the case of 25% migration (Fig. 5b)
initially exceeded the control mean this
difference diminished and by Generation-3
the A, D, and C means were statistically
identical. With continued selection the A
mean exceeded that of the C treatment by
an average of 45 adults per population
during generations four through seven (P
< .005 for Generations-4, 5 and 7; P <
.01 for Generation-6). The D treatment
mean was greater than that of the C treatment by 14 or 15 adults per population in
Generations-5, 6, and 7. This mean difference was not statistically significant in
Generation-5(.10 < P5 < .25) but became
so in Generations 6 and 7 (P6 < .05, P7 <
GROUP SELECTION
.005). This increase in the statistical
significance was achieved by a decrease in
the variance in adult numbers in the D
treatment and not by an increase in the
magnitude of the difference between the
D and C treatments.
For the case of 50% migration (Fig. 5c)
the trend in the difference between the A
and C treatment means was similar to that
described above for the case of 25%
migration. After an initial period of convergence (Generations-2, 3, and 4) the
mean number of adults in the A populations came to exceed that of the C populations by an average of 47 for generations
five through seven (P5 = P6 = P7 <
.005). The D treatment with 50% migration, unlike the D treatments with 0 and
25% migration in Experiment II and the
D treatment in ExperimentI, never significantly exceeded the control treatment in
mean numbersof adults. The B treatment,
however, maintained a mean difference
from the C of over 100 adult beetles per
population during generations two through
four and did not converge with C in mean
population size to the extent witnessed
with 0 and 25% migration.
Three significant differences are illustrated by the comparisonof Figures 5a, b,
and c and were noted in the discussion
above:
1) The mean of the D or random
selection treatment did not become significantly greater than the C mean in the case
of 50% migration (Figure 5c) as it did
with zero and 25% migration (Figure 5a
and b).
2) The mean deviation of the A or
high group selection treatment from the
controls was less with migration (Figures
5b and c) than it was without migration
(Figure 5a).
3) The mean deviation of the B or low
group selection treatment from the controls
was greatest in the case of 50% migration.
The trend in the D migration treatments
can be attributed to a decline in the
between-populationsvariance with increasing levels of migration. The higher the
level of migration the more homogeneous
147
the populations will become through
generation time. In addition, the experimental design itself results in fewer pairs
of parent populations with each increase
in the level of migration and in this way
also contributes to the decline in the between populations variance. It can be
concluded that the tendency toward a differential proliferation of populations in the
D migration treatments was not sufficient,
given the low level of between populations
variance, to result in a large difference
between the D and C treatmentmeans.
It is not clear that the above-mentioned
differences (2 and 3) observed in the A
and B migration treatments would have
persisted had Experiment II been continued for a longer period of time. The
inference drawn from this analysis is that
the effect of group selection upon population size is not significantly altered by
migration of the kind examined in Experiment II.
Figures 6a, b, c, and d illustrate a decline in adult numbers through generation
time. Because the decline affects all treatments it can be assumed that it does not
affect the between treatments comparisons
within any one generation. This decline
could be attributed to some form of density
dependent individual selection operating
within all populations. The increased intensity of individual selection and the
increased likelihood of interference by random effects in the A and D treatments
could result in a lower position for the
equilibrium population size determined by
the opposing forces of group and individual
selection. However, the actual cause of
the decline remains unknown.
An analysis of variance similar to that
performed on the data from the random
treatment of ExperimentI was not possible
in this experiment. The populations in a
given generation could not be partitioned
according to "parents" because often one
pair of parent populations had founded the
entire generation.
While several other interesting and important questions concerning the effect of
migration upon the equilibrium between
MICHAEL J. WADE
148
group and individual selection remain to
be explored in later experiments, the
answer to the fundamental question which
motivated Experiment II is clear: The
differential extinction and proliferation of
populations can cause or maintain genetic
differences whether the populations are
isolated or exchanging migrants, at least
under the conditions examinedhere.
The Inbreeding Effect Due to a Propagule Size of 16 Adults.-The control populations of Experiment II provide an assessment of the effect of inbreedingupon adult
population size. Each of the control populations in the "no migration" treatment,
C-0%, remained isolated from all other
populations for the duration of the experiment. On the other hand, each control
population in both the 25% migration,
C-25%, and the 50% migration. C-50%,
treatments exchanged some number of
migrants with another randomly selected
control population every generation.
Furthermore, it is extremely likely that
all females in a propagule are premated
(Park, 1933) and it is known that, although sperm transferred in later copulations takes precedence over sperm already
in the spermatheca,the two types of sperm
mix to some degree (Schlager, 1960). Both
of these aspects of Tribolium ecology serve
to decrease the effect of inbreeding due to
a founding propaguleof 16 adults.
Figure 6c illustrates the trend in the
mean number of adults at day 37 for the
C-0%, C-25%, and C-50% treatments of
Experiment II. All three treatments undergo a similar decline in the mean number
of adults. And, it can be concluded that
individual selection and not an inbreeding
effect is responsible for the trend toward
fewer adults in the control populations.
Figure 6c does show that the C-0%
populations generally achieved a somewhat lower number of adults at 37 days
than did either the C-25% or C-50%
populations. An empirical attempt was
made to assess the magnitude of this relative difference which could be attributed
to inbreeding. This was done in the followlin<yOrf
Wq
4. Comparison of the productivity of inbred and outbred populations from the control
treatments of Experiment II.
TABLE
C-0%
C-25%
C-50%
x (Outbred)
x (Inbred)
115.2
89.7
91.0
57.2
76.3
111.9
x = the mean number of adults at 37 days for six
replicates.
In Generation-6, six populations, in addition to the usual number of 18, were
established for each of the treatments:
C-0%, C-25%, and C-50%. In all three
cases, the six extra populations were
founded by choosing 1 or 2 adults at random from each of 10 populations also
chosen at random from the 18 populations
at Generation-6. The sex ratio of the
adults was left to chance. The six new
populations for C-0% were thus maximally
outbred and the mean number of adults
produced by these six populations could
be compared with the mean number of
adults produced by the inbred C-0% populations in Generation-7. Similar comparisons could be made between the inbred and
outbred populations of C-25% and C-50%.
The means of the inbred populations
were weighted according to the proportion
of adults that a given inbred population
contributed to the founding of the six
outbred populations (Table 4).
There are no statistical differences
among the three outbred means (F =
.347; df = 2,15; P > .25). There are
apparent differences among the inbred
means although using the weighted mean
prohibits statistical analysis. However, the
data from Generation-7, which are available for analysis using the Kruskal-Wallis
rank sum test, support the conclusion that
the order of the control means is C-0% <
C-25% < C-50% (P < .025). Thus the
tendency for the mean of the C-50% treatment to exceed that of the C-0% treatment
can be attributed to an increase in
homozygosity due to inbreeding.
However, the decline in mean adult
numbers through generation time by ap-
GROUP SELECTION
149
proximately 175 adult beetles is large rela- which sends out ten times as many propative to the difference between the means of gules but establishes fewer new populathe C-50% and C-0% treatments, which tions. This definition, therefore, defines a
averaged 35 adults during Generations 4 populational adaptation to be a trait which
through 6. For this reason, I have con- is the focus of or the result of a process of
cluded that individual selection, rather group selection.
than an increase in homozygosity due to
A large area of overlap exists between
inbreeding, is primarily responsible for the this definition of an adaptation of a popugeneral decline in productivity of the C lation and the definition of an individual
treatmentsin ExperimentsI and II.
adaptation. Any trait which increases the
probability of survival and reproductionof
DIscusSION
the individuals within a population and
It has been shown in Experiments I and at the same time increases the probability
II that both the group and the individual of survival and proliferation of the populaselection experiments have resulted in tion will be selected for by both individual
changes in the mean number of adult and group selection. Such a trait is conbeetles at 37 days. It has been pointed sidered to be both an individual and a
out that these changes occurred rapidly, populational adaptation. The definition of
often within two or three generations, and a populational adaptation suggested here
that the changes were large in magnitude, is thus very different from that suggested
at times exceeding 100 adult beetles per by Williams (1966). A populational or
population. The mechanism or mechanisms "biotic" adaptation in Williams' terms
responsible for the changes in population "is a mechanism designed to promote the
size remain to be elucidated. Experiments success of a biota, as measured by the
measuring sex ratio, fecundity, fertility, lapse of time to extinction" (Williams,
larval mortality, developmental time, the 1966, p. 97). If the design of such a
cannibalism of eggs and pupae by adults, mechanism also promotes the success of
the cannibalism of eggs by larvae, and individuals within the biota or population,
body weight of adults have been completed then, by the principle of parsimony, the
and will be presented in a later paper now mechanism must be judged an individual
or "genic" adaptation (cf. Williams, 1966,
in preparation.
An adaptation at the populational level pp. 92-124).
The major arguments against the operais any mechanism which enhances the
tendency of a population to send out tion of group selection, which were responpropagules and establish additional popu- sible in large part for the widespread
lations in new or vacant habitats. Under adoption of Williams' principle of parsithis definition the tendency for a popula- mony, were set forth in the introduction.
tion to persist in a habitat for a long It is of general interest at this time to
period of time is not consideredan adapta- reexamine each of these arguments in the
tion unless the number of new populations light of the experimental results discussed
founded by the population in question is in the previous sections.
It has been correctly argued that the
positively correlated with its persistence.
Similarly, an increase in the rate of generation time of the individual is short
production of propagules is not considered relative to the turnover time of the popuin iteroparous species. However,
an adaptation unless this increase results lation
this difference in and of itself does not
in an increase in the rate of establishment
warrant the conclusion that individual
of new populations. A population which selection is a faster and more efficient
sends out fewer but more successful propa- form of natural selection than is group
gules is considered to be better adapted, in selection. The rate of change in the freterms of this definition. than a DoDulation quency of a given allele depends as much
150
MICHAEL J. WADE
upon the magnitude and direction of the
selection coefficients as it does upon the
generation time. If the selection coefficients in natural populations are low,
say on the order of .01 to .001
(Lewontin, 1974), then individual selection would require 50 to 100 generations
to accomplish a significant change in the
frequency of the allele in question. It is
reasonable to expect at least one extinction
of the population during such a span ok
time even if the probability of extinction
of any given population is very small.
If the amount of between-populations
variance is large a single episode of differential extinction and recolonization can
result in a large genetic change. Therefore,
it is important in evaluating the relative
efficiencies of group and individual selection to consider not only the individual
generation and population turnover times
but also the magnitude of the individual
selection coefficients and the betweenpopulations variance.
It has been repeatedly emphasized that
a significant between-populations variance
is necessary for the operation of group
selection. It is the origin and maintenance
of this between-populations variance that
has been consideredanother major obstacle
to group selection. Most of the previous
theoretical work on group selection has
been based upon a number of assumptions
which do not provide for the development
of a significant amount of between-populations variance (Wilson, 1975, is a notable
exception). In the absence of the required
variance, it is not surprising that the conclusion reached by these papers has been
that group selection can operate only under
a restrictive set of parameters which are
not likely to be realized in natural populations.
The analysis of variance for the D
treatment populations (Experiment I) revealed that a pattern of random extinctions
with recolonization will create the necessary and favorable conditions for group
selection to occur. This is due to the
conversion of an increasing proportion of
t'hi t(ltsl
vu.ri.nc.e into t'he hi-twi-n-nonuila-
tions component of the variance. The
random treatments (D) of Experiment II
offer some insight into the way in which
migration between populations may affect
this process. The homogenizing influence
of 50% migration was sufficient to prevent
an overall increase in mean adult numbers
relative to the control populations (C),
whereas 255%migration was not. It can
be hypothesized that as the level of
migration between populations increases,
the rate of conversion of the variance will
decrease for any fixed level of extinction.
The third major argument that is
offered against the process of group selection states that random events, such as
temporarily unequal sex ratios or changing
age distributions, will introduce a large
margin of inefficiency into the group
selection process unless the number of
populations involved is large.
This objection can be met in part by a
reexamination of the design of Experiments I and II. Eighteen populations
were involved in each treatment of Experiment II and despite the uncontrolled sex
ratio of the founding propagules each
generation, the results of Experiment II
were qualitatively similar to those of Experiment I, which had approximately three
times as many populations per treatment.
It is reasonable, however, to expect that
the degree of inefficiency that can be
tolerated will be related to the intensity of
group selection.
In addition to modifying some of the
arguments that have been raised against
group selection, the experimental results
may prove useful in the understanding of
the process of speciation. Speciation can
be viewed as a process which converts the
variation within populations to variation
between populations (Lewontin, 1974).
Again referring to the data from the D
treatment populations of Experiment I, it
has been shown empirically that a process
of random extinctions with recolonization
will convert an increasing proportion of
the total variance into the between-populations component of the variance. Thus, in
those generations during which group
GROUP SELECTION
151
selection is not operating, an entirely
alter the progress of group selection
randomprocess of extinctions will be creatrelative to the case with no such
ing potentially favorable conditions for
migration.
group selection to occur at some later
ACKNOWLEDGMENTS
time.
If the population structure of certain
It gives me great pleasure to acknowlorganisms is such that local extinctions edge the helpful advice and criticism of
occur relatively frequently, one would ex- Dr. Thomas Park, Professor Emeritus at
pect a large between-populations variance the University of Chicago; I have also
to accumulate rapidly. These types of benefited from the discussion of my ideas
organisms might therefore be expected to with Montgomery Slatkin, David Mertz,
have a greater rate of speciation than Michael Nathanson, Joel Sohn, R. C.
organisms for which local extinctions are Lewontin, Janice Spofford, R. D. Alexa relatively rare occurrence. Group selec- ander, Don Willard, Richard Horwitz, and
tion might very well be one of the greatest Patricia McElroy. The comments of C.
creative forces for evolutionary change as Istock and an anonymous reviewer much
Wright (1931) suggested over 40 years improved the original manuscript. Ora
ago.
Lee Watts and Timothy Wade provided
SUMMARY
technical assistance in the laboratory at
In summary, the empirical data gathered various times during the course of the
in this experimental study of group selec- experimental work. This work was supported in part by a USPS Training Grant
tion permit the following conclusions:
awarded to the Department of Theoretical
1. When group and individual selection Biology at the University of Chicago,
operate upon a trait in opposite Grant Number GM-2037.
directions, group selection can accomplish a genetic change which
LITERATURE CITED
occurs rapidly and is in large magni- ALLEE, W. C. 1940. Concerning the origin of
tude.
sociality in animals. Scientia 1940:154-160.
2. When group and individual selection AMADON,D. 1964. The evolution of low reproductive rates in birds. Evolution 18:105-110.
operate in the same direction upon a
1954.
ANDREWARTHA, H. G., AND L. C. BIRCH.
trait, the rate of change of the trait
The distribution and the abundance of aniin question can be significantly
mals. Univ. of Chicago Press, Chicago, Illinois.
accelerated relative to the rate of BOORMAN, S. A., AND P. R. LEVITT. 1973.
Group selection on the boundary of a stable
change of that trait under individual
population. Theoret. Pop. Biol. 4:85-128.
selection alone.
J. 1962. Evolved regulatory mech3. A process of random extinctions will BRERETON,
anisms of population control. pp. 81-73 In
establish the ideal and favorable
Evolution of living organisms. G. W. Leeper
conditions for group selection to oc(ed), Melbourne Univ. Press, Melbourne.
cur by converting an increasing pro- BROWN, W. L. 1958. General adaptation and
evolution. Syst. Zool. 7:157-168.
portion of the total variance in adult
soft selecnumbers into the between-populations CHRISTIANSEN, F. B. 1975. Hard and
tion in a subdivided population. Amer. Natur.
componentof the variance.
109:11-16.
4. A process of random extinctions can CROW, J. F., AND M. KIMURA. 1970. An introbecome group selection if there is a
duction to population genetics theory. Harper
and Row, Publishers, New York.
differential proliferation of the surC. 1878. The origin of species. D.
DARWIN,
viving populations.
and Co., New York.
Appleton
5. Migration, defined to be founding of
DUNBAR, J. S. 1960. The evolution of stability
new populations by varying proporin marine environments: natural selection at
tions of migrants from two parent
the level of the ecosystem. Amer. Natur. 94:
129-136.
populations, does not qualitatively
152
MICHAEL J. WADE
P. L. 1934. Vulnerability of BobWhite populations to predation. Ecology 15:
110-127.
FISHER,
R. A. 1930. The genetical theory of
natural selection. Clarendon Press, Oxford.
GADGIL, M.
1975. Evolution of social behavior
through interpopulation selection. Proc. Nat.
Acad. Sci. 72(3):1199-1201.
GMPIN,
M. E. 1975. Group selection in predator-prey communities. Princeton Univ. Press,
Princeton, N. J.
HARTMANN, L. VAN.
1955. Clutch size in polygamous species. Acta XI. Cong. Int. Ornith.,
Basel. pp. 450-453.
HALDANE, J. B. S. 1932. The causes of evolution. Longmans, Green & Co., New York.
HAMILTON,
W. D. 1964. The genetical evolution of social behavior I, II. J. Theoret. Biol.
7:1-52.
. 1966. The moulding of senescence by
natural selection. J. Theoret. Biol. 12:12-45.
HORN, H., AND R. H. MAcARTHUR.
1972. Competition among fugitive species in a harlequin
environment. Ecology 53:749-752.
HINTON, H. E. 1942. Secondary sexual characteristics of Tribolium. Nature 149:500.
KING, C. E., AND P. S. DAWSON.
1972. Population biology and the Tribolium model. Evol.
Biol. 5:133-227.
LACK, D.
1954. The natural regulation of animal numbers. Clarendon Press, Oxford.
LESLIE, P. H., AND T. PARK.
1949. The intrinsic rate of natural increase of Tribolium
castaneum Herbst. Ecology 30:469-477.
LEVIN, B. R., AND W. L. KILMER.
1974. Interdemic selection and the evolution of altruism:
a computer simulation study. Evolution 28:
527-545.
LEVIN, S. A. 1974. Dispersion and population
interactions. Amer. Natur. 108:207-228.
LEVINS, R.
1970. Extinction. In Some Mathematical Questions in Biology. Amer. Math.
Soc. 2:75-108.
LEVINS,
R., AND D. CULVER. 1971. Regional
coexistence of species and competition between
rare species. Proc. Nat. Acad. Sci. 68:12461248.
LEWONTIN, R. C. 1958. Adaptations of populations to varying environments. Cold Spring
Harbor Symp. Biol. 22:395-408.
. 1962. Interdeme selection controlling a
polymorphism in the house mouse. Amer.
Natur. 96:65-78.
1965. Selection for colonizing aLility. In
The Genetics of Colonizing Species. Edited
by H. G. Baker and G. L. Stebbins. Academic
Press, New York.
. 1970. The units of selection. Annu. Rev.
Ecol. Syst. 1:1-18.
. 1974. The genetic basis of evolutionary
change. Columbia Univ. Press, New York.
ERRINGTON,
R. H., AND E. 0. WILSON. 1967.
The theory of island biogeography. Princeton
Univ. Press, Princeton, New Jersey.
MARUYAMA, T. 1970. Effective number of alleles in a subdivided population. Theoret.
Pop. Biol. 1:273-306.
J. 1964. Group selection and
MAYNARD-SMITH,
kin selection. Nature 201:1145-1147.
D. J., AND L. J. DAVIDSON. 1965.
McDONALD,
Population fitness in Tribolium. I. Amer.
Natur. 99:463-470.
D. J., AND L. STONER. 1968. PopuMcDONALD,
lation fitness in Tribolium. II. Population
characteristics influencing the capacity for survival. Amer. Natur. 102:323-336.
D. B. 1969. Age distribution and
MERTZ,
abundance in populations of flour beetles. I.
Experimental studies. Ecol. Monogr. 39:1-31.
* 1970. Notes on methods used in life history studies. In Readings in ecology and
ecological genetics. J. H. Connell, D. B.
Mertz, and W. W. Murdoch (eds.), Harper
and Row, New York.
. 1972. The Triboluim model and the
mathematics of population growth. Annu.
Rev. Ecol. Syst. 3:51-78.
M. 1975. The effect of resource
NATHANSON,
limitation on competing populations of flour
beetles, Tribolium spp. Bull. Ent. Res. 65:
1-12.
1933. Studies in population physiolPARK, T.
ogy. II. Factors regulating the initial growth
of T. confusum populations. J. Exp. Zool.
65:17-42.
. 1934. Observations on the general biology of the flour beetles Tribolium confusurn
Duval. Quart. Rev. Biol. 9:36-54.
* 1948. Experimental studies of interspecies
competition. I. Competition between populations of the flour beetles, Tribolium confusum
Duval and Tribolium castaneum Herbst. Ecol.
Monogr. 18:265-308.
1954. Experimental studies of interspecies
competition. II. Temperature, humidity, and
competition in two species of Tribolium.
Phys. Zool. 27:177-238.
1948. The fePARK, T., AND M. B. FRANK.
cundity and development of the flour beetles,
Tribolium confusum and Tribolium castaneum
at three constant temperatures. Ecology 29:
368-374.
1964.
PARK, T., P. H. LESLIE, AND D. B. MERTZ.
Genetic strains and competition in populations
of Tribolium. Phys. Zool. 36:97-162.
PARK, T., D. B. MERTZ, W. GRODZINSKI, AND
T. PRUS. 1965. Cannibalistic predation in
populations of flour beetles. Phys. Zool. 38:
289-321.
RAND, A. L. 1954. Social feeding behavior of
birds. Field. Zool. 36:1-71.
SCHLAGER, G. 1960. Sperm precedence in the
MAcARTHUR,
GROUP SELECTION
fertilization of eggs of Tribolium castaneum.
Ann. Ent. Soc. Amer. 53:557-560.
SHRODE,R. R. 1960. Evidence that mating is
random in Tribolium castaneum. Tribol. Inform. Bull. 2:15-16.
SIMBERLOFF, D. S., AND E. 0. WILSON.
1969.
Experimental zoogeography of islands: the
colonization of empty islands. Ecology 50:
2 78-296.
SKUTCH, A. F. 1961. Helpers among birds.
Condor 63:198-226.
SLATKIN, M. W. 1974. Competition and regional coexistence. Ecology 55:128-134.
SOKOLOFF, A. 1974. The biology of tribolium,
Vol. 2. Clarendon Press, Oxford.
STANLEY, M. S. M., AND A. W. GRUNDMANN.
1965. Observations on the morphology and
sexual behavior of Tribolium confusum
(Coleoptera: Tenebrionidae). J. Kan. Ent.
Soc. 38:10-18.
STURTEVANT, A. H. 1938. Essays on evolution.
II. On the effects of selection on social insects. Quart. Rev. Biol. 13:74-76.
VAN VALEN,L. 1975. Group selection, sex, and
fossils. Evolution 29:87-94.
WMLLIAMS, G. C. 1964. Measurement of consociation among fishes and comments on the
evolution of schooling. Mich. St. Univ. Mus.
Publ.. Biol. Ser. 2 :351-383.
153
. 1966. Adaptation and natural selection.
Princeton Univ. Press, Princeton, New Jersey.
. 1971. (Ed.).
Group selection. Aldine
Atherton, Inc., New York.
WMSON, D. S. 1975. A general theory of group
selection. Proc. Nat. Acad. Sci. 72:143-146.
WILSON,E. 0. 1973. Group selection and its
significance for ecology. Bioscience 23:631-638.
WILSON, E. O., AND D. S. SIMBERLOFF.1964.
Experimental zoogeography of islands: defaunation and monitoring techniques. Ecology 50:267-278.
WRIGHT,S. 1931. Evolution in Mendelian populations. Genetics 16:93-159.
. 1945. Tempo and mode in evolution: a
critical review. Ecology 26:415-419.
. 1956. Modes of selection. Amer. Natur.
90: 5-24.
J. C. 1962. Animal disperWYNNE-EDWARDS,
sion in relation to social behavior. Hafner
Publishing Company, New York.
YOUNG, A. M.
1970. Predation and abundance
in populations of flour beetles. Ecology 51:
602-619.
ZEIGLER,J. 1972. Regulation of unconfined
populations of Tribolium. Ph.D. Thesis, Univ.
of Chicago.