ENZYME VARIABILITY IN NATURAL POPULATIONS OF
DAPHNIA MAGNA 11. GENOTYPIC FREQUENCIES
IN PERMANENT POPULATIONS
PAUL D. N. HEBERT
School of Biological Sciences, University of Sydney, Sydney, Australia
Manuscript received October 25, 1973
Revised copy received January 7, 1974
ABSTRACT
In permanent habitats populations of the cyclical parthenogen, Daphnia
magna, reproduce by continued parthenogenesis and are subject to only sporadic sexual recruitment. The genetic effects of this breeding system have
been investigated by analyzing allozyme frequencies in thirteen populations
of D. magna.-Genotypic frequencies at polymorphic loci characteristically
deviated markedly from Hardy-Weinberg proportions and gametic phase imbalance between loci was frequent. Genotypic frequencies were subject to
violent, selectively determined oscillations over short periods of time. These
observations suggest that permanent populations of D. magna ordinarily consist of a limited number of highly structured genotypes. The adaptational advantages offered by such structuring may have been a major selective factor
favoring the evolution of cyclical Parthenogenesis.
CYCLICAL parthenogenesis has evolved among numerous invertebrate groups
including trematodes, rotifers, cladoceran crustaceans, and several insect
families such as the aphids (SUOMALAINEN
1950). Its adaptive significance has
generally been related to the doubling of the intrinsic rate of increase which
occurs during parthenogenesis and the selective importance of such an increase
in organisms inhabiting ephemeral environments where r selection will be
stringent (WEISMANN
1904; MAYR1963). The validity of this hypothesis has not
been critically examined. There has been no demonstration of a correlation
between environmental instability and the incidence of cyclical parthenogens.
Indeed, in very ephemeral habitats cyclical parthenogenesis would seem disadvantagous because of the necessity to complete at least two generations before
a reproductive cycle is finished. It may be for this reason that cladocerans are
largely supplanted by sexually reproducing copepod and phyllopod crustaceans
in ephemeral fresh water habitats. Moreover those cladocerans, such as Daphnia
middendor#iam, which successfully inhabit ephemeral environments, have often
1955). The assumption that
abandoned cyclical parthenogencsis (EDMONSTON
cyclical parthenogens are subject to stringent r selection also appears somewhat
dubious. Ecological analysis has demonstrated that population growth in these
animals often shows signs of being resource-limited (ALLAN1973; HALL1964;
1965).
KEEN1973; TAPPA
Genetics 77:323-334 June, 1974
324
P. D. N. HEBERT
The importance of genetic factors in the evolution of cyclical parthenogenesis
has been given little consideration. The prevalence of breeding systems characterized by obligate sexuality has led many geneticists to regard unusual breeding
systems as adaptively inferior. Referring to cyclical parthenogenesis, CARSON
(1968) suggests that “such downgrading of the sexual mode of reproduction has
a dampening effect on all evolutionary processes”. Other geneticists (FISHER
1930; WRIGHT1931, 1960) have, however, pointed out the severe constraints
which sexual reproduction imposes on the organization and utilization of genotypic variability. Under sexual reproduction allelic variation must be in HardyWeinberg proportions and variation at different loci must generally be in equilibrium. As a result only the additive component of the total variance in fitness
can be exploited, whereas during asexual reproduction the dominance and interaction components can be utilized as well. In varying environments, parthenogenesis has the additional advantage of allowing more rapid res-prise to changing
selection pressures than does sexual reproduction, as favored genotypes under
sexual reproduction will generate progeny of other genotypes. In purely parthenogenetic species the major obstacle in making use of these advantages rests in the
difficulty of constructing the necessary genotypes (MULLER1932; CROWand
KIMURA1965). Populations of cyclical parthenogens are, however, subject to
sexual recruitment. This factor would seem to be of the utmost importance, f o r
populations will be able to synthesize a wide variety of genotypes by sexual
reproduction and well-adapted genotypes can be multiplied by parthenogenesis
regardless of their structural complexity. In summary it is possible that cyclical
parthenogenesis enables more sophisticated manipulation of genetic variation
than does obligate sexuality and if so the evolution of cyclical parthenogenesis
could well be related to these advantages.
Daphnia magna, a cladoceran crustacean, provides a unique opportunity to
investigate the genetic effects of both short-term and protracted parthenogenesis.
In temporary habitats, that is in ponds which are filled with water for only a part
of the year, populations are reestablished each year from sexual eggs and reproduce parthenogenetically for two or at most three generations. In permanent
habitats, however, populations reproduce by continued parthenogenesis for long
periods and are subject to only sporadic sexual recruitment.
The sizes of the permanent populations studied varied both seasonally and
from one habitat to another, but many thousands of individuals were normally
present. Minimum population densities usually occurred during late winter and
maximum densities developed during late May or June. Periods of high population density were occasionally followed by a precipitous decline in population
size, apparently due to starvation of the population. More frequently, however,
a large population was maintained which reproduced little and existed under
conditions of strong intraspecific competition. Equilibrium populations, such as
these, ordinarily became smaller during the late autumn and in most habitats
population size wzs subject to the annual fluctuations described.
Sexual reproduction invariably accompanied the period of high population
density in late spring and occasionally occurred in the late autumn as well
E N Z Y M E VARIABILITY IN D A P H N I A
325
(BANTAand BROWN1929; STROSS
and HILL1965),but at no time were parthenogenetically reproducing individuals completely absent from a population. During
the periods of sexual reproduction large numbers of sexual eggs were produced
(1966) has shown that
which ordinarily sank to the bottom of the ponds. STROSS
an inhibitor must be destroyed by oxidation before the development of sexual eggs
can begin. In many of the deeper permanent habitats, it seemed probable that
the sexual eggs were ordinarily unable to hatch due to the reducing conditions
which were present at the bottom of the ponds. However, not all of the sexual eggs
were subjected to such unfavorable conditions. Many of the ponds fluctuated in
size and eggs which were deposited along the perimeter in the spring were dried
and subsequently resubmerged when the ponds refilled in the late autumn. These
eggs as well as the eggs which happened to come to rest in a non-reducing environment within the ponds should develop. In summary, the populations of D.magna
in permanent habitats reproduce parthenogenetically for long periods of time,
but these parthenogenetic populations are subject to a certain if variable amount
of sexual recruitment.
The present study has been directed largely toward analyzing the effects of
this long-continued parthenogenesis on the genetic variability present within
populations, but some ini'ormation has also been obtained on the amount and
nature of sexual recruitment in these habitats. A companion paper deals with
similar aspects in the intermittent populations which occur in temporary habitats.
MATERIALS A N D M E T H O D S
The populations of D.magna analyzed were located within a 50-mile radius of Cambridge,
England. A population is considered to be the Duphniu present within a single pond. Populations
are named after the nearest town. Where several populations are situated in close proximity
they have the same site name but a different number, e.g. Upware-1 and Upware-2. The precise localities of the populations and sampling techniques have been described previously
(HEBERT
1974a).
Electrophoresis was performed on polyacrylamide gels. DetaiIed methodology and a characterization of the electrophoretic variants have also been described (HEBERTand WARD1972).
Genotypic frequencies have been determined by analysis of female individuals only.
RESULTS
Genotypic frequencies: Nine of the permanent populations were analyzed on
only a single occasion. In four of the nine populations polymorphic for malate
dehydrogenase, marked deviations from H.-W. proportions were observed (Table
1) . These deviations were not the result of a consistent deficiency of any one
genotypic class. In the Past Bourn, Rookery Farm, and Stow Longa-2 populations
large heterozygote excesses were observed. In contrast, heterozygotes were absent
in the Winston Church population, which consisted entirely of individuals homozygous for either the M or I; allele of MDH. Significant deviations from H.-W.
proportions were observed in three of the eight populations polymorphic for
EST-I (Table 1). An excess of heterozygous individuals was evident in the
Wicken and Upware Farm populations, but heterozygotes were completely
absent from the Winston Church population.
326
P. D. N. HEBERT
TABLE 1
Genotypic frequencies in permanent populations+
Location and sample date
Barham
4/21/72
Boundary Farm
5/6/72
Cretingham
6/1/72
Past Bourn
10/25/71
Rookery Farm
5/6/72
Stow Longa-2
4/21/72
Upware Farm-2
4/16/72
Wicken
4/ 16/72
Winston Church
5/6/79
n
144
96
144
112
144
80
96**
120
160*
96
120*
120
140
142'*
132
106**
96**
96**
ss
SM
MM
MF
98
.02
.29
.71
.01
.79
.I8
.64
.4s
.96
.43
.01
1.00
.03
.35
.45
SF
.84
.03
.I5
.Ol
.35
.09
.03
.66
.34
.52
.53
.w
.39
.43
.92
.45
.03
.I7
.15
.42
.46
.46
.04
.I3
.25
.38
.21
.09
.02
FF
.os
.01
.34
.66
.35
.65
*P<.O2
** p < .001
f Roman : MDH
Italic: EST-I
Genotypic frequencies at several loci: When genotypic frequencies at several
polymorphic loci in the same population were compared with H.-W. proportions,
there appeared to be little correlation in the degree of differentiation at different
loci (Table 2). For example, in the Wicken and Upware Farm populations genotypic frequencies at the EST-I locus deviated markedly from H.-W. proportions,
while at the MDH locus genotypic frequencies were in close agreement with
H.-W. expectations. The highly significant deviations at both the EST-I and the
MDH loci which were observed in the Winston Church population were unique.
Moreover, the similarity of gene frequencies and the absence of heterozygotes
TABLE 2
Fit to Hardy- Weinberg proportions of genotypic frequencies in eight permanent populations
MDH
EST-I
> .80
> .80
P > .05
P > .40
P < .02
P < .Of
P > .30
p < ,001
> .IO
p > .IO
P > .30
P < .Qo1
P > .50
P>.60
P < ,001
P<
Location
Barham
Boundary Farm
G-etingham
Upware Farm
Rookery Farm
Stow Longa-2
Wicken
Winston Church
p
P
p
TO
p
< .001
P
> .40
327
ENZYME VARIABILITY I N DAPHNIA
at both loci in this population suggested some simple explanation. When single
individuals from Winston Church were analyzed for both enzymes it was found
that there was complete gametic phase imbalance between the two loci. Individuals homozygous for the M allele of MDH were invariably homozygous for
the S allele of EST-I, while the individuals homozygous for the F allele of EST-I
were also homozygous for the F allele of MDH. Since D.magna has a chromosomal number of 2nz2.F (MORTIMER
1936) it is unlikely that the EST-I and
MDH loci are on the same chromosome.
Temporal analysis of genotypic frequencies: Four of the permanent populations
were analyzed on several occasions to investigate the temporal stability of genotypic frequencies.
Longstowe: The Longstowe population was polymorphic for the S and M alleles
of MDH (Table 3). The SS genotype was not observed in any of the samples, but
drastic changes in the frequencies of the MM and SM genotypes occurred during
the six-month period in which the population was analyzed. The frequency of the
SM heterozygote increased from .I5 in April of 1971 to .58 by June and then
declined rapidly to a frequency of .22 by August. Due to the fluctuations in the
frequency of the SM heterozygote, genotypic frequencies in some samples were
in close agreement with H.-W. proportions, while in other samples frequencies
differed markedly from H.-W. expectations.
Hatley Hill: When first analyzed in early 1971, the population at Hatley Hill
consisted entirely of individuals which phenotypically resembled the MF heteroTABLE 3
MDH genotypic frequencies
Date
4/20/7 1
5/17/71
6/15/71
7/ 7/71
8/26/71
10/25/71
Date
2/24/71
6/14/71
9/13/71
10/20/71
11/29/7 1
1/13/72
3/14/72
5/19/72
* p < .01
** p < .OQI
n
ss
72
120'
126**
96*
120
48
n
%**
120**
72**
96**
96' *
72 *
SM
MM
.15
.85
.60
.42
.55
.78
.79
.40
.5 8
.a
.22
.21
MM
88**
72' *
Longstowe
.01
.26
2.3
.33
.I9
.35
.#
Hatley Hill
MF
1.cM)
.99
.74
.77
.67
.81
.65
.51
FF
328
P. D. N. HEBERT
zygote of MDH. As it was initially suspected that either gene duplication or
polyploidy might be involved, sexual eggs were collected from the population.
However, when these eggs were hatched, it was found that segregation occurred
and genotypic frequencies were in close agreement with those expected, assuming the individuals at Hatley Hill were all heterozygotes.
A single M M homozygote was detected in the June 1971 sample, and when
the population was re-analyzed in early September, the frequency of the M M
homozygote had increased considerably (Table 3). The frequency of the M M
genotype remained relatively stable at a value close to .25 throughout the fall
and winter of 1971. In the March, 1972 sample the frequency of the MM genotype was higher than in any of the previous samples, and by May its frequency
was close to .50. Despite the large increase in the frequency of the M M homozygote during the course of the study, the FF homozygote was not observed in any
of the samples.
Drastic shifts in genotypic frequencies also occurred at the EST-I locus (Table
4). The frequency of the M M and MF genotypes declined throughout the survey,
while the frequency of the SF genotype increased dramatically. The frequencies
of the SS and SM genotypes remained relatively stable, while the FF genotype
was not observed in any of the samples.
Longstowe Field-2: The Longstowe Field habitat was exceptional among the
permanent habitats because of its small size and extreme shallowness. In virtually the whole of the pond the water was less than 50 cm. deep and during the
summer months the pond contracted in size rather substantially. These factors
suggested that the Longstowe Field population might be subject to more sexual
recruitment than the other three permanent populations analyzed temporally.
The population was polymorphic for the S and M alleles of MDH and gene
frequencies at this locus were determined at regular intervals over a one-year
period (Table 5). Genotypic frequencies in these samples were on the whole
remarkably similar. The M M homozygote was consistently more frequent than
the SS homozygote, while the frequency of the SM heterozygote remained close
to .50 throughout the year. Genotypic frequencies were not significantly different
from H.-W. proportions in any individual sample. However, from May until
October of 1971 genotypic frequencies were in rather poor agreement with H.-W.
TABLE 4
EST-1 frequencies at Hatley Hill
Date
2/24/71
9/13/71
10/20/71
11/29/71
1/13/72
*P<.o5
** p < .001
n
120**
148*
96*
72**
96**
Genotypic frequencies
ss
SM
MM
IMF
.13
.25
.I8
.08
.15
.42
.35
.49
.41
.34
.I7
21
.21
.2a
.06
.a1
.01
.04
.04.
.06
FF
SR
.I3
.li
.46
.41
329
ENZYME VARIABILITY IN D A P H N I A
TABLE 5
MDH frequencies at Longstowe Field-2
Date
5 / 4/71
6/14/71
7/ 9/71
8/26/71
9/28/71
10/201/71
11/22/71
I / 3/72
2/25/72
3/27/72
5/19/72
n
96
144
146
96
119
120
96
125
119
144
1M
ss
.23
.I6
.I9
.21
.I9
.23
.20
.18
.20
.24
.24
Genotypic frequencies
SM
MM
.56
.56
.57
.57
.5 7
.56
.53
.50
.53
.48
.21
.2a
.24
.22
.24
.21
.27
.32
.27
.28
.52
.24
proportions, and considered as a whole, genotypic frequencies in these samples
were markedly different from H.-W. expectations ( xI2 = 12.23, p < .OOl). From
November, 1971 until May, 1972 genotypic frequencies were in good agreement
with H.-W. proportions in both individual samples, and in the samples taken as a
group (xI2= 0.50, p > .40). This was due to a reduction in the frequency of the
SM genotype from a value of .57 in the earlier samples to one closer to .50 in the
later samples. With the exception, then, of this single minor shift, genotypic
frequencies in the Longstowe Field population remained stable throughout the
sampling period.
Moulton: When first analyzed in 1970 the Moulton population was fixed for
heterozygotes at both the MDH and ALK-2 loci (Table 6). The population
remained fixed until at least May, 1971 but when the population was reanalyzed
four months later homozygotes were present at both loci (Table 6) and each of
the four homozygote classes were present at frequency of close to .20.
Genotypic frequencies were analyzed at both the ALK-2 and MDH loci at
monthly intervals from September of 1971 until June of 1972. During this ninemonth period the frequency of each of the homozygotes declined considerably.
The frequency of the MM homozygote of MDH remained close to .20 until
February of 1972, but in the following months it declined to a frequency of .04.
The frequency of the FF homozygote of MDH declined from .20 in September
to .10 by early December, but thereafter its frequency remained relatively
stable. The frequency of the SS homozygote of ALK-2 declined to a frequency
of .10 by early January and remained near this level for the rest of the study.
The frequency of the FF homozygote of ALK-2 declined less rapidly than the
frequency of the SS homozygote until March of 1972, but in the following months
its frequency declined rapidly. By mid-June the combined homozygote frequencies at each of the loci were less than .15, whereas nine months earlier they had
been present at a frequency of approximately .40.
As the homozygotes at both the MDH and ALK-2 loci were at an apparent
330
P. D. N. HEBERT
TABLE 6
Genotype frequencies at Moulton
Date
n
5/ 4/70
5 / 6/70
6/ 6/70
6/22/70
3/ 1/71
5/18/71
9/ 9/71
9/27/7 1
10/18/71
11/ 6/71
12/10/71
1/I 0/72
2/21/72
3/24/72
4/29/72
5/26/72
6/23/72
MM
48**
52**
48**
72**
48* *
120**
I%**
216'
IN**
128,'
144*
168**
120**
96**
120**
120**
120**
.18
.I9
.06
.20
.19
.20
.19
.IO
.08
.05
.03
MDH
MF
FF
1.oo
1.00
1.m
1.oo
1.oo
1.oo
.65
.61
.72
.67
.71
.75
.70
.87
.82
.88
.91
a1k-2
n
SS
56**
48**
.17
.20
.22
.13
.IO
.05
.11
.03
.10
.07
.06
120**
96
96,
57**
96**
96**
120**
72**
96**
loo**
96**
96**
.23
.I5
.I4
.I5
.13
.IO
.ll
.10
.I2
.G9
.09
SF
1.oo
1.oo
1 .oo
58
.67
.72
.68
.72
.77
.78
.76
.81
.86
.87
FF
.19
.I8
.14
.I7
.I5
.13
.11
.14
.07
.05
.W
* < .01
** p < .001
selective disadvantage, it was of interest to investigate whether the frequency of
individuals homozygous at both loci declined more rapidly than the frequency of
individuals homozygous at one locus and heterozygous at the other. When individuals in the late September sample were analyzed for both ALK-2 and M D H
it was found that the frequency of double homozygotes was approximately onehalf the frequency of homozygotes at one locus (Table 7 ) . As this ratio did not
change appreciably in the later samples, it can be concluded that the double
homozygotes were not subjected to more stringent selection than the homozygotes
at a single locus.
DISCUSSION
Investigation of the population structure of Daphnia magna has suggested that
populations are founded from a single or at most a few individuals (HEBERT
TABLE 7
Indiuiduals homozygous at either one or both of the MDH and ALK-2 loci al Moulton
~
~~~
~
Date
Double
homozygotes
Single
homozygotes
Ratio
9/27/71
11/ 9/71
1/10/72
3/24/72
11
20
12
8
19
43
30
17
.58
.47
.40
.47
ENZYME VARIABILITY IN DAPHNIA
33 1
1974a). It might be suggested that the Hardy-Weinberg disturbances characteristic of permanent populations result from this factor coupled with an absence
of sexual recruitment.
The clearest evidence against this viewpoint was obtained at Moulton. The
appearance within this population of homozygotes at the MDH and ALK-2 loci
at frequencies close to .20 in September of 1971 undoubtedly resulted from a
massive emergence of sexual eggs. Assuming a IAA : 2Aa : laa ratio of genotypes
among these sexual recruits, then the Moulton parthenogenetic population must
have been swamped by a hatch of ephippial individuals four times as numerous
as itself. The rapid decline in homozygote frequencies at both loci during the
following nine months indicated either strong selection against the enzyme homozygotes or alternatively strong selection against sexual recruits. The latter argument was favored by data which indicated that individuals homozygous at both
enzyme loci did not decline in frequency more rapidly than individuals homozygous at one locus and heterozygous at the other. The sexual recruits were apparently competing unsuccessfully with a highly structured genotype whose genome
was characterized by heterozygosity at the MDH and ALK-2 loci.
Clear evidence of sexual recruitment was not obtained in any of the other
populations, but large changes in genotypic frequencies were observed. I n the
Hatley Hill population the MM homozygote of MDH increased in frequency
from less than .01 to .49 during a 15-month period, but as an FF homozygote was
never encountered, it seems extremely unlikely that this change was the result
of emerging sexual eggs. Genotypic frequencies at the EST-I locus in the same
population also showed marked changes during the study, and no tendency
toward re-establishment of Hardy-Weinberg proportions was detected. Similar
fluctuations in genotypic frequeiicies were observed in the Longstowe population. In both cases, populations consisted of many thousands of individuals-so
stochastic changes in frequencies can be ruled out. Only in the Longstowe Field
population were genotypic frequencies relatively stable. As the Longstowe Field
habitat was extremely shallow, large amounts of sexual recruitment may have
occurred and been important in the genotypic stability of this population.
The present results reinforce those obtained in an earlier study (HEBERT,
WARD
and GIBSON1972) and suggest that marked instability of genotypic frequencies
is in general a characteristic of permanent populations of D. magna. In contrast,
genotypic frequencies in intermittent populations of the same species are comparatively stable, and this suggests that the instability of frequencies in permanent populations is related to the continued parthenogenesis in such habitats
rather than with selective coefficients of the enzyme variants per se. The explanation of this may lie both with the sources of genetic variability which can be
exploited and the types of selective processes which occur during parthenogenesis.
CROW(1956) has argued that epistasis will be of extreme importance in clonally reproducing organisms, and has demonstrated that chloramphenicol resistance was achieved in asexual clones of E. coli by the selection of epistatic
complexes of genes. WHITE (1970) has speculated that the dominance component may be of more importance, and that heterotic gene complexes will be
332
P. D. N. HEBERT
characteristic of parthenogenetic forms. These viewpoints are not mutually
exclusive, and in the present study evidence was found for the importance of both
factors. The Hardy-Weinberg disturbances in permanent populations were
generally associated with heterozygote excesses-clear evidence that heterosis
either at the gene or chromosomal level is important. Strong gametic phase
imbalance was observed in the Winston Church population, although no evidence
was obtained that this imbalance resulted from selective forces acting on epistatic
gene complexes. Suggestive evidence was obtained, however, in the Audley End
population where it was observed that the intensity of imbalance varied temporally (HEBERT197413). An important consequence of the presence of epistatic
interactions affecting fitness is the existence of multiple peaks of equilibrium
(WRIGHT1931, 1960). In sexual reproduction selection drives the population to
the nearest peak, and movement from one peak to another occurs only through
stochastic forces, assuming the adaptive topography is stable. In contrast, populations reproducing by cyclical parthenogenesis are capable of occupying several
peaks simultaneously, and can move from one peak to another across recombinational valleys. FORD
(1971) has suggested that the landscape model is “dangerously misleading”, and feels that there is no temporal continuity in the selective
demands placed on populations. This argument ignores the existence of environmental cycles, but, more importantly. makes the tacit assumption that welldefined adaptive alternatives necessitate environmental stability. In parthenogenetic populations the stability of genotypes suggests that adaptive peaks could
be based on relationships between the genotypes themselves. Populations of
daphniids might, for example, be subjected to “centrifugal” selection based on
some form of competitive exclusion. The rationalization f o r such a model is clear;
clones with reduced ecological overlap are more likely to tolerate one another’s
presence in a n environment than clones with similar characteristics. In its
simplest form where each population is founded from a single individual, the
selective process can be envisaged quite clearly. Each newly-founded population
would begin at a fitness center and as sexual reproduction generated an array of
genotypes, would spread out from this point forming a roughly spheroidal topography. Fitness (G) of the population would be measured by the mean deviation
of the points on the topography from the original fitness center, but the Darwinian fitness of any genotype would depend upon maximizing its linear distance
from the other points on the topography. Initially, the idealized spheroidal topography would be maintained by interaction between the fitness of each genotype
and its €requency. Eventually, however, as the variance in ZZbecame exhausted,
the density of points on the sphere would become less and less because of the
impossibility of synthesizing large numbers of alternative highly-structured
genotypes. In this critical phase, holes in the topography would begin to appear,
and as the density of points became further reduced the spheroidal topography
would decay into a collection of points widely separated in n-dimensional space.
The occurrence of this sort of selective process should in principal be testable, as
selection should lead to the development of well-defined alternative genotypes
within habitats. The evidence obtained so far is rather contradictory. At Moulton
ENZYME VARIABILITY IN D A P H N I A
333
there was good evidence for the selective maintenance of a highly structured
genotype, but no evidence for the existence of a number of genetically different
clones. The populations at Audley End (HEBERT,
manuscript in preparation)
and Winston Church showed several well-defined genotypes, but there was no
good evidence that the genotypes were the result of selective factors. To decide
conclusively whether permanent populations of D.magna ordinarily consist of a
limited number of highly structured genotypes, it will be essential both to extend
the number of polymorphic systems which can be analyzed and study the populations over long periods of time to determine the selective basis of changes in
genotypic frequencies.
It is clear from the present study that permanent populations of D. magna
regularly undergo large genetic rearrangements. Such changes may indicate the
recombinational production of novel genotypes or a readjustment in the frequencies of existing, highly-structured genotypes in response to environmental
changes. Regardless of which interpretation is correct, these results suggest that
cyclical parthenogenesis enables Daphnia populations to organize genetic variation in ways nut open to sexually-reproducing organisms.
Research was carried out at the Department of Genetics, University of Cambridge and I
should like to thank PROF.J. M. THODAY
and DR. J. B. GIBSONfor their interest in the project.
I am particularly grateful to DR. R. D. WARD
for many helpful discussions and for his assistance
with the collection of material. The support of a Commonwealth Scholarship during the research
program and a Rutherford Scholarship ar,d a University of Sydney postdoctoral fellowship during
the preparation of the manuscript is gratefully acknowledged. I would like as well to thank
PROF.L. C. BIRCH,DR. J. A. SVED,and the referees for thejr constructive comments on tbe paper.
LITERATURE CITED
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