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BiologicalJoumal of the Linnean Society, 14: 303-3 1 7 . With 3 figures
November/December I980
Temporal changes of gene frequencies in Cepaea hortensis
SARAH WALL*, M. A. CARTER ANDBRYAN CLARKE**
Department of Biological Sciences, Portsmouth Polytechnic King Henry I Street, Portsmouth POI 2DY, England
Accepted for publication April 1980
There have been few studies analysing long-term changes of gene frequencies in natural populations. This work is the first report of such changes in the land snail Cepaea hortensis (Mull).
Collections of C . hortensis were made at Silbury Hill, Wiltshire in 1957, 196s and 1978. The banded phenotype significantly declined in frequency between 1963 and 1978. I t is argued that the decline, which was statistically homogeneous at 15 separate sites within the area, was a consequence of natural selection. The average selection coefficient against the banded homozygote is estimated to have been greater than 10%.
KEY WORDS : -Cepaea hortmis - directional selection- selective intensities.
CONTENTS
Introduction . . . . . . . : . . . . . . . . . . . . . . 303 Description of the sampling area . . . . . . . . . . . . . . . . . 304 Methods . . . . . . . . . . . . . . . . . . . . . . . 305 Results . . . . . . . . . . . . . . . . . . . . . . . . 306 Discussion . . . . . . . . . . . . . . . . . . . . . . . 3 14 Acknowledgements . . . . . . . . . . . . . . . . . . . . 3 16 References . . . . . . . . . . . . . . . . . . . . . . . 3 16
INTRODUCTION
Cepaea hortensis, like its close relative C. nemoralis (L.1, shows a striking genetic polymorphism in the colour and pattern of its shell (Cain & Sheppard, 1954; Clarke, 1962). In several regions of lowland Britain both species show variations of phenotype frequencies that are related to the types of habitat in which they live. Because the phenotypes are known to be determined genetically and because the environment has little or no direct effect on their expression (see Murray, 19751, the differences between habitats are almost certainly the result of natural selection. The best explanation, for some of the differences at least, is that they are due to selective visual predation, which has been demonstrated ex- perimentally in C. nemoralis (Sheppard, 1951; Wolda, 1963; Carter, 1967).
In other regions, particularly where the snails live on sand dunes or chalk downland, the pattern of variation is rather different. The frequencies of
'' Prcsent dtldt r%: Departinent of Botany, The University, Manchester M I 3 9PL, England. *'Genetics Research Unit, Queen's Medical Centre, Clifton Boulevard, Nottingham NG7 ZUH, England.
303 0024-4066/80/070303 + 15$02.00/0 0 1980 The Linnean Society of London
304 S . WALL ET AL.
phenotypes in populations are more easily related to geographical position than to the nature of the habitat. Areas much larger than the panmictic unit show characteristic frequencies of phenotypes, and may be separated from other such areas by sharp morph-ratio clines. The causes of these ‘area effects’ have been the subject of debate (Cain & Currey, 1963; Goodhart, 1963; Wright, 19651, but in some sand dune populations of C . nemoralis, where sampling has been repeated over long intervals of time (Clarke & Murray, 1962a, b; Murray & Clarke, 19781, it has been possible to demonstrate selection and to estimate selection coefficients. Murray 8c Clarke (1978) note that studies of long-term genetic changes in natural populations can only be accomplished under a rather special set of circumstances. Populations of C . hortensis are potentially as satisfactory for this kind of analysis as those of C . nemoralis.
A group of populations of C. hortensis on Silbury Hill, Wiltshire, has been studied intermittently since 1957. On the basis of recent evidence about the life history of hortensis (Williamson, 19791, we can conclude that this period covers about five generations. During the period the frequencies of some phenotypes have remained approximately stable, but there have been clear and consistent changes in the frequency of the banded morph.
DESCRIPTION OF THE SAMPLING AREA
Silbury Hill, Wiltshire, stands beside the A4 London-Bath road (Ordnance Survey Grid Reference SU 100685). Approximately 4500 years old (Vatcher & Vatcher, 19761, it is the tallest prehistoric structure in Europe and consists of a truncated conical chalk mound 40 m high, tapering from the base, which has a diameter of about 160m, to a flat top with a diameter of about 30m.
Detailed quantitative measurements of the vegetation have not been made, but we have noted the major plant species present in each sampling area. The hollow between the road and the hill (see Fig. 11 is dominated by long grass with Heracleum sphondylium L. and Urtica dioica L. Other plant species in the area include, Rumex acetosella L., Ranunculus repens L., Plantago lanceolata L. and Geranium sp.
The hill is covered mostly by grass, which is shorter than that in the hollow. Our notes suggest that the grass on the hill was longer in 1978 than in previous years. Other plant species found on the hill include Cirsium sp., Urtica dioica, Heracleum sphondylium and Galium aparine L.
Cepaea hortensis is common over the hill, and in the area immediately surrounding it; C. nemoralis has not been found there. Helix aspersa Mull., Arianta arbustorum (L.) and Trichia striolata (Pfeiffer) occurred in most of our samples. Helicella itala (L.) was found at a single site (251 in 1978 and at the same site, and an adjacent one, in 1963.
During the period of our work the sampling area has suffered disturbance. Archaeological excavations took place in 1959 and 1968. The 1968 excavation formed the subject of a B.B.C documentary and made the hill a popular tourist attraction. Since then a fence has been erected around the base of the hill to prevent access by the public, and man-made disturbance has been curtailed. Rabbit warrens were observed at two sites (20,231. Judging by the occurrence of faeces, rabbits were scarcer in 1978 than in 1957.
GENE FREQUENCIES IN CEPAEA HORTENSIS 305
Figure I . Sketch map of Silbury Hill, Wiltshire. 0 1957, 1963 and 1978 collecting areas; + 1957 and 1978 collecting areas;. 1963 and 1978 collectingareas; 0 1978 collectingareas.
METHODS
Sampling
Samples of C. hortensis were collected during 1957, 1963 and 1978, care being taken to avoid collecting only those snails that were obvious to the eye. Figure 1 shows the location of the collecting sites. Seventeen of the localities sampled in 1978 had been sampled in 1963 and/or 1957. The position of each site was described by reference to permanent topographical features. This allowed quite accurate relocation to the populations, particularly because one of us (B.C.) was present at every occasion when samples were taken. It is estimated that, with one exception, the maximum error in relocation is f 5 m. The exception is that the exact position of sample 2 (1957) is uncertain because of faulty recording. It corresponds either to sample 11 or to sample 12 of 1978, but neither the field notes nor the gene frequencies discriminate between these alternatives. Both alternatives have been considered during our analysis.
306 S . WALL ET A L
The size of the panmictic unit for C. hortensis is not known. I t is generally considered to resemble that of C. nemoralis, and to be 30-40m in diameter (Lamotte, 195 1 ; Murray, 1963). The samples at Silbury, with four exceptions, were collected within areas of 7 x 7 m and are therefore likely each to contain snails from a single panmictic unit. Three exceptional samples were collected within areas of 10 x 10 m. The fourth (sample 1 of 1957) was taken from an area of 40 x 10 m, and has not been used in the analysis. As far as possible the areas were sampled to extinction.
Live snails were collected and classified by age (mature or immature) and by shell colour and pattern according to the criteria given by Clarke (1960). The shell phenotypes were, in general, unambiguous. Exceptions were a few shells that were brown in colour, but with a pinkish tinge. They were classified as brown. The only other ambiguities were in the scoring of band-fusions, but these uncertainties were also rare. In no case did ambiguous phenotypes exceed 2% of a sample, and most samples were free of them.
RESULTS
Table 1 records the phenotypes of the live adult snails collected at Silbury Hill. As mentioned above, the position of sample 2 of 1957 is uncertain, although it
is near the 1978 locations 11 and 12. We note, however, that pairing sample 2 with either of the 1978 samples makes no significant difference to the results of the analysis. In the Tables, sample 2 of 1957 has been paired with sample 11 of 1978. This gives the closer correspondence in the proportions of the various morphs. When 2 is paired with 11, the estimated decline in the frequency of the banded gene from 1957 to 1978 is 0.005. When it is paired with’12, the estimated decline is 0.129. Thus we have chosen the combination that minimizes the change in gene frequency.
A comparison of the samples from 1957 and 1963 shows that there are differences in the frequencies of morphs between them, but that the differences do not seem to be consistent between localities, either in direction or magnitude (Table 1). A comparison of the 1963 and 1978 samples, however, shows differences too large and too consistent to be due to sampling errors. The largest and most regular changes were in the frequency of the banded phenotype. There was an overall decrease between 1957 and 1978, due almost entirely to changes between 1963and 1978 (seeFig. 2).
All our samples contained banded snails. There are five pairs of samples available for comparing the years 1957 and 1963, fifteen pairs for comparing 1963 and 1978, and seven pairs for comparing 1957 and 1978. For the last comparison there are eight possible pairs, but one of them (sample 1 of 1957 with sample 14 of 1978) has been excluded from the analysis because the 1957 sample was taken from a large area (40 x 10 m). If it is included the decline in banded morphs becomes even more significant.
The methods of estimating selection coefficients and their variances, and of determining the overall mean selection coefficient and its variance (weighted for sample size), have been discussed by Clarke 8c Murray (1962a, b) and Murray 8c Clarke (1978).
The banded gene is inherited as a Mendelian recessive. Its phenotypic expression seems not to be affected directly by the environment, and segregation
GENE FREQUENCIES IN CEPAEA HORTENSIS 307
1957 1963 1971
Figure 2. Cepaea hortensis at Silbury Hill, Wiltshire, showing the percentage of banded shells in samples from 1957, 1963 and 1978. The proportions are recorded to the nearest percent.
ratios in the laboratory conform closely to Mendelian expectations (Murray, 1963).
With selection against a recessive, and two samples separated in time, the selection coefficient against the recessive homozygote is estimated by:
S =
log.[ q n ( 1 - 4 0 ) I--+- 1 1
t +log.(;) - - 1 1 ' +- 4d1-4") 4" 40
4" 40
where qo and qn are the initial and final gene frequencies (obtained from the square root of the frequency of the recessive phenotype), and t is the number of generations. The variance is given by:
YS) =
where No and Nn are the initial and final sample sizes. If they are not significantly heterogeneous, the various estimates can be combined into a weighted mean selection coefficient:
EL s - % I )
4 9
which has the variance
Tab
le 1
. The
com
posi
tion
of s
ampl
es o
f Ce
paea
hor
tens
is co
llect
ed a
t Silb
ury
Hill
in 1
957,
196
3 an
d 19
78
Ye!l
ow
Pink
B
row
n
5 1 53
2 36
71
34
13
19
72
21
6 35
38
28
53
22
33
13
39
16
15
5 11
22 8 4 3 9 5 19
12 6 10 4 2 3 2 1 22
3 1
4
-_
_
1 1
1
43
1
1
2 1
1 2
1
1
1
21
2
I
44
19
9 15
18
21
13
15
1.5
3 3
1
3
31
3-
-
124 86
2 17
1
11
73
122 40
129 43
Y 12
045
110
Y 12
345s
px2
74
Y I0
345
82
1 5
21
12
41
21
1
6
Y1(
23)4
5
PB
JD
MA
C
SW
BC
C
PB
JD
MA
C
SW
BC
C
MA
C
BC
C
AC
PB
JD
M
AC
SW
B
CC
PB
JD
M
AC
SW
B
CC
M
AC
B
CC
A
C
PB
JD
MA
C
SW
BC
C
MA
C
BC
C
AC
PB
JD
M
AC
SW
B
CC
M
AC
B
CC
A
C
JDC
11/7
/18
11/7
/18
3 1/
8/63
vl s r
11/7
/18
h
Y b r-
11/7
/78
3 1/
8/63
11/7
/18
31/8
/63
12/7
/78
3 1/
8/63
1511
15 7
>ENE FREQUENCIES I N CEPAEA HORTENSIS 30 9
P- . P- . .c
m P-
P-
W m ‘ D . . m . . F- .
F- . - N 2 - - m
N
F- 00
m W
F- m
D a Ic1
* m N >
N N 00
m 4
- N N
N
v)
m
P-
N v) v) N m m - N
N N - c v) m
2
m
P- m
N 2
r- + N W
0, W 0 h
- m
m d m
N N
2 * v) W
h - d m
w - 2 m
b, P- m 2
w
- 0 -
Tab
le 1
cont
inue
d
Yel
low
Pi
nk
Brown
22
43
2 1
2 1
1
15
50
60
14
1 3
1 1
5
I
16
22
16
93
82
11
1
2 3
1
PB12345
Y(d
dd)(
dd)
11
25
12
41
1
11
1
3 1
Y12
345s
px5
21
12
11
1 12
2
4 1
1
51
1
17
28
21
6 8
1
3 2
Y1(
23)(
45)
18
13
I6
6 3
1
11
1
2 B
12(3
45)
19
28
57
10
1 4
11
32
3
1 Y
(12)
345
20
26
31
21
3 9
2 3
23
21
84
62
1
21
16
22
7 6
1 1
1
92
33
23
1
1 1
Y12
345s
p
14
138
69
66
72
10
45
112
101 68
54
44
BC
C
MA
C
sw
PB
JD
BC
C
SW
MA
C
MA
C
BC
C
AC
B
CC
PB
JD
M
AC
SW
B
CC
PB
JD
M
AC
SW
B
CC
PB
JD
M
AC
SW
B
CC
PB
JD
M
AC
SW
B
CC
M
AC
B
CC
A
C
PB
JD
MA
C
SW
BC
C
MA
C
BC
C
AC
JD
6/6/
57
12/1
/18
12/1
/18
3 1/8
/63
v, s r
12/1
/78
Y
1211
17a
1/7/
51
F h
L r
12/1
/18
12/l
l18
31/8
/63
12/7
/78
3 1/
8/63
5 5
1
5
22
25
40
4 1
3
23
38
24
15
3 9
21
16
10
12
2
9 14
8
71
24
43
28
27
1 20
4
2
7 6
10
6
25
23
1 13
12
1
1
11
2 10
.5
2 1
26
41
3 9
16
2
13
1 3
8 2
28
42
40
8 2
2
29
38
21
12
1 10
1
30
27
22
12
6 I7
3
1
Y: 5
45
2 2
1 2
2
1
11
2
1
2 2
1
3
11
12
11
1
1 1
1
1
1
1
23
2
1 4
1
1 2
12
17
1
Y: 5
4.5
Y( 1
2K34
5)x 2
17
77
95
67
41
136 31
52
32
79
29
102 90
103
BC
C
PB
JD
MA
C 5W
BC
C
PB
JD
MA
C
5W
BC
C
MA
C
BC
C
AC
BC
C
PB
JD
MA
C
SW
BC
C
MA
C
BC
C
AC
PB
JD
M
AC
SW
B
CC
M
AC
B
CC
A
C
PB
JD
MA
C SW
BC
C
MA
C
BC
C
AC
PB
JD
M
AC
5W
B
CC
PB
JD
M
AC
SW
B
CC
PB
JD
M
AC
SW
B
CC
1/7/
57
12/7
/78
12/7
/78
3 1/
8/63
1/7/
57
12/7
/18
3 1/
8/63
12/7
/78
3 1/8
/63
12/7
/78
3 1/
8/63
12/7
/78
12/7
/78
1217
17 8
E
312 S. WALL ET AL
(5P)SZI
SPSZI
. 00000
24
a .s{ 00000
GENE FREQUENCIES IN CEPAEA HORTENSIS 313
Table 2. The selection coefficients of the banded homozygote at Silbury Hill, Wiltshire
Numbers of adult Banding gene Sample" snails collected frequencies Selection coefficients Variances Number 1957 1963 1978 qo qm qn S, s2 s, V(d, VM? VM,
2 181 86 0.776 0.755 0.0499 0.00854 4 39 122 0.716 0.627 0.1842 0.01564 5 44 130 0.723 0.656 0.140 0.0 1432 6 82 76 110 0.848 0.851 0.809 0.019 0.1099 0.0754 0.09807 0.01105 0.00564 7 7 1 99 0.864 0.841 0.0684 0.01341 8 106 87 0.858 0.788 0.1280 0.00510
1 1 87 104 157 0.719 0.700 0.714 0.1023 -0.0313 0.0087 0.06355 0.00886 0.00481 12 122 66 0.653 0.590 0.1354 0.01320 13 93 120 0.803 0.639 0.3203 0.00745 16 72 66 69 0.842 0.904 0.816 -0.9526 0.2395 0.0493 0.375.55 0.01347 0.00773 20 68 101 0.813 0.856 -0.1350 0.0 1703 21 1 7 44 54 0.840 0.892 0.828 -0.6423 '0,1809 0.0251 0.70029 0.02022 0.02257 23 47 67 95 0.875 0.819 0.754 0.3264 0.1509 0.2074 0.08219 0.01141 0.00744
0.02006 24 30 136 0.875 0.809 0.1756 2 5 32 52 0.810 0.747 0.144 1 0.02275 26 30 79 0.730 0.636 0.1934 0.02079 30 5 8 103 0.830 0.842 -0.024 1 0.00822
* 1978 numbering (see Table I) . ya,, the frequency of the banding gene in 1957, qn, in 1963 and q" in 1978. S, , the selection coefficient estimated for the period 1957-1963; S,, for the period 1963-1978; and S, for the period 1957- I97 8.
The estimates for the 'banded' gene, assuming a generation time of five years, are given in Table 2. The selection coefficients obtained from the different pairs were statistically homogeneous :
1957-63: X2(4)=4.38, P > 0 . 3 ; 1963-78: X2(14) ~ 1 4 . 5 5 , P>0.3,
and were therefore combined, giving weighted mean values of
1957-63: s=0.0458 f 0.1539 (not significant), 1963-78: S = O . 1292 f 0.029 ( P < 0.001).
The gene for yellow shell colour has generally increased in frequency, but there is much variation between sites. From 1963 to 1978 eleven localities showed an increase, and four a decrease. The mean selection coefficient for this interval is 0.0934 & 0.242 (not significant).
The frequencies of shells with fused bands show some interesting patterns (see Fig. 3). In the five comparisons between 1957 and 1963 two showed a decrease and three an increase. In the fifteen comparisons between 1963 and 1978 eight showed a decrease and seven an increase. Although the changes were not consistent in direction, some of them were large (for example a decrease of about 20% at sites 16 and 21 between 1957 and 1963, and a decrease of c. 30% at site 23 between 1963 and 1978).
The relative lability of band-fusions is manifested in space as well as in time. Generally the sites higher on the hill have higher frequencies of fusions. This tendency is strongest on the south side, where there is a change in frequency from
314 S. WALL ET AL.
1957 1963 1971
Figure 3. Cepaea hortenszs at Silbury Hill, Wiltshire, showing the percentage of fused shells in samples &om 1957, 1969 and 1978. The proportions are recorded to the nearest percent.
about 30% in the hollow (site 4) to about 90% on the hill (site 261, over a distance of 25 m. Possible reasons for this lability are discussed below.
Because the inheritance of band-fusions is probably multitactorial, as in C. nemoralis (Wolda, 19691, and because there remains a possibility that their incidence is to some extent influenced directly by the environment, we have not estimated selection coefficients.
DISCUSSION
The assumptions of the method of estimating selection coefficients, and its associated problems, have been discussed by Clarke & Murray (1962a, b). We have assumed five years for the generation time because of recent work by Williamson (1975, 1979) on populations of C. hortensis. He found that most juveniles took three years to develop lips, and that snails with lips were 'sub- adult' during their first year, when they had only small gonads. Williamson found that adult survival was approximately 50% per annum in a population of C. hortensis near Durham. These figures suggest a generation time of five years, although in some circumstances the interval may be shorter (Wolda, 1963; Oosterhoff, 1977). We have considered the effect on the estimated selection coefficient of changing the generation time assumed. The equation is such that there is a linear relationship between the generation time and the estimated selection coefficient (Clarke 8c Murray, 1962). Assuming a three-year generation, the estimated selection coefficient for 1963-78 is approximately 0.08, and still highly significant.
An alternative equation to derive the variance of the selection coefficient has been suggested by Dr P. O'Donald (personal communication) :
.- . I +lo&- - - + -
40 ¶" 4. ' 40 '3'
GENE FREQUENCIES IN CEPAEA HORTENSIS 315
Using this equation, the variance becomes relatively greater as the value of q decreases. However, the frequencies of the banded gene in our samples are high enough to make the estimates of variance derived from the two equations very similar. The choice of formula does not affect the statistical significance of the results.
The systematic increase in the frequency of the unbanded morph during the period 1963-1978 is very unlikely to have been due to biases in sampling. Repeated collections from populations of C. hortensis taken over short periods are statistically homogeneous (Clarke, 1962), and any serious biases are likely to have been consistent over the years (for a discussion of this matter see Clarke & Murray, 1962a, b). The case against the 1963-1978 changes being due to bias is made stronger by the lack of such changes in the period 1957-1963. The consistency of the shifts at many different sites makes untenable an interpretation of them in terms of random genetic drift. Nor can we suppose that during the period from 1963 to 1978 the populations on the hill were invaded from elsewhere by snails with a lower average frequency of banded forms. This possibility is excluded by the persistence throughout the period of clines in phenotype frequency across the area samples (see Figs 2 & 3). Any invasion of new snails in sufficient numbers to alter the average frequency of bandeds would have produced severe distortions in the clines, and no such distortion has been observed. Thus it appears that the temporal changes were due to natural selection.
If we conclude that the changes were caused by natural selection, it is necessary to enquire what has been the agent of this selection. In relation to the general problem of polymorphism of Cepaea, two major selective agents have been suggested: predators and the effects of climate (for reviews, see Jones, Leith 8c Rawlings, 1977 ; Clarke, Arthur, Horsley 8c Parkin, 1978). Predators are known to select against morphs that stand out against the background of vegetation on which they live, but it is not obvious how the change in vegetation (an increase in its height since 1963, mentioned above) could produce a background more favourable to unbandeds. It is tempting to ascribe the shift in frequency to the effects of an exceptionally hot summer in 1976, since apriori we would expect the darker banded shells to be more susceptible to death by overheating in sunlight. Richardson (1974, 1979) found evidence in natural populations of C. nemoralis that banded shells do indeed suffer disproportionately from overheating. However, the effect was evident only in pink shells. Yellow bandeds fared as well as, or better than, yellow unbandeds. The agent of selection remains uncertain.
Finally, it is necessary to comment upon the great lability, in both time and space, of the frequency of shells with two or more bands fused together. The change in this frequency from about 30% in the hollow to about 90% on the south side of the hill over a distance of 25 m means that significant differences could be detected in samples of 100 snails taken from localities separated
only 5 or 6 m. This observation has the corollary that, regardless of
environment, the populations of C. hortensis are differentiated over extremely short distances. Migration would tend to reduce this differentiation, and we therefore conclude that although the snails are easily capable of moving five metres in a day, either they do not normally do so, or they have a tendency to return to a very limited local territory. Thus it seems likely that the estimate of the panmictic unit given above is an exaggeration.
w bil ether the changes are entirely genetic or wholly due to direct influences of the
3 16 S . WALL ET AL.
Because the fusion of two adjacent bands on the shell is the consequence of them being wide enough to abut on to each other and because the width of the bands appears to be a continuously varying character under the control of many genes (perhaps with a direct contribution by the environment during growth), the existence of a band-fusion is merely one extreme of a continuous distribution. In other words band-fusion is a ‘threshold character’, and the transition from an unfused state to a fusion may involve a very small developmental change. This may help to explain the great lability of the character.
I t is worth noting that the pattern of band fusions shows some regularity in relation to the habitat. Populations on the higher parts of the hill have higher frequencies, and this effect is strongest on the well-insolated south side, where the frequencies of fusions reach 90%. The hollow and the north side of the hill show the lowest fre uencies. It is not clear why this pattern occurs, because a
resisting exposure to heat from the sun. It is generally supposed that paler shells are favoured in regions of high insolation.
This study has raised several interesting and unanswered questions about the patterns of variation in C. hortensis. At the same time, however, it has produced unusually strong evidence for the occurrence of natural selection. I t seems certain that the ‘banded’ gene has suffered a severe disadvantage during the past fifteen years. The agent of this disadvantage remains to be discovered.
general darkening o 9 the shell, as produced by band fusion, seem ill-adapted to
ACKNOWLEDGEMENTS
We are very grateful to Dr Ann Clarke, Professor J. D. Currey, Miss Julia Dionian and Mr Paul Barrow, who helped with the collections, to the Department of the Environment (Ancient Monuments and Historic Buildings) for permission to collect on Silbury Hill, and to the Science Research Council and the Nuffield Foundation for financial support.
REFERENCES
CAIN, A. J. & CURREY, J. D., 1963. Area effects in Cepaea. Philosophical Transactiow of the Royal Soceity of
CAIN, A. J. & SHEPPARD, P. M., 1954. Natural selection in Cepaea. Genetics, 39: 89-1 16. CARTER, M. A., 1967. Selection in mixed colonies of Cepaea nemnralis and Cepaea horten5is. Heredity, 22:
CLARKE, B., 1960. Divergent effects of natural selection on two closely related polymorphic snails. Heredity,
CLARKE, B., 1962. Natural selection in mixed populations of two polymorphic snails. Heredity, 17: 3 19-345. CLARKE, B., ARTHUR, W., HORSLEY, D. T. 8c PARKIN, D. T., 1978. Genetic variation and natural selection
in pulmonate molluscs. In V. Fretter & J. Peake (Eds), The Pulmonates: 219-270. London: Academic Press. CLARKE, B. & MURRAY, J., 1962a. Changes ofgene-frequency in Cepaea nernoralis (L.). Heredity, 17: 445-465. CLARKE, B. & MURRAY, J., 1962b. Changes of gene-frequency in Cepaea nernorafis (L.); the estimation of
GOODHART, C. B., 1963. “Area effects” and non-adaptive variations between populations of Cepaea
JONES, J. S . , LEITH, B. H. & RAWLINGS, P., 1977. Polymorphism in Cepaea: a problem with too many
LAMOTTE, M., 195 1. Recherches sur la structure gknktique des populations naturelles de Cepaea nernoralis.
MURRAY, J., 1963. The inheritance of some characters in Cepaea hortensis and Cefaea nernoralis (Gastropoda).
MLJRRAY, J. J., 1975. The genetics of the Mollusca. In R. C. King (Ed.), Handbook ofGenetics, 3 : 9-31. New
London, B, 246: 1-8 1.
117-139.
1 4 : 423-443.
selective values. Heredity, 17: 467-476.
(Mollusca). Heredity, 18: 459-465.
solutions? Annual Review of Ecology and SystematicJ, 8: 19-43.
Rillletin Biologique de la France et de la Belgique, Suppl. 35: 1-239.
Genetics, 48: 605-616.
York: Plenum.
GENE FREQUENCIES IN CEPAEA HORTENSIS 317
MURRAY, J. & CLARKE, B., 1978. Changes of gene frequency in Cepaea nernoralis over fifty years. Malacologia, 1 7 : 317-381). . . . . . . . . . .
OOSTERHOFF, L., 1977. Variation in growth rate as an ecological factor in the landsnail Cepaea nemoralis.
RICHARDSON, A. M. M., 1974. Differential climatic selection in natural population of landsnail Cepaea
RICHARDSON, A. M. M., 1979. Morph frequencies of empty intact shells from Cepaea nrmoralis (L.) colonies
SHEPPARD, P. M., 1951. Fluctuations in the selective value of certain phenotypes in the polymorphic land
VATCHER, F. de M. & VATCHER, L., 1976. The Avebury Monumenls: 43 pp. London: Her Majesty’s Stationery
WILLIAMSON, P., 1975. The Feeding Ecology and Energetics of a Grassland Population of the Snail Cepaea
WILLIAMSON, P., 1979. Age determination of juvenile and adult Cepaea. Journal of Molluscan Studies, 4 5 :
WOLDA, H., 1963. Natural populations of the polymorphic landsnail Cepaea nernorali,. Archives Nkrlandaises de
WOLDA, H., 1969. Genetics of polymorphism in the landsnail, Cepaea nemoralis. Genetica, 40: 475-502. WRIGHT, S., 1965. Factor interaction and linkage in evolution. Proceedings ofthe Royal Society oflondon, B, 162:
Nrtherlnnd Journal of Zoology, 2 7 : 1-132.
nemornlis. Nature, 247: 572-573.
on sand dunes in south.west England. Journal ofMolluscan Studies, 4 5 : 98-107.
snail, Cepaea nernoralis (L.). Heredity, 5 : 125-134.
Office.
nemoralis. Ph.D. thesis. Portsmouth Polytechnic.
.5 2-60,
Zoologic, 1 5 : 38 1-47 I .
20-104.
