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Biological Journal of the Linnean Society (2000), 69: 431–441. With 2 figures
doi:10.1006/bijl.1999.0402, available online at http://www.idealibrary.com.on
Changing views on melanic moths
L. M. COOK
The Manchester Museum, University of Manchester, Oxford Road, Manchester M13 9PL
Received 7 June 1999; accepted for publication 19 November 1999
The rapid rise in frequency of melanic morphs in several moth species, especially the
peppered moth Biston betularia, in industrial regions during the 19th century, and the
subsequent rapid decline, indicate the action of strong selection. There has recently been a
tendency to criticise and question all aspects of research on industrial melanism, including
the experiments which suggest that selective predation plays an important part in the changes.
These experiments are reexamined, together with evidence for changes in appearance of
tree surfaces and for relation of initial melanic frequency to subsequent rate of decline. It is
suggested that intense pollution may have been required to drive the carbonaria morph to a
high frequency, with frequency patterns over a mosaic environment smoothed by migration.
Improvements in these extreme locations then triggered the decline, with little indication of
the environmental changes in areas of moderate pollution. Reasons for criticism of past work
are discussed. Industrial melanism continues to provide an exceptional opportunity to analyse
a pattern of selection and change in gene frequency.
 2000 The Linnean Society of London
ADDITIONAL KEY WORDS:—industrial melanism – peppered moth – visual selection –
adaptation.
CONTENTS
Introduction . . . . . . . .
Fitness and frequency . . . . .
Historical context and implications
Conclusion . . . . . . . .
Acknowledgements
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References . . . . . . . .
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“. . . evolution is nothing but a by-product of improvement of adaptation. Biologists
are . . . fortunate in that they have a cast-iron example of how adaptation has
arisen, under man’s eyes, in the last hundred years. It is in the Peppered Moth
Biston betularia, which was mottled grey in colour, matching the lichens on the
barks of trees so perfectly that the moths were difficult to see, not only by man,
but also by birds that prey on them. This protective colouration was therefore
adaptive.” (De Beer, 1972)
Email: [email protected]
0024–4066/00/030431+11 $35.00/0
431
 2000 The Linnean Society of London
432
L. M. COOK
“Natural selection serves to eliminate those less qualified in the competition; that
is, to stabilize forms. Darwin, however, thought of selection not so much as
elimination of the unfit as the opportunity of the fitter, that is, adaptive change.
The best studied and most frequently cited example is the alteration of the British
peppered moth (Biston betularia). . . . The victory of the darker variety is interesting,
but it does not prove that such a selective process can account for the ability of
chameleons to camouflage themselves by reflex in a few minutes.” (Wesson, 1993)
INTRODUCTION
Melanism in moths was first noted in Britain in the early 19th century. Some
examples were referred to as industrial melanics because of the association of high
frequencies of dark coloured types with industrialized regions, but the reason for
the connection was, and continues to be, incompletely resolved. Three kinds of
explanation were considered, that darkness was caused by ingested pollutants, that
dark individuals were favoured by the overcast conditions of urbanized areas, or by
northern latitudes, and that dark individuals were better camouflaged against the
prevailing darker backgrounds. The most graphic example was the peppered moth
Biston betularia, which has a dominant melanic from carbonaria and some intermediate
dark phenotypes. Poulton (1890) discussed the effect of colour on thermal efficiency.
Heslop Harrison and others examined possible induction of melanic forms by direct
effect of pollutants (reviewed in different ways by Ford, 1964, Robinson, 1971 and
Lambert et al., 1986). Tutt (1891) noted the association of melanics with more humid
regions and the possible advantage conferred by camouflage. Leigh (1911) asked
whether one or many factors were involved: “It is very desirable and important to
know whether the colour of these dark races of moths is protective, or whether it
has some other significance. The ‘protective’ theory certainly appears to be a very
feasible one, for many of the moths have become darker in manufacturing districts
where the trees and other natural objects upon which they rest have assumed a
blackened aspect due to increase of smoke. On the other hand, I do not think we
can press the theory of ‘protection’ too closely at present, for there are many wellknown cases in which dark varieties of moths are found in localities far removed
from the influence of smoke and where they most probably rest upon light-coloured
objects.”
Work by H. B. D. Kettlewell suggested that selective predation was the main
determining factor in B. betularia, and probably in a wide range of other examples
as well. His evidence consisted of surveys which put the correlation between melanic
frequencies and urbanization on a quantitative basis (Kettlewell, 1958, 1965),
demonstration that wild birds would eat the moths if they found them (Kettlewell,
1955), and the now famous demonstration that birds discovered most readily the
forms least like the daytime backgrounds on which they rested (Kettlewell, 1973;
Rudge, 1999). Colour of resting background and heterogeneity due to epiphyte
cover, appeared to affect relative visibility. Selective predation became the accepted
explanation for the rise in morph frequency (Majerus, 1998).
Since then, further evidence has been collected. Over the last two decades
industrial environments have become cleaner and melanic frequencies lower (Clarke
et al., 1990; Mani & Majerus, 1993; Grant et al., 1998; Cook et al., 1999). There has
CHANGING VIEWS ON MELANIC MOTHS
433
also been some revision of interpretation. It has been shown that experiments
designed to detect and measure selective predation were carried out in places where
moths were not usually likely to rest if left to their own devices (Mikkola, 1979,
1984; Liebert & Brakefield, 1987; Grant & Howlett, 1988; Majerus, 1998). There
is by no means a one-to-one relation between reversion of morph frequency and
reversion of epiphyte pattern (Bates et al., 1990; Grant et al., 1998). These findings
cause us to reexamine the story, but they do not obviously require a radical revision.
Estimations of selection appear to show a correspondence between fitness and
frequency. The correlation between the condition of the sites used in experimental
studies and those actually used by the insects is likely to be high. Further lines of
experimentation are suggested, but no previously held view has been overturned.
The general tone of commentary on Biston studies has, however, altered. From
being treated as a vivid demonstration of natural selection (Luria, Gould & Singer,
1981, provide an excellent example) and good field experimentation (Hagen, 1999),
the work concerned has come to be viewed with suspicion (Sermonti & Catastini,
1984; Cherfas, 1987). In a recent review by Sargent et al. (1998) almost every
reference to past work is predicated by expressions of doubt, reworking ground
covered by Lambert et al. (1986). When discussing predation experiments they
conclude “. . . there seems to be no clear and consistent relationship between the
relative survivorship of different morphs . . . and the frequencies at which the morphs
naturally occur in different environments”. Coyne (1998) adopts a similar tone,
saying that the flaws in the work are too numerous to list. This has led to some
alarming reporting, such as Matthews (1999) in the Daily Telegraph newspaper in
Britain, who refers to a “series of scientific blunders” and states that the experiments
are “now thought to be worthless”. This article in turn was linked in its electronic
web version to the Creation Science home page. Recent commentaries are quoted
on more than one anti-evolution web site. A balanced account, which shows the
strength of the data in the face of recent criticism, has been provided by Grant
(1999). I propose here to illustrate the predation results, which Sargent et al. did not
do when they criticized them, and to consider why a radical change in view should
have occurred.
FITNESS AND FREQUENCY
Direct experiments on selection were carried out by placing dead animals of
different phenotypes on tree trunks and noting the numbers removed by predators,
or more rarely by releasing and recapturing live individuals. In Figure 1 fitness of
typical relative to carbonaria is plotted on typical frequency for data from Kettlewell
(1955, 1956), Clarke and Sheppard (1966), Bishop (1972), Lees and Creed (1975),
Steward (1977), Whittle et al. (1976), Bishop et al. (1978), Murray et al. (1980) and
Howlett and Majerus (1987), who each give details of their experimental procedures.
The estimates are logarithms of cross product ratios of numbers presented and
numbers remaining, with their standard errors (Manly, 1985), extending the data
illustrated by Lees (1981).
There is a general correspondence between frequency and fitness. The vertical
line at 50% typical frequency separates differing results. Typicals are at an advantage
where typical frequency is high (9 estimates to 1), and more often than not
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L. M. COOK
3.0
Fitness of typical
2.0
1.0
0.5
0.25
0.0
0.5
Frequency of typical
1.0
Figure 1. Fitness of typical compared with extreme melanic morph in the peppered moth Biston betularia
in relation to average typical phenotype frequency at the experimental site. Data from experiments
by Kettlewell (1955, 1956; Φ), Clarke and Sheppard (1966; Ε), Bishop (1972), Less and Creed (1975),
Steward (1977), Whittle et al. (1976), Bishop et al. (1978), Murray et al. (1980) and Howlett and Majerus
(1987; Β). Bars represent standard errors. In some cases typical frequencies at the same site have
been shifted slightly to avoid overlap.
disadvantageous where typical frequency is low (16 to 9). If a linear regression is
fitted, the slope is significantly greater than zero when estimates are weighted by
reciprocals of their variances (t=6.14, P<0.001), and when they are unweighted
(t=2.79, P<0.01). Clarke and Sheppard (1966) conducted some experiments in
which the light and dark moths were placed on different combinations of light and
dark parts of the trunks [Fig. 1 (Ε)]. The results show an excess of typical removed
except in one case when they placed both morphs on pale backgrounds. Howlett
and Majerus (1987) carried out pairs of tests [Fig. 1 (Β)] at two sites with different
natural frequencies, in which the moths were presented respectively on exposed
parts of the trees or in more protected positions. The difference in result between
locations on trunks is small in each case, while there is a difference between sites
not unlike that originally observed by Kettlewell [Fig. 1(Φ)].
It may be that typical is at an advantage even when natural typical frequencies
are as low as 20%, but that does not negate the evidence from the sites which
suffered intense pollution. No expected relation between fitness and frequency
dictates that the regression should be linear or the neutral point at the centre of the
frequency range. Some observations suggest that different morphs tend to rest on
surfaces they most closely resemble, other studies that they adopt random resting
places or show individual differences in preference (Grant & Howlett, 1988; Majerus,
1998; Sargent et al., 1998). Visual selection could be affected by preferential settling
behaviour, and further experimentation is required before we can say whether it is
or is not a feature of the species. However, the evidence for differential removal
CHANGING VIEWS ON MELANIC MOTHS
435
Fitness of typical
2.0
1.5
1.0
0.75
0.0
0.5
Frequency of typical
1.0
Figure 2. Relation of fitness of typical, estimated from increase in frequency over the last 25 years, to
starting frequency. Data from Mani and Majerus (1993), Grant et al. (1998) and West (1994). Curve
is maximum fitness compatible with change over time interval.
and change in morph frequency does not depend on the result. Considering the
variety of techniques used, the lack of control of predation level and the fact that
selection exerted during a trial does not estimate the amount experienced in a
generation, these experiments seem remarkably consistent.
Since Carbonaria started to decline in frequency in the 1970s records have been
made which indicate the rate of change. An invaluable set was collected by the
Clarkes in NW England, not far from Liverpool, close to rural N Wales (Clarke et
al., 1990; Grant et al., 1996). The data are continuous from 1959 to the present,
during which time melanic frequency has fallen from 93% to about 10%. The
change in frequency does not indicate constant selection with dominance of fitness
(see illustration in Grant et al., 1996). The fit is improved if one assumes some
combination of the following: change in fitness with time, change in fitness with
frequency, non-visual advantage to carbonaria homozygotes, immigrants from other
polymorphic populations which are themselves changing in frequency. Relative
fitness must have altered during the progressive decline in atmospheric pollution,
but there is insufficient evidence to dismiss any of the other possible contributory
factors or to rank them in order of importance. At a number of other sites at least
two records are available. Figure 2 shows the relation of fitness of typical to typical
frequency at the start of the decline, using data taken from Mani and Majerus,
(1993), Grant et al. (1998) and West (1994). In each case 25 generations of constant
selection have been assumed. Fitness is then estimated from the integrated difference
equation (Manly, 1985) and checked by iteration. The lower the initial typical
frequency the greater the apparent advantage of typicals. For a given elapsed time
there is a maximum detectable selection level, represented by the curve on the
graph. Within this limit, however, there is no necessary negative trend. One possible
reason why fitness should appear smaller when typical frequency is higher is that
the change has occurred in a shorter elapsed time. Where there is a series of data
points, however, the trend can be seen to be shallower where the initial frequency
of melanics is lower (see references above). The alternative explanation is that fitness
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is more sensitive to reversion where there was extreme pollution than where it was
less extreme.
In order to examine the relation of morph frequency to epiphyte status of tree
trunks, a survey was carried out along the transect from polluted Manchester to
unpolluted N Wales (Bishop et al., 1975). The fraction of the trunk at 1.5 m which
was bare bark or covered in algae, lichens or bryophytes was scored on samples of
five trees at 53 sites, and light reflectance was measured at four cardinal points on
each tree, using the methods of Lees et al. (1973). When plotted on typical frequency
at a site the change in light reflectance from the bark surface follows a pattern
similar to that in Figure 1, with lower than average reflectance levels where typicals
are 20% or less in frequency, higher than average elsewhere. At the polluted extreme
very little epiphyte was present; crustose lichens and then foliose lichens and
bryophytes became progressively more extensive and varied as one proceeded
westward toward higher frequencies of typicals. This 1973 survey was followed by
a resurvey in 1986 (Cook et al., 1990), by which time environmental improvement
was well under way. Where little epiphyte was originally present (to east of the
transect) there was an increase in area and taxonomic diversity of crustose and
foliose lichens, not so in the formerly rich western section. A non significant increase
from 14.0 to 16.2% was recorded in lichen and bryophyte cover (t=1.96, 52 df ),
but for the 29 sites where typical frequency was 20% or less at the start, there was
a significant increase from 8.5 to 11.2% (t=3.60, df=28, P<0.01). The mean
number of lichen taxa recorded in the survey went down overall (from 6.6 to 6.2,
t=0.78). At the sites with less than 20% typicals, however, it increased from 1.1 to
1.9 (t=7.1, df =28, P<0.001). Cook et al. (1990) suggested that the poor showing
at the less polluted sites may be due to greater dispersal of SO2 by the later date.
Whether or not that is so, a significant increase in extent and diversity took place
at sites which were initially the most heavily polluted.
These examples of selective removal, morph frequency change and change in
tree surface appearance demonstrate consistent patterns, despite the doubts which
have been expressed. Taking the three types of evidence together, the critical change
in environment, as it affects fitness of Biston morphs, appears to result from intense
pollution. Where that occurred carbonaria had a substantial advantage, which was
reversed with environmental amelioration. Moderate pollution had a lesser effect
on fitness, resulting in less extreme reversal and little or no change in tree surface.
As a working hypothesis, we may suggest that increase in melanic frequency was a
consequence of 19th century industrial foci of very heavy smoke and toxin deposition,
with homogenization of frequency patterns resulting from the quite high dispersal
found in the species (Bishop, 1972; Brakefield & Liebert, 1990). This suggests that
gene frequency changes (both up and down) might sometimes be seen in areas of
moderate pollution where there was little manifest evidence of the environmental
changes causing them.
HISTORICAL CONTEXT AND IMPLICATIONS
The work by Kettlewell was carried out with the support of E. B. Ford (Berry,
1990) at Oxford when it was a flourishing centre for ecological genetics. Although
the associations between the research workers were not formal (compare Cain, 1988,
CHANGING VIEWS ON MELANIC MOTHS
437
and Turner, 1985) there was certainly a common view on evolutionary problems
which included the belief that they could be investigated and solved by means of
simple field observation and experiment (e.g. see Ford, 1964; Sheppard, 1956, 1961).
The subject matter was polymorphic butterflies, tiger moths and snails, as well as
melanic moths and beetles. The intellectual antecedents went back to the pre-war
period, when predation was little regarded as a possible selective agent (H.B. Cott’s
1940 book was an attempt to change this view) and random processes were widely
thought to be responsible for much genetic change. Robson and Richards (1936)
and Diver (1939) were both influential in putting forward a non-selectionist view of
evolution. The intellectual climate can be seen in Huxley’s (1942) outline of the
eclipse of Darwinism in Evolution. The modern synthesis. The interaction between Fisher
and Ford and Sewall Wright over the importance of random drift is famous (Fisher
& Ford, 1947; Wright, 1948; Provine, 1986), but there were many other threads. It
is sometimes now implied that the principal Oxford players deliberately ignored
work by their predecessors (Owen, 1997 in the case of Biston) or suppressed
unfavourable results (Clarke et al., 1993 in the case of tiger moths). There is no
evidence for such a view, but ecological genetics did, of course, have an agenda.
The experience of those involved indicated strong and fluctuating natural selection,
which would overlay drift effects brought about by small population size. Much of
the selection appeared to arise from competition or predation. Simple experiments
could be devised which would, it was felt, show earlier assumptions about lack of
selection to be wrong. Characters rendered polymorphic by selection could then
undergo modification of phenotypic expression so as to become more stable. As
Cain and Provine (1992) put it, selectionism was enormously successful during this
time. Turner (1992) discussed the Oxford work in relation to that of R. A. Fisher
and, inevitably, of Sewall Wright, but in addition there was another important
influence.
Niko Tinbergen arrived in Oxford in 1949, having already carried out influential
experiments on animal behaviour (Hinde, 1990). By means of simple manipulation
using red-coloured markers he studied the reaction of stickleback males to females
and to rival males. In Oxford the subjects of study included breeding behaviour of
gulls. Artifacts representing beak markings of parents would elicit responses from
chicks which allowed behaviour patterns to be analysed. Simulated eggshell fragments
could be added to or removed from nests to demonstrate adaptive housekeeping
responses in breeding adults. A nest without shell fragments is less visible to predators.
This level of experimental modification of a natural situation is similar to that
used by Kettlewell in his moth predation work; the film of birds attacking moths
was actually taken by Tinbergen (Kettlewell, 1973). In The Study of Instinct (1951)
Tinbergen distinguished causation, adaptedness and evolution as aspects of a
behavioural trait which could be studied. Hinde (1990) suggests that he changed
from being primarily interested in causation to concentrating on function and
evolution. Although the experiments were similar in the ethological and the ecogenetic
studies, they addressed slightly different aspects. The shell-removal work was primarily
designed to elucidate function. The experiments were robust because the behaviour
pattern was well embedded; birds would respond vigorously and it was clear what
the behaviour was for. The response must evidently have evolved, but that process
could have taken millions of years and its experimental investigation would require
a different approach.
Shell-removing behaviour in gulls is more nearly analogous to the phenotypic
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difference itself in the Biston experiments, than to the selective removal by predators.
A gull experiment with the same aim as the Biston one would follow the response
of crows or foxes to various conditions of nests, rather than the response of parents
to eggshells. For the moths, interest lies in the evolutionary rather than the functional
aspect. Unfortunately, a predation experiment in which differential response is easily
demonstrated is likely to be over-simplistic, while if it were more realistic (inaccessible
sites, a low frequency of exposure to each potential predator and so forth) it would
be extremely difficult to conduct. Furthermore, the Oxford selectionist position was
that the experiment itself shed light on the evolutionary implications. Selection was
strong and the change in frequency inferred was evolution. Nearly all the arguments
of the 20th century to that time concerned whether or not the elementary dynamics
of gene frequency really could give a satisfactory account of evolution (or was it
necessary also to investigate macromutation, shift in genomic balance, coadaptation,
mate recognition or some other higher-order process?). The experiment was therefore
practically limited as a way of measuring natural predation, and at the same time
unsatisfying to many as a demonstration of evolution.
The same kind of problems affect field experiments on mimicry (compare
Goldschmidt, 1945 and Ford, 1964). Mimicry in butterflies was first inferred from
associations. Seemingly distasteful species are brightly coloured. Edible species which
resemble them tend to be rare and sometimes polymorphic. Different mimicry
complexes exist in different regions. When first discussed, these types of evidence
convinced some biologists (e.g. Poulton, 1890; Eltringham, 1910) that progressive
improvements occurred by small steps, while others (e.g. Punnett, 1910) felt that
small changes would not be selected and that resemblances could only arise from
parallel mutations of large effect. The experimental demonstration of poisons in
some but not in others, that similar patterns could arise by different morphogenetic
routes and observation that predation actually occurs certainly helped the mimicry
argument. More direct engagement is, however, difficult. Brower et al. (1967) carried
out an experiment in which edible moths were dressed up to look like distasteful
butterflies in order to measure the level of protection afforded. This was an example
of ecological genetics optimism springing from the Oxford environment. It was
partially successful and certainly led to deeper knowledge of the effect of field
conditions. In the end, however, the results were ambiguous (Cook et al., 1969),
possibly because control insects were inadvertently protected by resemblance to
another mimicry system (Waldbauer & Sternberg, 1975) or perhaps simply because
the predators were too wily. At root lies the problem of performing a field experiment
relevant to a process which usually takes place over geological time. Much valuable
insight may be gained but the results are not literally evidence of the evolutionary
process. That requires other types of information, of which association is still an
important component (a point also made, inter alia, by Rudge, 1999).
CONCLUSION
In industrial melanism of Biston betularia, both the original increase and recent
decline in frequency of melanics are striking examples of natural genetic change
closely related to change in the environment. They must have a selective basis. The
experiments demonstrate selective removal. There is a general correspondence of
CHANGING VIEWS ON MELANIC MOTHS
439
morph frequency and appearance of backgrounds likely to be adult resting sites.
None of this is in doubt. The evidence is, however, limited in two ways. First, nonvisual components of selection have not been investigated directly in this species.
Analysis of segregating progenies suggests pre-adult survival differences (Creed et al.,
1980) with carbonaria homozygotes having an advantage over other morphs. Nonvisual selection is certainly indicated in studies of other melanic moths (Bishop &
Cook, 1980), but we have little more idea than Leigh (1911) how it may operate.
Secondly, the experimental and observational evidence cannot on its own carry
the burden of a particular view of evolution, such as found in Oxford ecological
genetics. Smocovitis (1996) describes how the view of the Synthesis with which it
was associated came to seem ‘constricted’ to many students of evolution, and to
generate a reaction in favour of more complex models; the last three decades have
been a period of lively debate and controversy. Distrust of the evidence of industrial
melanism may sometimes arise from a wish to question how the example relates to
more complex levels of evolutionary theory. Criticism on these grounds is misplaced,
and can attract the attention of advocates of creationism who see an evolutionary
field in apparent disarray. The Biston story continues to provide an exceptional
opportunity to analyse a pattern of selection. It should be pursued, along with study
of other species with related but different responses to environmental change.
ACKNOWLEDGEMENTS
I am grateful to Bruce Grant and John Muggleton for helpful comments.
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