Biological Journal ofthe Linnean Soczep (1990), 39; 301-322. With 4 figures
Industrial melanism and peppered moths
(Bistom betularia (L.))
R. J. BERRY
Department of Biology, University College London, Gower Street, London WClE 6B T
The spread of melanic forms of the peppered moth (Biston betuluriu (L.)) over polluted areas of
Britain from the mid-nineteenth century onwards, has become widely known and quoted as a
classical example of microevolutionary change. Probably the most important factor in the spread
(and subsequent decline, following the Clean Air Act) of the melanics has been bird predation on
less cryptic individuals, but a range of other factors may also affect the maintenance of allele
frequencies at any one place (site selection, dispersion, heterosis, frequency dependent selection,
larval hardiness, etc). The development of the “Peppered Moth Story” is described, and suggestions
made about needed research.
KEY WORDS:
pollution.
Peppered moth
-
microevolution
natural selection
-
bird prrdation
-
air
CONTENTS
Introduction . . . . . . . . . .
Observations and interpretations . . . . .
Genetics . . . . . . . . . .
Geographical distribution . . . . . .
Natural selection, etc . . . . . . .
Behaviour.
. . . . . . . . .
. . . .
Multiple factor analysis and models
Acknowledgements
. . . . . . . .
References.
. . . . . . . . . .
Appendix A: Tutt (1896) on peppered moth melanism
Appendix B: Suggestions for further work . . .
Appendix C: History of peppered moth melanism work
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IN’I’RODUCTION
The spread of black forms (several insularia phenotypes and the more extreme
carbonaria) of the peppered moth (Biston betularia (L.)) in the mid-nineteenth
century following the widespread increase of air pollution, and their subsequent
maintenance by bird predation, has become a standard text-book example of the
operation of natural selection. Savage (1977: 84) has described its elucidation as
a series of “brilliant investigations (which) provide an exciting insight into the
operation of selection under natural conditions”; Wright (1978: 186) called it
“the clearest case in which a conspicuous evolutionary process has been actually
observed”. MacArthur & Connell (1964: 67) point out, “It used to be argued
+
0024-4066/90/040301 22 $03.00/0
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0
1990 The Linnean Society of London
302
K. J. BEKKY
that natural selection was only a conjecture, because it had not been actually
witnessed. By now we have become aware of many examples of natural selection
in action. One of the best documented cases deals with the peppered moth . . .”
The classical peppered moth work is properly associated with the work of
H. B. D. Kettlewell who collected “evidence for selective elimination through
experiments of release and recapture coupled with direct observations of bird
predators capturing selectively one or the other form. The complementary series
of experiments in contrasting habitats is especially impressive” (Spiess,
1964: xlviii). It has been a major factor in the recognition that “selection
pressures in operation on natural populations are of greater importance than
theorists such as Sewall Wright and R. A. Fisher thought them to be. Selective
advantages for alleles were calculated at the level of 0.5 to 1.0 per cent. Study of
natural selection by investigators such as J. B. S. Haldane, S. Gershenson, E. B.
Ford and H. B. D. Kettlewell indicate to the contrary that selective advantages
from 20 to 40 per cent are not uncommon” (Hamilton, 1967: 28).
Kettlewell was a general medical practitioner and keen lepidopterist. After an
extended collecting trip in central Africa, at the age of 45 he took up a fellowship
in E. B. Ford’s laboratory in the Department of Zoology at Oxford University,
where he remained until his retirement in 1974. He died in 1979 (Lees, 1979).
His Biston betularia studies were published in nine primary papers between 1955
and 1977 (Kettleworth, 1955a, 195513, 1 9 5 5 ~1956a,
~
1958, 1959, 1965a, 196513;
Kettlewell & Conn, 1977), and largely summarized in his definitive book T h e
Evolution o f Melanism, published in 1973.
Kettlewell’s work remains the core of our knowledge of industrial melanism in
general, and the peppered moth in particular, but it has been continued and
extended by a number of workers (reviewed Bishop & Cook, 1980; Lees, 1981;
Brakefield, 1987, 1988; Majerus, 1989). In most cases, these later studies have
confirmed Kettlewell’s conclusions, but in some respects, the emphasis has been
changed. I n particular, the maintenance of melanic frequencies is now perceived
to be less directly dependent on bird predation than Kettlewell believed. The
purpose of this paper is to summarize work on the peppered moth so that current
work and criticisms can be put into context, and, following a workshop
organized by L. M. Cook and G. S. Mani in November 1987, to identify gaps in
our current understanding (Appendix B).
OBSEKC‘ATIONS AND IN’I’EKPKETATIONS
The first published observation of a melanic peppered moth seems to have
been that of Edleston (1964) (although Ford, 1975, records that a carbonaria
caught from an unknown locality prior to 1811 is in the Entomology
Department collection of the University of Oxford). Writing from Manchester,
Edleston noted “Some sixteen years ago the ‘negro’ aberration of this common
species (B.betularia) was almost unknown; more recently it has been had by
several parties . . . Last year I placed some virgin females in my garden in order
to attract the males, and was not a little suprised to find that most of the visitors
were the ‘negro’ aberration: if this goes on for a few years the original type of
B. betularia will be extinct in this locality”.
Edleston’s report has led to 1848 becoming the accepted date for the start of
the rise of frequency of carbonaria in north-west England. By the 1870s the
INDCSTRIAL MELANISM AND PEPPERED M O T H S
303
amateur entomological journals contain many references to black individuals as
the melanics spread to other parts of the country (Cook, 1981). A remarkable
(for the time) account of the status and industrial dependence of peppered moth
melanism was given by T u t t (1896) (see Appendix A). In 1900, the Evolution
Committee of the Royal Society attempted to collect evidence of the history and
increase in industrial melanism, but was frustrated by the lack of firm
information. T h e data available were summarized by Doncaster (1906). He
cited Barrett (1901) that only the typical form was known “until about 1848”,
and carbonaria (then known as doubledayaria) “appeared in the Manchester district
1850, at Cannock Chase in 1878, in Berkshire in 1885, Cambridge 1892, Norfolk
1893, Suffolk 1896, London 1897”. The best review of the spread of carbonaria is
that of Steward (1977a) (Fig. 1). His conclusion is that carbonaria was widely
distributed in northern England and the Midlands by 1885, but was still absent
from a large area of southern Britain. T h e report that ‘black’ and typical forms
were equally common in Newport, Monmouth in 1870 probably refers to the less
intensely melanic form, insularia rather than carbonaria, since the former still
occurs at over 40% there. Similarly, a “dark individual” caught by Holland
(1884) near Reading in 1885 may also have been a n insutaria.
After 1890, carbonaria seems to have spread very rapidly through a large area
including East Anglia and London. For example, James (1915) found no
melanics in 77 B. betularia caught in Highgate (north London) in 1894, but had
74% carbonaria in a large sample taken in the same place in 1915. Despite the fact
that the conditions in London were apparently ripe for the spread of industrial
melanics, carbonaria did not reach I:/, there until 1895.
Many workers have commented on the lack of quantitative information
available for carbonaria*. There is even less information for the other peppered
moth melanic, insutaria. It was present in Manchester at the same time (or soon
after) carbonaria was first caught (Stephenson, 1858)) and Kettlewell (1958)
concluded that it was common in Folkestone (on the south coast of England)
before carbonaria appeared there.
The first record of carbonaria on continental Europe was in 1867 at Breda in
Holland, and it was subsequently recorded progressively at places to the east. By
the early 1900s it occurred all over north-west Europe, apart from Scandinavia.
Carbonaria was not recorded in Denmark and Sweden until the 1940s) and now
occurs at low frequencies in Denmark and Sweden; it is absent from Finland
(Mikkola, 1975, 1984b; Douwes, Petersen & Vestergren, 1976).
* I n a book which (according to Bennett, 1983) considerably influenced R. A. Fisher, Punnett (1915: 102)
pointed out “two things are ofinterest in the case ofthe peppered moth --the rapidity with which the change in
the nature of the population has taken place, and the fact that the two forms exhibit Mendelian heredity,
doubledgaria (=carbonana) being dominant and belularza (=!@a) recessive . . . This rase of the peppered moth
shows how swiftly a change may come over a species. It is not a t all improbable that the establishing of a new
variety at the expense of a n older one in a relatively short space of time is continually going on, especially in
tropical lands where the conditions appear to be more favourable to variation and where generations succeed
one another in more rapid succrssion. At present, however, we are without data . . . Much could be learned if
some common forms were chosen for investigation in which there are both mimetic and non-mimetic forms.
Large numbers should be caught at stated intervals, large enough to give trustworthy da ta as to the
proportions of the different forms that occurred in thr population. Such a censiis of a polymorphic species, if
done thoroughly and ocer a series of years at regular intervals, might be expected to give us the necessary data
for deciding whether the relative proportion of the different forms was changing whether there were definite
grounds for supposing natural selection to be at work, and if so what was the rate a t which it brought the
change about”. Three-quarters of a century later, this exhortation is still not properly assimilated (Taylor,
1989; Berry, 1989).
304
R . J. BERRY
Figure 1. Spread of carbonaria in England and Wales. Solid circles indicate first reports of carbonaria;
solid squares show sites where carbonaria was already reported as common at the date indicated; open
circles are sites where carbonaria was reported as absent. T h e dashed lines separate areas where
carbonaria was present before 1890, from where it appeared later. Based on Steward (1977a).
The North American equivalent of carbonaria is the swettaria form of Biston
cognataria (which is phenotypically indistinguishable from carbonaria). It was first
recorded in Philadelphia in 1906. It was then found in New Jersey in 1920,
Chicago 1935, and New York City only in 1948. But its spread was rapid: by
1961, it constituted over 90% of the population in parts of Michigan (Owen,
1961, 1962).
Genelics
The earliest recorded controlled cross involving peppered moth melanics was
in 1868, only three years after Mendel published his results (Orville, 1868;
Lemche, 193l ) , but arguments about environmental us. genetic determination of
melanism persisted until the turn of the century ( T u t t , 1891; Doncaster, 1906).
Nowadays, it is commonly assumed that melanism is inherited as a simple
dominant. (Harrison, 1928, 1956, claimed that melanism was the result of
directed mutation produced by the ingestion of pollutants; this assertion was
repudiated in detail by Kettlewell, 1956b, see also Thomson & Lemche, 1933;
Fisher, 1933.) In fact five alleles are known at the melanism pattern locus in the
peppered moth: t , i', i2, i3 and C. carbonaria. T h e form is produced by C, and is
INDUSTKIAL MELANISM AND PEPPERED M O T H S
305
inherited as a condition fully dominant to the other alleles. The typical form is
produced by the tt homozygote. All combinations of the i alleles with each other
and with t produce insularia phenotypes (Lees & Creed, 1977; Steward, 1977b),
although i3i3and i3t may be difficult to distinguish from carbanaria (Clarke, 1979;
Bishop & Cook, 1980).
Kettlewell argued that peppered moth melanism was a clear example of the
evolution ofdominance, as advocated by R. A. Fisher (1928). The context for his
belief was the fact that the great majority of industrial melanic forms are
inherited as dominants, implying (on Fisher’s theory) that melanism had been
selected for at some time in the past. Kettlewell suggested that a melanic
peppered moth form may have been adaptive in some previous geographical or
climatic situation, and that carbonaria attained dominance under those
conditions. Kettlewell’s interest in such non-industrial melanism led to his work
on Amathes glareosa in Shetland (Kettlewell, 1961; Kettlewell et al., 1969),
Lasiocampa quercus in Caithness, North Scotland (Kettlewell, Cadbury & Lees,
1971) and Boarmia repandata in the primaeval Black Wood of Rannoch in the
Central Highlands of Scotland (Kettlewell, 1973: 171--4).
Kettlewell’s evidence of dominance evolution in the peppered moth was based
on the presence of white markings on the wings of nineteenth century melanics
(Kettlewell, 1958) and the fact that the British C allele did not produce distinct
melanic and typical phenotypes when British moths were crossed with typical
peppered moths from Canada (where melanism was unknown); in other words,
there was a breakdown of dominance when the allele was introduced into a
genome where dominance might be expected not to have evolved (see also Ford,
1955). Just as Ford showed in his classical test of Fisher’s theory with Abraxas
grossulariata (Ford, 1937), Kettlewell found that clear carbonaria-typica expression
and segregation was restored when “broken-down” melanics (phenotypically
indistinguishable from &pica) were crossed with British &pica (Kettlewell, 1965a).
However, this evidence is not as clearcut as it may appear. West (1977)
crossed British carbonaria with &pica from the Appalachians where the melanic
had a frequency of only about 1%, and observed no breakdown in dominance.
Likewise, Mikkola (1984b) found no breakdown in crosses between carbonaria
from Liverpool and typica from Finland. Moreover, individuals like Kettlewell’s
“ancient” carbonaria are regularly found in modern samples from the Liverpool
and Birmingham areas (Lees, 1971; Bishop, Cook & Muggleton, 1978).
Notwithstanding, there is plenty of circumstantial evidence suggesting that
dominance modifiers may be acting (Haldane, 1956; Steward, 1977a); the
subject needs more study.
Geographical distribution
Kettlewell (1958, 196513) made the first extensive survey of the distribution of
any industrial melanic in Britain, compiling data supplied largely by amateur
entomologists. Later data have been collected by Lees & Creed (1975), Steward
(1977a), Bishop el al. (1978) and Cook, Mani & Varley (1986). As is wellknown, the distribution of both carbonaria and insularia show a correlation with,
and a displacement down-wind from, sources of industrial pollution. In other
words, they exhibit industrial melanism.
The broad outline of the spread and distribution of melanics has been known
R. J. BERRY
306
loo.
90 -
80 -
70 -
T
AB = I -50 years
B = Primary mutation occurs
BC = -t 29 years at 30 per cent
advantage
BD = f 38 years at 30 per cent
advantage
DE = ? I5 years Period of
rapid increase
EF = 2 1000 years Period of
slow elimination or
balanced polymorphism
60-
a,
0
B
50-
0
K
3
40-
30 -
2010IA
- -&
B
C
/.
D
E
F
Figure 2. Rate of increase of a melanic mutant, assuming a constant advantage of the heterozygote
over the typical homozygote. Based on Haldanc (1956; after Kettlewell, 1973).
for several decades. Punnett ( 1915) referred to increases in carbonaria frequencies
as evidence that natural selection may produce observable evolutionary change,
and concluded that the melanics must have some advantage over the typical
form. H e cited the experience of breeders who found that melanics were
“somewhat hardier, at any rate in captivity”.
The next step was Haldane’s (1924) use of the available data to postulate a
period of establishment of carbonaria, followed by a rapid increase in frequency,
and than an apparent equilibrium (Fig. 2). From this he calculated that in
smoke polluted areas typica and homozygous carbonaria had fitnesses relative to
the heterozygote of 0.5 and 0.92 respectively (Haldane, 1956).
Detailed studies of B. betularia melanics have subsequently been in the North
Wales to Liverpool-Manchester conurbation, and in South Wales. Following an
initial survey by Clarke & Sheppard (1966),Bishop (1972) carried out a detailed
investigation of the factors affecting frequencies over a 120 km transect, and
modelled the expected cline using estimates of movement and differential
predation he obtained himself (Fig. 3 ) . Like Haldane, he concluded that there
was apparently some heterozygous advantage.
INDUSTRIAL MELANISM AND PEPPERED M O T H S
3
307
5
.o
'6
Clegyr Mawr
Miles
% carbonaria
in samples
20 -
Distance from Sefton cbrk, Liverpool ( m i l e s )
Figure 3. Change in the frequencies of carbonaria between Liverpool and North Wales. Aboue,
Percentage carbonaria frequencies. Below, Cline, along the line drawn in the above figure. T h e heavy
line shows the observed frequencies; the lighter line the expected frequencies, based on the best
available estimates of predation, differential migration rate and heterozygous advantage. Based on
Bishop (1972).
This work led on to a series of comparisons between the factors affecting
melanic frequencies in B . betularia and Gonodontis bidentata (Askew, Cook &
Bishop, 1971; Bishop & Cook, 1975; Bishop et al., 1978): whereas carbonaria
frequencies declined smoothly westward into rural areas, the G. bidentala melanic,
nigra, does not extend into rural North Wales, and ranges in frequency from 10
to 80% with marked peaks and troughs in the area between the River Dee and
Manchester (where carbonaria is consistently over 85%). At least part of the
308
R. J . BERRY
difference must depend on different dispersal distances in the two species.
The present frequencies of carbonaria are imperfectly known, although they
have certainly declined substantially since the classical surveys were carried out.
In Britain, a Clean Air Act was finally passed in 1956; it was stimulated by post
war building, a change from coal to oil heating (Bishop & Cook, 1980), but also
a response to a smog in which prize cattle died at the (national) Smithfield Show
and opera performances at Sadlers Wells Theatre had to be cancelled because
the audience could not see the stage rather than to rational political (or
scientific) pressure (Ashby & Anderson, 1981). Cook, Askew & Bishop (1970)
published data showing that the frequency of &pica at Didsbury on the outskirts
of Manchester had increased from zero in 1952-1964 to 2.6% in 1966-1969
(whereas insularia remained constant at c. 1.3%). Clarke, Mani & Wynne (1985)
extended these data, showing that frequencies of carbonaria in Clarke’s garden in
the Wirral (c. 15 km west of Liverpool) declined increasingly rapidly from 927”
in 1959 to 61% in 1984; by 1989 the population contained only 30% (Clarke,
Clarke & Dawkins, 1990). Cook et al. (1986) reported a large scale survey
showing a pattern of decline over the country from 1952-1970 to 1983-1984
which resulted in a north-easterly movement of the steep cline which runs
obliquely from NW to SE England. Brakefield (1990) has described a similar fall
in the Netherlands.
Natural selection, etc.
Perhaps taking his cue from Punnett, (1915)*, E. B. Ford (1937) put forward
the hypothesis that industrial melanism was the result of natural selection
operating “in favour not of the colour but of the physiological advantages
possessed by those black forms which have spread” and which were eliminated
by predators before pollution made melanic colouration less of a handicap than
previously. He maintained these views in print a t least as late as 1953. Viability
differences do exist between the melanic and typical forms of some species, but
for B. betularia, Kettlewell (1973: 78c see also Robinson, 1971: 363) reviewed the
available evidence and found it “unconvincing”, (although) “until broods from
contrasting areas in Britain are bred on a large scale under stress (for example,
fed on leaves contaminated with the various types of pollution, starvation,
polyhedrosis, etc.), we shall not know whether f.carbonaria survives better than
J opica . . . (But) the rate of spread of the carbonaria form throughout polluted
Britain could be accounted for entirely by the cryptic advantage of the imago
alone”.
However, Creed, Lees & Bulmer (1980) showed significant pre-adult viability
deficiencies between genotypes involving both heterozygous insularia-carbonaria
(they did not distinguish between insularia allelles) and homozygous carbonaria in
laboratory stocks (fitness of heterozygote relative to carbonaria homozygote was
0.52; of carbonaria homozygote to insularia homozygote was 0.72). In contrast,
homozygous carbonaria had a much greater viability than &pica (1.48: 1). These
estimates were based on all the data from different sources then available, so that
effects of local stocks or rearing conditions are minimized.
Indirect estimates of viability differences from change in phenotype frequency
*Ford (1980) described Punnett as a most dedicated and vociferous selectionist, but “he did nnt carry as
much weight as he might have because he knew absolutely no genetics at all”.
INDUSTRIAL MELANISM AND PEPPERED M O T H S
309
TABLE
1. Summary of Kettlewell's original mark-release-recapture experiments
Dorsct (carbonarta frequency under 1 ' l o )
Birrninghan (carhonana frequency 87",,)
Releawd
Recaptured
Released
Recaptured
ppica
carbonaria
Jv
496
62 (12 5",)
137
18 (13.2",,)
473
30 (6 3",,)
447
123 (27.5",,)
969
92
584
141
with time, have indicated a 8- 15y0 disadvantage of carbonaria homozygotes
compared to carbonaria-typica heterozygotes (Haldane, 1956; Clarke & Sheppard,
1966). However in neither case is the possible effect of migration on the morph
frequencies considered (cf. Bishop el al., 1978). Lees & Creed (1975) suggested
on the basis of discrepancies between the results of predation experiments and
sample frequencies in East Anglia, that non-carbonaria has a physiological
disadvantage of up to 30%, and that this could explain the existence of carbonaria
in rural areas of North Wales (Bishop, 1972).
As is well known, the key observations and experiments on the importance of
visual predation on non-cryptic forms were carried out by Kettlewell (1955a,
1956a). Having shown that great tits (Parus major) in an aviary eat both melanic
and typical peppered moths, taking them in the same order of conspicuousness as
scored by a human observer, in 1953 and 1955 Kettlewell released marked
moths of both morphs in a wood near the industrial centre of Birmingham,
repeating the experiment in 1955 in a heavily lichened and pollution-free wood
in Dorset, southern England. The experiments are summarized in Table 1. In
Birmingham 28% of the marked carbonaria were recaptured, but only 13% of
&pica; whereas in Dorset 13% of the typicals were recaptured, but only 6%
carbonaria. Historically as important in convincing the scientific community of
the effectiveness of bird predation was a film made by Kettlewell in
collaboration with Niko Tinbergen. I n Dorset, five species of birds were observed
selectively to prey on the more conspicuous form.
Kettlewell's predation results have been confirmed in a t least five different
studies: by Clarke & Sheppard ( 1966) (using killed and deep-frozen specimens),
Bishop (1972), Lees & Creed (1975), Steward ( 1 9 7 7 ~ and
)
Bishop et al. (1978).
They have been criticized on the grounds that the density of prey moths in them
was far greater than under normal conditions (Lambert, Millar & Hughes, 1986;
Millar & Lambert, 1990), but there can be no doubt that "bird predators exert
a significant influence on the B. betularia polymorphism in heavily polluted areas
where the melanic frequency is very high and in completely rural areas where it
is low. At intermediate frequencies and pollution levels their effect is less clear"
(Lees, 1981).
Behauiour
A. Dispersal
The relationship between selection, giving rise to local adaptation, and
dispersal, tending to obscure it, has received much attention (Haldane, 19471948; Kettlewell & Berry, 1969; Endler, 1977). The influence of dispersal on
differences in melanic distributions between B. betularia and G. bidentata has
already been noted; mean adult flight distances are several times greater in the
former species than the latter (Bishop, 1972; Bishop et al., 1978). Individual
R . J . BERRY
310
Figure 4. Flight distances of marked peppered moths released in a park in the centre of the Wirral
Peninsula. The black circles are moth traps. Built-up areas are shaded. After Bishop (1972).
peppered moths may fly up to 5 km in a single night (Fig. 4);indeed Brakefield
(1990) indicated that even longer distances are common. Bishop et d. (1978)
concluded that the maintenance of carbonaria frequencies in the North Wales
cline (Fig. 3) can be explained entirely as a balance between migration and
visual selection, with no need to invoke heterozygous advantage (see also May,
Endler & McMurtrie, 1975).
B. Resting site selection
Consistent camouflage while resting depends, of course, on the ability of
individuals to choose backgrounds on which they are cryptic. Kettlewell (1955b)
released typical and melanic peppered moths into a large cider barrel ( 1 m high,
TABLE
2. Rrsults of offering Qpzca a n d carbonaria forms of the peppered
moth equal a r r a s of black a n d whitr surfaces, i n barrels, to rest upon
(from Kettlewell, 1955b)
gpzia
carbonaria
--
~-
~
~
~~
Total
~
Rlnrk hnc kground
\Vhire bat kground
38
21
20
39
58
60
fotal
59
59
118
INDUSTRIAL MELANISM AND PEPPERED MOTHS
311
0.7 m diameter) lined with alternate black and white vertical stripes, and found
that a significant proportion were on a matching background when scored the
following morning (Table 2). He confirmed this result in further experiments
(Kettlewell, 1973: 69, 88; Kettlewell & Conn, 1977). In contrast, Sargent (1966,
1974) failed to find such clear background choice. Kettlewell (1973: 70) argued
that Sargent’s experimental chambers were too small and crowded.
Mikkola ( 1979, 1984a) criticized the conclusions from predation experiments,
particularly those involving the placing of dead specimens on trees, on the
grounds that they were all based on the assumption that the moths rest naturally
on tree trunks. His observations on partly paint-sprayed trunks and branches in
an outdoor cage led him to believe that the normal resting place of the peppered
moth is actually on the underside of branches in the canopy. Howlett & Majerus
(1987) have confirmed this experimental conclusion on the basis of the sites
where peppered moths have been found in the wild, with most individuals found
close to a trunk/branch joint. They showed that the chance of a dead moth
disappearing was significantly greater if it was placed on a trunk rather than on
a branch.
Liebert & Brakefield (1988) have extended knowledge about the natural
behaviour of peppered moths by watching virgin females released after confining
them in a cage until initial dispersal flights was over. Pairing usually occurred
quickly, and once females paired they walked short distances and did not fly. If
their initial alighting site is close to the niche identified by Mikkola, Howlett and
Majerus, this would bring them near to epiphytic growth except in the most
polluted environments. Mated pairs remain in copulation for 20-24 hours; &pica
pairs in particular resemble foliose lichens, whilst typica and carbonaria are likely
to be at a disadvantage in most situations when compared with other
combinations.
Howlett & Majerus (1987) analysed the light reflected from the wings of
peppered moths. They showed that the wings of typica are partially translucent,
and hence are more similar to a plain black surface than a plain white one.
They inferred from this that both forms should prefer a darker surface when
offered a choice, and found this to be so experimentally (Table 3).
Finally, texture has been shown to be important in the choice of resting
position for many species which have melanic polymorphisms (Sargent, 1969;
Kettlewell, 1973; Lees, 1975).
Kettlewell ( 195813) put forward a “contrast/conflict” hypothesis of site
selection. He suggested that light stimuli from the resting substrate are compared
by alighting moths to the colour and pattern of the circumocular scales. If the
two are dissimilar, the moth moves until this contrastlconflict is reduced. Sargent
TABLE
3. T h e resting sites of the typica, iiisularia and carbonaria forms of
the peppered moth when presented with a choice of black and white
rurfaces of equal area in cylinders (after Howlett & Majcrus, 1987)
QJpzta
znmlnrza
~ _ _ _ _ ~ _ _ _ _ _ _ _ _ _ _
Black \ide
58
30
20
7
Whit? sidc
21
5
Floor
Otdl
99
4“
rarbonnrin
7 otal
70
14
158
41
36
62
120
26 I
312
R. J . BERRY
(1968) attempted to test this idea by painting the tufts of scales around the eyes
of two North American moths, Catocala actinympha and Campaea perlata, but found
no difference in their behaviour. But, as Kettlewell (1973: 72) pointed out, both
these species are monomorphic, and have had no cause to evolve differential site
choice. Grant & Howlett (1988) showed that some individual peppered moths
appear to have preferences for backgrounds of particular colours, but that these
preferences are not correlated with the moth’s phenotype.
C. Evolution of resling site choice
Sargent (1968) and Steward (1985) have argued that differential rest site
selection is inherited. This raises the problem that the selection must be either a
pleiotropic effect of the melanism locus, or the behavioural gene must be tightly
linked to the melanic-controlling one (these two alternatives are very similar in
effect). Howlett (1989) has modelled the evolution of resting site preferences in
the absence of linkage to the colour pattern locus. His results suggest that the
selection of appropriate resting sites will only evolve if there is linkage between
the colour pattern locus and the behavioural locus. The likelihood of such a
system evolving could thus be, at least in part, a function of the length of time
that the various alleles for the different forms and the different resting
preferences have existed in the population.
Majerus (1989) has pointed out that the occurrence of different frequencies of
carbonaria in populations of the peppered moth throughout Britain over the last
140 years will mean that if alleles which cause moths to rest preferentially on
dark surfaces arise by mutation, but are not linked to the carbonaria locus, some of
these will spread to fixation (in areas of high carbonaria frequency), others being
lost from populations (where typica predominates). Consequently three types of
population may be envisaged: (a) Those in which a dark preference allele has never
arisen or has failed to spread, so the peppered moths in the population all tend to
rest on pale heterogeneous backgrounds. (b) Those in which a dark preference
allele has recently arisen and is in a state of transient polymorphism as it spreads
towards fixation. In these populations some peppered moths will have a
preference to rest on pale heterogeneous backgrounds, others will prefer dark
homogeneous ones. (c) Those in which a dark preference allele has become fixed
in the population so that all the moths show a tendency to rest on dark
homogeneous surfaces.
If this is so, it is important to know from where Kettlewell obtained the moths
he used in his choice experiments. It is possible that he only used moths trapped
in Oxford which he collected nightly at that time but he also had extensive
stocks of bred material and was working at that time both in Dorset and
Birmingham, and may have used moths from any of these sources. l h e problem
of the variation in results is unresolved, but it should not be difficult to design
tests to resolve this controversy, in the light of the suggestion that the
phenomenon of rest site selection is a dynamic one.
M U L I I P L E FACTOR ANALYSIS AND MODE1.S
It is clear that melanic peppered moth frequencies are determined by much
more than differential visual predation by birds. Jones (1982) encapsulated this
in a review called “more to melanism than meets the eye”. Lees, Creed &
INDUSTRIAL MELANISM AND PEPPERED MOTHS
313
TABLE
4. Multiple regression analyses of carbonaria and insularza gene frequencies (after
Steward, 1977b)
Dependent variable (gene
frequency)
Independent variable
Smoke (J[Pgm-31)
Sulphur dioxide (J[pg m-'1)
Distance north (min)
Distance west (min)
Altitude (ft)
Rainfall (mm)
March
June
October
Temperature ("C)
Winter minimum
Spring minimum
Summer maximum
Autumn minimum
R2
First variable entered
R2 at first step
Carbonaria
Insularia
~
6.497***
0.107***
-0.105***
-
-0.036**
-
0.079*
-0.459**
0.883***
-0.223*
-0.128
-.
0.160***
-0.530***
0.607***
0.159
-
0.722
Sulphur
dioxide
0.467
0.313
Distance
north
0.107
The partial regression coefficients of the independent variables included in the
multiple regression equation are shown at the step where the next variable to be
entered would increase the coefficient of multiple determination (R') by less than l(yo.
The values of R2 at the first and final steps are given. The significance of the deviation
of the partial regression coefficient from 0, as indicated by the value of Student's 1
statistic, is shown: *P < 0.05; **P < 0.01; * * * P < 0.001.
Duckett ( 1973) used multiple regression techniques to investigate variation in
frequency in B. betularia and P.pilosaria in southern Britain in terms of the
more obvious environmental variables (eight physical, e.g. temperature, rainfall
etc; and six biotic characteristics of the surface of trees). For P.pilosaria, tree
trunk reflectance was the most important variable; for the peppered moth, the
three most important variables were bryophyte height, January temperature,
and sulphur dioxide concentration, indicating that crypsis was less important,
although lichen cover would clearly be affected by sulphur dioxide
concentration. I n contrast, Bishop et al. (1975) found tree trunk surface and
epiphyte cover to be the most important factors in north-west England and
North Wales.
A more extensive analysis of peppered moth data from 165 sites in Britain by
Steward (1977b) identified sulphur dioxide as the most important of 13 variables
included in the analysis of carbonaria frequency. In contrast insularia frequency
showed no clear associations with any of the variables (Table 4).In an analysis
of carbonaria frequency from 92 of the sites, distance west was more important
than pollution level in predicting frequency; correlation showed that this
relationship could not be accounted for by any geographical trend in pollution
concentration. Bishop et al. (1975) properly emphasized the weakness of multiple
regression analysis for identifying causal factors or distinguishing the relative
importance of visual and non-visual selection.
Mani (Cook & Mani, 1980; Mani, 1980, 1982) has extended Bishop's
314
R. J . BERRY
computer simulations to national carbonaria frequencies. H e has shown that a
balance between selection and migration is enough to explain why the areas of
rapid decrease in melanic frequencies do not coincide with urban boundaries.
However, his fit to observed values and to spread of the carbonaria allele since
1850 was improved by including constant non-visual fitness differences, albeit
different ones to those obtained by Creed, Lees & Duckett (1973) from their
laboratory breeding experiments. T h e development and problems of the model
are reviewed by Mani (1990).
ACKNOLVLEDGEMEN'IS
'The stimulus for this paper came from a workshop organized by L. M . Cook
and G. S. Mani to which all the European peppered moth workers were invited.
It was supported by the Linnean Society. I am grateful to all who have provided
information for this background paper, particularly for Appendix C.
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APPENDIX A
Tutt (1896) on peppered moth melanism
“The speckled peppered moth as it rests on trunks in our southern woods is
not at all conspicuous and looks like a . . . piece of lichen and this is its usual
appearance and manner of protecting itself. But near our large towns where
there are factories and where vast quantities of soot are day by day poured out
from countless chimneys, fouling and polluting the atmosphere with noxious
vapours and gases, this peppered moth has during the last fifty years undergone
a remarkable change. T h e white has entirely disappeared, and the wings have
become totally black. As the manufacturing centres have spread more and more,
so the ‘negro’ form of the peppered moth has spread at the same time and in the
same districts. Let us see whether we can understand how this has been brought
about! Do you live near a large town? Have you a greenhouse which you have
tried to keep clean and beautiful with white paint? If so what is the result?, the
paint is put on, all is beautifully white, but a little shower comes and the beauty
is marred for ever. But in country places . . . it is not spoilt . . . No! near large
towns, when the rain falls it brings down with it the impurities, the smoke and
dirt, hanging in the air . . . and so we find fences, trees, walls and so on getting
black with the continual deposit on them.
Now let us go back to the peppered moth. I n our woods in the south the
trunks are pale and the moth has a fair chance of escape, but put the peppered
moth with its white ground colour on a black tree trunk and what would
happen? It would . . . be very conspicuous and would fall a prey to the first bird
that spied it out. But some of these peppered moths have more black about them
than others, and you can easily understand that the blacker they are the nearer
318
K.J. BEKKY
they will be to the colour of the tree trunk, and the greater will become the
difficulty of detecting them. So it really is; the paler ones the birds eat, the darker
ones escape. But then if the parents are the darkest of their race, the children will
tend to be like them, but inasmuch as the search by birds becomes keener, only
the very blackest will be likely to escape. Year after year this has gone on, and
the selection has been carried to such an extent by nature that no real black and
white peppered moths are found in these districts but only the black kind. This
blackening we call melanism”.
APPENDIX B
Suggestions f o r future work
The Manchester workshop reviewed past work and present understanding. It
agreed that the latter was well presented by Brakefield (1987), who has clearly
showed the complexity of factors that operate on the B. betularia polymorphism;
conversely, there is no justification for the assertion of some that selection is
trivial (or even non-existent). Legitimate criticisms of published work are:
(1) Artefacts arising from experiment:
(a) excessive densities,
(b) site selection assumptions naivety,
(c) resting position (and use of dead specimens).
(2) Heterogeneity of sampling sites.
( 3 ) Over-concentration on crypsis at expense of non-visual effects.
Gaps in knowledge
(1) Effects on moths of the physical nature of their resting surface, and their
perception thereof (including possible asymmetry).
(2) Initial dispersal phase of females.
(3) Intensity and range of predation, including possibility of non-avian
predators and importance/persistence of search images.
(4)Factors affecting fitness at different stages during the life history, noting
the extended period of copulation and consequences for cry psis of disassortative
mating.
(5) Effects of ‘genetic background’ especially:
(a) possibility of repeated melanic mutations,
(b) differences between betularia and cognataria.
(6) Comprehension of niche of betularia, including
(a) other moths,
(b) nature of biological background (e.g. crypsis is strongly influenced by
the epiphytic flora including crustose and foliose lichens where they are
present; eggs are laid in foliose lichens),
(c) significance of SO,.
(7) Znsularia maintenance and selection.
(8) Effects of non-visually determined difference in fitness between morphs.
Waysforward
( 1 ) Analysis of the effect of differences within the life cycle on net fitness (cf.
INDUSTRIAL MELANISM AND PEPPERED MOTHS
319
the poor disguise of melanic Boarmia repandata when resting, but excellent crypsis
when on flight-which is often necessary because of disturbance by ants).
(2) Studies of physiology and biochemistry, particularly energetics.
( 3 ) Evaluation of niche perception by moth and predators, building on
Endler’s techniques (Endler, 1984, 1990). Collaboration between disciplines will
be particularly necessary here.
(4) Need to consider and interpret betularia as part ofwidespread occurrence of
melanism, including
(a) other lepidopteran industrial melanics,
(b) industrial melanism in other groups,
(c) non-industrial melanics in Lepidoptera, e.g. Western Scotland and
islands (q.v. Thornson’s (1980) studies of Scottish butterflies) and in ‘high
latitudes’ (North Atlantic islands, Scandinavia).
APPENDIX C
History of peppered moth melanism work
Peppered moth work went through a bottle-neck and flowering with the work
of H. B. D. Kettlewell in early 1950s. I t does not seem to be known how much
E. B. Ford suggested the details of the mark-release studies to Kettlewell, and
how much Kettlewell contributed himself. Miriam Rothschild recalls long
discussions with Ford, and her pointing out to him that melanics were not new
events in history, but that they must have repeatedly recurred in prehistoric
times (as R . A. Fisher had argued in deriving his theory of the evolution of
dominance).
Kettlewell had three successive research assistants: James Cadbury, David
Lees and David Conn, and all three were involved in some extent in the
peppered moth work (although the earlier classical work was over by the time
Cadbury began working with Kettlewell).
Kettlewell had an enormous respect for Philip Sheppard, who was working in
Oxford when he (Kettlewell) joined Ford. Sheppard was not initially interested
in B. betularia; Sheppard’s studies on the species began after his move to
Liverpool, when he teamed up with Cyril Clarke, then Reader in Medicine at
Liverpool University and a Cambridge contempory of Kettlewell. Kettlewell
visited Liverpool in 1956, and suggested to Clarke and Sheppard that sampling
peppered moths in the Liverpool conurbation would be highly rewarding.
Clarke’s sampling began in 1957.
Jim Bishop came to Liverpool for a post-doctoral year with Sheppard, having
worked on the ecology of crustacea in his native Sydney. In Liverpool, he began
by studying the isopod Sphaeroma, but soon got involved in the B. betularia work of
Clarke and Sheppard, particularly in estimating selective predation in the cline
of declining carbonaria. In 1966 he moved to Manchester and joined Laurence
Cook, who writes,
“At that time Manchester was still distinctly satanic in appearance but was
being cleaned and rebuilt. Since it was the type locality for the melanic moth it
seemed obvious that we should survey the morph frequencies in the area. O u r first
paper (Nature, 227: 1155, 1970) compared the results with earlier data of H. N.
Michaelis and showed that an increase in frequency of typicals had occurred.
320
R . J . BERRY
Subsequently, Jim returned to Liverpool; his 1972 paper in the Journal o f h i m a 1
Ecology on work carried out when he was first in Liverpool, was published after
his return there. We developed a research programme together and I managed
to get a grant to support John Muggleton to work on the survey and fitness
estimations. As part of this programme, we decided to use the Lees & Creed
method of scoring epiphytes and reflectance on trees, and we approached Mark
Seaward as a lichen specialist to provide taxonomic expertise. My first letter
from him, agreeing to join in, dates from March 1973”.
Cook’s own initiation into industrial melanism occurred “inadvertantly as an
undergraduate at University College London, when I bumped into J. B. S.
Haldane on the stairs saying that he had just come back from a very boring
afternoon at the Royal Society. I t was a discussion meeting arranged by E. B.
Ford (Proc. Roy. SOC.Lond. B, 145: 1956), where Haldane pointed out that the
change in melanic frequency in peppered moths in Manchester could be
accounted for by assuming a degree of heterozygote advantage*. Subsequently, I
put a fair amount of effort into arguing that the mobility of the insects makes
heterozygote advantage unnecessary to explain the frequencies and that it
probably does not exist.
I went to Oxford in 1957 to do research on scarlet tiger moths (Punaxia
dominula), and therefore soon got to know the three people who had been most
involved with them; Kettlewell, Sheppard and Ford. I always assumed that
Ford’s concern with the industrial melanism story arose from his preoccupation
with systems exhibiting strong selection and his awareness of the survey
published by Barrett (1901) and related work. In his 1924 paper Haldane has
also stressed the significance of the high selection pressure operating, and the
rapid change it should produce. Kettlewell’s work on industrial melanism was
supported by the Nuffield Foundation at the instigation of Ford. O n my first
meeting with Kettlewell he took me to visit some tiger moth colonies in the south
of England and then to pick up a specimen of “unpolluted” tree trunk from
Dean End Wood, Dorset, which was to be an exhibit at another Royal Society
meeting organized by Ford featuring industrial melanism. It is somewhat
ironic that as we swung around a sharp corner on the return journey I was
nearly crushed to death in the back of Kettlewell’s Plymouth by the log which
probably gave rise to the impression that this was the best location for betulariu to
be found. He knew better than that; I can remember him telling me of a bearded
gamekeeper in his youth who used to point out resting moths to him.
When I moved to Leicester I continued to keep in touch with Philip
Sheppard, who was studying the betularia cline from Liverpool to North Wales
with Sir Cyril Clarke; some of the sites are good pubs and/or fly fishing rivers
chosen by Philip. My first samples of melanic moth data were scalloped hazel
moths collected in Leicester. My first contact with Jim Bishop was also at
*Cook comments that “Ford ncvcr got on with Haldane, although Haldane did not seem to notice”. O ne of
Robert Creed’s stories about this concerned a day when Haldane was looking for Ford while on a visit to
Oxford. Very agitated, Ford sought out Robert saying “take mc homr, I do not want to talk to that man”. At
that time Robert had a Brooklands Rilry competition rar which was a w r y small open two-seater in which one
sat about four inches from the ground. When Ford had inserted himself, with hat and briefcase and Robrrt was
at the front cranking the engine, Haldane turned up, bent down and said “Ah Henry, I wanted to talk to you”
To this Ford replied from his position near the road, “I am so glad to see you, Jack. I would br delighted to
talk to you- -but we are very busy. In fact, as you see, we are so busy that we have to use a motor racing car in
order to gct about”.
INDUSTRIAL MELANISM AND PEPPERED MOTHS
32 1
Leicester, where he wrote to me through a mutual acquaintance about the
possibility of a post-doctoral year there. In the event, he went to Liverpool and
worked with Sheppard”.
G. S. Mani was a colleague of Cook’s in the Physics Department at
Manchester, who came to peppered moth studies through his interest in
modelling biological populations.
Meanwhile David Lees and Robert Creed moved from Oxford to Cardiff, and
studied melanism in a number of invertebrates, notably ladybirds and
leafhoppers. Steward was a postgraduate student of Lees at Cardiff.
Paul Brakefield was inspired by the possibilities of field studies in genetics by
reading E. B. Ford’s Ecological Genetics before going up to Oxford as an
undergraduate. H e spent some time with Lees at Cardiff, but his interest in
melanism began when he was a postgraduate student of Sheppard’s in Liverpool,
working on Maniolajurtina. He then studied melanism in Adalia ladybirds in T h e
Netherlands, and only began to take an active interest in melanic moths and
crypsis when he began collaborating in 1983/4 with Tony Liebert. Liebert was
another Clarke-Bishop protegi., and a dedicated amateur in the Kettlewell
mould.
The other group in Britain who have contributed significantly to the peppered
moth story, work in the Cambridge University Genetics Department; their
leader (M. Majerus) was inspired by E. B. Ford’s New Naturalist books. Majerus
writes:
“In 1964, for my tenth birthday, I was given a copy of Ford’s Butterjies. I
used my pocket money to buy the companion volume Moths in May 1964, and
these two books undoubtedly influenced the rest of my life. From that summer I
began to do more than make a child’s haphazard collection of butterflies and
moths. I began to run a moth trap, and to record religiously, all species taken,
forms, when I could identify them, notes on behaviour, and finally I began
trying to rear broods from pairings between different forms, following the advice
given in Ford’s books. My own experience is testament to the truth of Ford’s
contention that the basic elements of Mendelian genetics can be understood by a
child of eleven in a n afternoon and thereafter applied (although I was only ten).
I think the likely course of my career was laid down with the gift of that
book. My interest in polymorphic Lepidoptera was certainly conceived in 1964,
and has persisted now for 25 years. I read Ford’s Ecological Genetics in 1972, and
the idea of working on green versus brown lepidoptera larvae for a PhD came
from that reading and subsequent delvings into the bibliography. Although I
never met Ford or Kettlewell (I did hear both of them speak on several
occasions, but in those days I was a shy retiring youth), I think it is true to say
that Ford influenced my interest very considerably”.
Majerus’s student, Rory Howlett was an undergraduate at Oxford in the early
80s where, during his studies he carried out a n undergraduate project on the
marbled white, under Ford’s supervision.
The main non-British contributor to the peppered moth story has been Kauri
Mikkola of Helsinki. H e stayed with Kettlewell in 1978 at the latter’s home
north of Oxford, at a time when he (Mikkola) was developing his own ideas
about the resting position of B. betutaria. H e writes (personal communication)
322
R. J. B E R R Y
that he decided during the weekend “not to tell Bernard my views about the
resting background of the moth . . . when I heard the sad news about Bernard
Kettlewell’s death in the next spring, I was most happy that I did not argue with
him about the resting background”.
To end on a personal note: I took my degree from the Genetics Department at
Cambridge University. One of the courses I attended was on ecological genetics,
taught by George Owen, with R. A. Fisher (who was Head of the Department)
sitting in the front row and taking notes. Whilst the course was in progress, an
article by Bernard Kettlewell on “How industrialization can alter species” was
published in the December 1955 issue of the popular science magazine Discovery;
it was probably the first account of Kettlewell’s peppered moth work
(Kettlewell, 1955d), appearing in the same month as his original Heredity paper.
I wrote to Kettlewell, and the following summer helped him on field-work in
Aysgarth, Yorkshire (where a medical survey has found “too much” bronchitis
for a rural area, and Kettlewell had been asked to assess pollution levels as
indicated by melanic moth frequencies), the central valley of Scotland, and the
Black Wood of Rannoch in Perthshire, a classical site for “relict” melanics.
Kettlewell used to claim that I was the first field assistant he ever had.
Subsequently I worked with Kettlewell and other associates (including James
Cadbury, David Lees, Christopher Perrins, now Director of the Edward Grey
Institute for Ornithology, and Peter Harper, Professor of Medical Genetics in the
University of Wales) on geographic melanism in Amathes glareosa in Shetland and
Lasiocampa quercus in Caithness (Kettlewell & Berry, 1961; Kettlewell et al., 1969;
Kettlewell, Cadbury & Lees, 1971; Slatkin, 1973). Some years later I wrote:
“Kettlewell was an exciting person to be with, full of lore and anecdotes. He
was the best naturalist and almost the worst professional scientist I have ever
known. Writing research papers with him was traumatic; as an experienced
clinician he made rapid diagnoses, and refused to be diverted by what he
regarded as irrelevant evidence. I learned an enormous amount from Bernard
Kettlewell, and was enthused by him at a crucial time in my life when I was in
danger of becoming a closet biologist” (Berry, 1988).
I have no reason to change my judgement.