Industrial melanism in the moths, Diurnea fagella (Oecophoridae) and Allophyes oxyacanthae (Caradrinidae)

Comparative studies of melanism in the two cryptic moth species, Diurnea fagella (Denis & Schiffermüller) and Allophyes oxyacanthae (L.), have been carried out in southern England and south Wales. Estimates of the relative crypsis of the melanic and typical forms of both these species have been made at a number of sites and these were compared with the melanic frequencies in samples from these sites. These comparisons showed that selective prédation could be a major factor in the variation of melanic frequencies of both of these species. A consideration of the spread of melanism in these species suggests that non-visual selection may favour the melanics of D. fagella in urban areas and that non-visual selection, not closely associated with urban conditions, may be responsible for the restriction of melanics in A. oxyacanthae to Britain. The results for these two species are discussed in relation to investigations of melanism in other moth species.     

The rise and fall of the Carbonaria form of the peppered moth

The evidence for change in frequency of the melanic carbonaria morph in the peppered moth Biston betularia (L.) (Lepidoptera: Geometridae) in England and Wales is reviewed. At mid-20th century a steep cline of melanic phenotype frequency running from the north of Wales to the southern coast of England separated a region of 5% or less to west from 90% or more to northeast. By the 1980s the plateau of 90% frequency had contracted to northern England. The frequency has since continued to drop so that the maximum is now less than 50% and in most places below 10%. There have been similar declines in Europe and North America. Evidence from surveys and from two-point records shows the change to require 5% to 20% selection against the melanic. The melanic is more disadvantageous in regions where its frequency was initially high than in regions where it was low. Experiments to investigate predation by birds show a net advantage to carbonaria morphs in regions where typical frequencies were low at the time of the experiment, and a disadvantage where typical frequencies were high. This would be expected if environment and frequency were associated, and selective predation played a part in generating the association. The cryptic advantage of carbonaria was large in areas of heavy pollution where typical frequencies were 20% or less. The moth usually has a low density but is relatively highly mobile. The ability of present information to explain the patterns has been tested in simulations. They indicate a system under strong selection that has always been in a dynamic state without equilibria.     

Melanic frequencies in three species of moths in post industrial Britain

Changing patterns of morph frequency in three moth species ( Biston betularia , Odontoptera bidentata and Apocheima pilosaria ) have been investigated using data from the Rothamsted Insect Survey. All three exhibited industrial melanism during the period of high atmospheric pollution in Britain. Three historical and habitat types are compared, the old industrial north of England, rural Scotland, Wales and South-West England, and a southern English intermediate region of high human population density but generally low industrialization. Between 1974 and 1999 the carbonaria morph of B. betularia declined in frequency in the industrial region and is nearly absent from rural areas. It is the form which most closely tracks atmospheric change. It is shown that the insularia forms of B. betularia and the melanic morphs in the other two species have decreased in the industrial region, commencing later than carbonaria , but have maintained their presence and possibly reached equilibrium elsewhere. They may be non-industrial polymorphisms. B. betularia is rarer than the other species and all three species are at lower densities in industrial than in non-industrial regions. © 2002 The Linnean Society of London , Biological Journal of the Linnean Society , 2002, 75 , 475–482.     

Theoretical models of melanism in Biston betularia—a review

The various theoretical models that have been constructed to explain the spatial and temporal changes in the frequency of the melanic morph of the moth Biston betularia are reviewed. The assumptions that are made in these models are discussed. It is shown that these models do explain the gross features of the spatial and temporal distribution of melanic variety in England and Wales. The models have been fairly successful in quantitative prediction of the observed decline in the frequencies of the melanic forms by relating selective differentials to the sulphur dioxide levels. Thus these models do yield a reasonable and consistent picture of the gross pattern of changes in melanic frequencies within the limitation of the available data. The models are robust and can thus accommodate changes to the data on the biology and behaviour of the moth. It is shown that neither heterozygote advantage nor non-Darwinian mechanism need to be invoked to understand the observed evolution of melanism in B. betularia.     

Fitness of insularia morphs of the peppered moth Biston betularia

In recent years the industrial melanic carbonaria morph in the moth Biston betularia (L.) has decreased rapidly in frequency in Britain as air pollution has decreased. The intermediate melanic insularia has shown a variable response. We have estimated the fitness of insularia, compared with the other two morphs, for several data sets. As a rule its fitness lies between that of carbonaria and typical, but nearer to typical and sometimes very close to it. The intermediate position is expected if fitness relates directly to phenotype. The results suggest that insularia may continue polymorphic while carbonaria is likely to disappear. The past high frequency of insularia in South Wales may have been due to an initial increase in insularia frequency before carbonaria reached the region. Differences in dynamics of frequency change in insularia and carbonaria are evidence against induction, which has sometimes been invoked to explain the spread of melanism in this species.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 359–366.     

A decline of melanism in the peppered moth Biston betularia in The Netherlands

Melanic forms of the peppered moth Biston betularia were well established in The Netherlands by the end of the 19th century, indeed the first records of the black carbonaria form in 1867 are only about 20 years later than in England. Analysis of extensive sampling data collected by B. J. Lempke for a period of several years beginning in 1969 shows that carbonaria was at a frequency of about 60 to 70% in most of the country where epiphyte communities on trees were reduced due to the effects of air pollution. The pale typica and the three intermediate insularia forms were each at similar, low frequencies. Only in the extreme north and south-east of The Netherlands where epiphyte floras were richer was carbonaria at a lower frequency of less than 40%. Samples collected from seven localities in 1988 show that carbonaria has dramatically declined to a frequency of less than 10%. In contrast to England, the fully black form is being replaced not only by typica but also by the darkest of the insularia phenotypes. The decline in melanism coincides with a period of decreasing levels of sulphur dioxide and of increasing species diversity of lichens on trees.     

Industrial melanism in Mesopsocus unipunctatus (Müll.) (Psocoptera) in northern England

Abstract. 1. The light and melanic morphs of M.unipunctatus are described, their genetic inheritance considered, and their geographic distribution over a pollution gradient in Yorkshire is examined.
2. There is an obvious colour dimorphism. The light forms are disruptively patterned while the melanic forms are uniformly dark.
3. Genetic crosses indicate that the melanic character is inherited as a Mendelian dominant and that separate alleles, linked on the same chromosome, control the respective melanisms of the head-thorax and of the abdomen.
4. In Yorkshire, there is a decrease in the frequency of melanics from the industrial south to the rural north.     

A theoretical analysis of the morph frequency variation in the peppered moth over England and Wales

The migration-selection model for the spatial and temporal variation of morph frequencies of Biston betularia over England and Wales (Cook & Mani, 1980) has been extended to include effects due to non-visual selection. The parameters for non-visual selection were chosen from the recent determination by Mani (1980) and by Creed et al . (1980). The morph frequencies over England and Wales were obtained through computer simulation and the results were compared with data along the Manchester-Yorkshire, Central Wales-East Anglia and South Wales-London transects. Best fits to the data were obtained by using the non-visual selective values of Mani for carbonaria and modified values of Creed et al . for insularia . It is concluded that the observed polymorphism could be well explained through a balance of migration and visual and non-visual selections.     

Evolution of resting behaviour in polymorphic 'industrial melanic' moth species

The behaviour of individually marked melanic and typical forms of Allophyes oxyacanthae was followed in four successive tests in an apparatus comprising bark of three different reflectances. In samples of wild populations, melanics showed a moderate preference for dark bark, while typicals did not seem to prefer or avoid this substrate. However, in four of the eight families of known parentage tested, both melanics and typicals preferred to rest on dark bark. These four families were the progeny of dark typicals which had shown a preference for dark bark and were the families containing the darkest typicals. In A. oxyacanthae the variation in resting behaviour is not therefore closely associated with the melanic allele but may be linked to a 'dark typical' allele which, together with other loci, produces polygenic darkening of the normal phenotype. The results with A. oxyacanthae are compared with those obtained with Biston betularia and other moth species.     

Taking the Peppered Moth with a Grain of Salt

H. B. D. Kettlewell's (1955, 1956) classic field experiments on industrial melanism in polluted and unpolluted settings using the peppered moth, Biston betularia, are routinely cited as establishing that the melanic (dark) form of the moth rose in frequency downwind of industrial centers because of the cryptic advantage dark coloration provides against visual predators in soot-darkened environments. This paper critiques three common myths surrounding these investigations: (1) that Kettlewell used a model that identified crypsis as the only selective force responsible for the spread of the melanic gene, (2) that Kettlewell's field experiments alone established that selection for crypsis was the most important factor in the spread of melanic forms, and (3) that Kettlewell's investigations in an unpolluted wood near Dorset constituted a control for his earlier Birmingham studies (contra Hagen 1993, 1996). This analysis further identifies two features that distinguish manipulative experiments in evolutionary biology from experiments in other contexts. First, experiments in evolutionary biology rest on a wealth of information provided by strictly observational ecological studies; in the absence of such information experiments in evolutionary biology make no sense. Second, there is a trade-off between how much control investigators have over the conditions being studied and how informative the results of the experiment will be with regard to natural populations.     

Melanic moth frequencies in Yorkshire, an old English industrial hot spot

A survey has been carried out in Leeds, England, in the west Yorkshire industrial heartland, and in neighboring York, surrounded by agriculture, of melanic frequency in the moth species Biston betularia, Odontoptera bidentata, and Apamea crenata. All show a decline in melanics in the postindustrial environment, the first over almost the full range from nearly 100% to less that 10%, the others to smaller extents. Changes in several species over as great a magnitude and as wide an area must result from selection. The results are compared with others along a transect through northern England. The onset of response is progressively later from west to east. The rate of decline is lower at the extremes of the transect to west and east than it is in the center. We still do not have a clear picture of the causes of the changes. One major factor is likely to be selective predation, which is shown to be critically dependent on predation rate. As a consequence, differences in settling behavior between the species could account for different responses even if the species are attacked by the same predators.     

Selective bird predation on the peppered moth: the last experiment of Michael Majerus

Colour variation in the peppered moth Biston betularia was long accepted to be under strong natural selection. Melanics were believed to be fitter than pale morphs because of lower predation at daytime resting sites on dark, sooty bark. Melanics became common during the industrial revolution, but since 1970 there has been a rapid reversal, assumed to have been caused by predators selecting against melanics resting on today's less sooty bark. Recently, these classical explanations of melanism were attacked, and there has been general scepticism about birds as selective agents. Experiments and observations were accordingly carried out by Michael Majerus to address perceived weaknesses of earlier work. Unfortunately, he did not live to publish the results, which are analysed and presented here by the authors. Majerus released 4864 moths in his six-year experiment, the largest ever attempted for any similar study. There was strong differential bird predation against melanic peppered moths. Daily selection against melanics (s ≈ 0.1) was sufficient in magnitude and direction to explain the recent rapid decline of melanism in post-industrial Britain. These data provide the most direct evidence yet to implicate camouflage and bird predation as the overriding explanation for the rise and fall of melanism in moths.     

Melanic morph frequency in the peppered moth in the Manchester area

Data are presented for the Manchester area, showing the recent change in frequency of the melanic morph carbonaria of the peppered moth Biston betularia (L.). The frequency has fallen from 90% in 1983 to below 10% at present; this decline shows that the phenomenon of industrial melanism, first noted in this species in Manchester, is now almost past. Data from the Wirral peninsula, to the west of Manchester, published by C. A. Clarke and F. M. M. Clarke, show a slightly less rapid decline starting some ten years earlier from a lower maximum. Records from north-west Kent, published by B. K. West, also show a less intense decline from a lower peak several years in advance of the Manchester decline. The changes observed agree with a migration–selection model, which predicts subsidence of the plateau of high carbonaria frequency, with contraction from the edges. Selection in this model includes a non-visual fitness advantage of carbonaria homozygotes, a fitness difference associated with change in atmospheric sulphur dioxide concentration (which may act through differential crypsis) and frequency-dependent protection of rare forms. When all available data are compared, there is a negative relation between estimated fitness of carbonaria over the period of decline and initial level of atmospheric pollution.     

Allelic melanism in American and British peppered moths

Parallel evolutionary changes in the incidence of melanism are well documented in widely geographically separated subspecies of the peppered moth (Biston betularia). The British melanic phenotype (f. carbonaria) and the American melanic phenotype (f. swettaria) are indistinguishable in appearance, and previous genetic analysis has established that both are inherited as autosomal dominants. This report demonstrates through hybridizations of the subspecies and Mendelian testcrosses of melanic progeny that carbonaria and swettaria are phenotypes produced by alleles (isoalleles) at a single locus. The possibility of close linkage at two loci remains, but the simpler one-locus model cannot be rejected in the absence of contrary evidence.     

Differential winter mortality and seasonal selection in the polymorphic ladybird Adalia bipunctata (L) in the Netherlands

Seasonal selection acting on the melanic polymorphism in the two-spot ladybird Adalia bipunctata was investigated in The Netherlands. An increase in melanic frequency over the spring-summer reproductive period was quantified. The selective advantage gained by melanics averaged 9%, but significant heterogeneity occurred between populations. Adult hibernation behaviour is described. The beetles when outdoors show a highly clumped distribution both between and within trees. The distribution of the morph classes between aggregations is random. Survivorship in a hibernating cohort (initial n= 1898) on a grid of 70 lime trees near Utrecht was monitored by making three counts over the winter of 1981–1982. Intense selection favouring each melanic morph occurred during December and January. The relative fitness of non-melanics was 0.55 (melanics =1). The discovery of dead beetles in late January (about 5% of total losses) and the absence of spatially density-dependent mortality were consistent with a climatic stress rather than selective predation. The period of selection was associated with very cold temperatures averaging up to 4°C below normal and an overall mortality of nearly 75%. There was no change in morph frequency, near normal temperatures and a lower mortality from February to early April. Examination of groups of nearby trees in late January strongly suggested that similar differential mortality had occurred except on some willows. This difference was probably due to the more protected hibernation sites available on these trees. Samples of hibernating cohorts at three other sites showed no evidence of differential mortality. Laboratory experiments with hibernating beetles found no difference in survivorship or rate of weight loss between starved non-melanics and melanics in temperature regimes with and without periods of adult activity. It is concluded that the intense winter selection on the study limes is probably exceptional. Examination of changes in morph frequency through the annual cycle suggests that at some sites the selection favouring melanics during reproduction is counterbalanced by selection against melanics in late summer or early autumn. The results are discussed in relation to mathematical models of cyclical selection and to other field studies including that of Timoféeff-Ressovsky (1940), who found large decreases in melanic frequency during hibernation in Berlin.     

The understanding of industrial melanism in the peppered moth (Biston betularia) (Lepidoptera: Geometridae)

Melanic polymorphism in B. betularia has been extensively studied. Correlations between high melanic frequency and high levels of air pollution have been demonstrated. Kettlewell and others have shown that differential bird predation has an important effect on the maintenance of the polymorphism, and coefficients of visual selection have been obtained on the assumption that the moth habitually rests on tree trunks. Computer models based on these selective coefficients show that they are not sufficient accurately to explain observed melanic frequencies. Other non-visual selective factors and weak frequency-dependent selection have been invoked to improve fits. Analysis of the resting positions of moths recorded in the wild demonstrates that B. betularia does not usually rest in exposed positions on tree trunks, but rather rests on the underside of branches, on trunks in shaded positions just below major branch joints or on foliate twigs. The results of a pilot selection experiment, while agreeing qualitatively with Kettlewell's results, suggest that fitness estimates that assume trunk-resting are quantitively incorrect. The error is greatest for melanic moths in rural areas. It is suggested that visual selective coefficients based on a true assessment of the resting behaviour of the moths may considerably improve the fit between computer predictions and observed phenotype frequency distributions.     

Peppered moth revisited: analysis of recent decreases in melanic frequency and predictions for the future

In a recent review article by Mani published in 1990, it was shown that the changes in the frequency of the morph carbonaria can be explained through a migration-selection model and the model is capable of reproducing the decrease in the carbonaria frequency since the enactment of Clean Air Acts. In this paper new data both for carbonaria and for insularia up to 1990 for West Kirby in NW England and for Cambridge are presented. In the earlier review, the data for West Kirby extended to 1987 and for Cambridge to 1985. Data not previously published for the carbonaria and the insularia frequencies at sites in Northwood in Middlesex, Egham in Surrey and Ringwood in Hampshire are also presented. A migration-selection model was used to predict the change in the frequencies of the melanic morphs up to the year 2010. All the data are compared with the predictions of the model. It is encouraging that the data follow the theoretical predictions.     

Industrial melanism and peppered moths (Biston betularia (L.))

The spread of melanic forms of the peppered moth ( Biston betularia (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.     

Decline of melanism in two British moths: spatial, temporal and inter-specific variation

The decline in industrial melanism over the last quarter century constitutes an exceptional case of an evolutionary change, varying in both time and space, and between species. In Biston betularia and Odontoptera bidentata, the change in melanic frequency is closely replicated at two sites 0.5 km apart. Between seven sites 50-100 km apart, there is heterogeneity in both the speed and timing of change. At sites that were heavily industrialized, the change is faster, from an initially higher frequency, and starts later than at sites which are more rural.We propose a method for estimating systematic change during sigmoid declines in melanic frequencies. This fails to show any significant change over time in selective coefficients. It is concluded that the overall pattern of change has been driven largely by events in the most polluted and industrialized parts of the country. Although migration may contribute to the estimated selective values, natural selection is the only credible explanation for the overall decline.     

Industrial melanism in the spittlebug Philaenus spumarius (L) (Homoptera: Aphrophoridae)*

The visible polymorphism of the spittlebug, Philaenus spumarius, has been investigated in the vicinity of a smokeless fuel factory in the Cynon Valley of south Wales. The factory is a significant source of local particulate air pollution. A striking relationship exists between the combined frequencies of the eight dark (melanic) morphs and proximity to the factory. Maximum melanic phenotype frequencies of over 95“, occur in both sexes immediately adjacent to it and decline to levels normal for south Wales 1.5–6 km away, depending on direction. This relationship is largely confined to sites within the valley; samples from adjacent localities outside it have melanic frequencies within normal limits for the south Wales area. Maximum melanic phenotype frequencies in the Cynon Valley are far higher than any known from elsewhere in the species range in Europe, Asia and North America. No consistent difference is apparent in total melanic frequency between males and females at any of the sites in this study. However, marked differences exist between the sexes in the relative contributions of the eight melanic phenotypes to the overall association with the factory. For females the industrial melanism is entirely attributable to the group flanicollis + gibbus + leucocephalus (mainly leucocephalus) whereas in males both this group and the group quadnmaculatus + albomaculatus + leucopthalmus contribute to the relationship. It is suggested that this relationship is due to the selective effects of the local air pollution from the factory. The exact nature of the selection involved is as yet uncertain; it would appear to be strong since the local adaptation involved has developed in a maximum of 40 generations since the factory was opened. Finally, comparison is made with two other insects, a ladybird and a moth, in which high frequencies of melanic forms are also associated with this pollution source.