Peppered Moth Research Articles

A bird’s eye view of the peppered moth

Abstract Industrial melanism in Biston betularia is one of the best known examples of the role of natural selection in evolution and has received considerable scrutiny for many years. The rise in frequency of the dark form of the moth (carbonaria) and a decrease in the pale form (typica) was the result of differential predation by birds, the melanic form being more cyptic than typica in industrial areas where the tree bark was darkened by air pollution. One important aspect of early work evaluating the relative crypsis of the forms of B. betularia on tree trunks with different lichen flora was the reliance on human observers. Humans, however, do not have the same visual capabilities as birds. Birds have well-developed ultraviolet (UV) vision, an important component of their colour processing system that affects many aspects of behaviour, including prey detection. We examined the UV characteristics of the two forms of B. betularia and a number of foliose and crustose lichens. In human visible light the speckled form typica appeared cyptic when seen against a background of foliose lichen, whereas the dark form carbonaria was conspicuous. Under UV light the situation was reversed. The foliose lichens absorbed UV and appeared dark as did carbonaria. Typica, however, reflected UV and was conspicuous. Against crustose lichens, typica was less visible than carbonaria in both visible and UV light. These findings are considered in relation to the distribution and recolonization of trees by lichens and the resting behaviour of B. betularia.

Changing views on melanic moths

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.

Fine Tuning the Peppered Moth Paradigm

Fine Tuning the Peppered Moth Paradigm

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 19...

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.

Retelling Experiments: H.B.D. Kettlewell's Studies of Industrial Melanism in Peppered Moths

H. B. D. Kettlewell's field experiments on industrial melanism in the peppered moth, Biston betularia, have become the best known demonstration of natural selection in action. I argue that textbook accounts routinely portray this research as an example of controlled experimentation, even though this is historically misleading. I examine how idealized accounts of Kettlewell's research have been used by professional biologists and biology teachers. I also respond to some criticisms of David Rudge to my earlier discussions of this case study, and I question Rudge's claims about the importance of purely observational studies for the eventual acceptance and popularization of Kettlewell's explanation for the evolution of industrial melanism.

A Bayesian Analysis of Strategies in Evolutionary Biology

Most work done in philosophy of experiment has focused on experiments taken from the domain of physics. The present essay tests whether Allan Franklin’s (1984, 1986, 1989, 1990) philosophy of experiment developed in the context of high energy physics can be extended to include examples from evolutionary biology, such as H. B. D. Kettlewell’s (1935, 1956, 1958) famous studies of industrial melanism in the peppered moth, Biston betularia. The analysis demonstrates that many of the techniques used by evolutionary biologists exemplify the strategies Franklin lists, and identifies an additional strategy that can likewise be justified by appeal to Bayes’s Theorem.

Thirty-Five Years of Thyme: A Tale of Two Polymorphisms

Genetic polymorphisms that have readily discernible effects on phenotype provide model systems for the study of the evolutionary dynamics of natural populations. Some of the best examples of such polymorphisms, such as shell color and banding pattern in Cepaea nemoralis (Jones et al. 1977), industrial melanism in Biston betularia (Kettlewell 1973), mimetism in swallowtail butterflies (Turner 1977), and heterostyly in plants (Barrett 1992), illustrate the general importance of polymorphic variation. A consistent theme in studies of genetic polymorphism is that variations in the abundance of different morphs are common. Examinations of the basis of such variations have produced much information on the relative

Geographic and temporal variation in the incidence of melanism in peppered moth populations in America and Britain

Industrial melanism in the peppered moth (Biston betularia is the classic example of observable evolution by natural selection. The phenomenon has been most thoroughly documented in Britain, where once rare melanic phenotypes increased in frequency in concert with increased levels of atmospheric pollution generated by industrial development. Populations of the American subspecies of the peppered moth (B. betularia cognataria) also experienced increases in melanisms, which are especially well documented in southern Michigan. Following a succession of governmental regulations designed to improve air quality, melanic phenotypes have been on the decline in moth populations in the United Kingdom and the United States. In both countries, the declines in melanism appear to be correlated primarily with reductions in atmospheric sulfur dioxide. Detailed studies of the evolutionary parallels have focused mainly on two locations: Caldy Common (near Liverpool) in England, and the George Reserve (near Detroit) in the United States. We have expanded the geographic range of American samples to include northeastern Pennsylvania and southwestern Virginia, and we have conducted a national survey in Britain to produce a current melanic frequency distribution map. The results clearly show that the decline in melanism is widespread in both countries, and the changes are generally consistent with decreases in levels of atmospheric SO2.

Parallel Rise and Fall of Melanic Peppered Moths in America and Britain

The moth (Biston betularia) is well known for the rapid rise in the frequency of alleles producing melanic phenotypes correlated with a general blackening of the environment following the nineteenth-century industrial revolution. In recent years the frequency of melanics has been dropping steadily in Britain in apparent response to improved air quality. Some regional American populations of this same species also experienced significant increases in melanics, by 1959 exceeding 90% in southeastern Michigan, but Michigan populations were not reexamined for over 30 years. In 1994 and 1995 we trapped moths in southeastern Michigan and here report that a parallel decline in melanism has occurred in American moths. Furthermore, we document that changes in Michigan's air quality as measured by atmospheric sulfur dioxide (SO2) and suspended particulates also parallel the changes recorded in Britain. The traditional interpretation is that pale phenotypes of moths at rest by day on lichen-encrus ted trees are camouflaged from bird predators; industrial fallout kills lichens and darkens resting surfaces, favoring darker colored moths. However, the changes in allele frequencies in the moth populations we sampled have occurred in the absence of perceptible changes in the local lichen floras. We suggest that the role of lichens has been inappropriately emphasized in chronicles about the evolution of melanism in moths. Industrial melanism in the Lepidoptera ranks among the best examples of observable evolution by natural selection. The most thoroughly documented case is that of the geometrid moth Biston betularia, with the fundamental details of its recent evolutionary history described in virtually every biology textbook. Its common name, peppered moth, describes the appearance of the so-called form or phenotype which is covered with white scales peppered with black over the wings and body. Several other pigmentation phenotypes are known. A melanic form, named carbonaria, is nearly solid black. Intermediates between the pale and fully melanic phenotypes are called insularia. The range in variation from lightest to darkest is continuous, but the phenotypic differences result from multiple alleles at a single locus which exhibit an approximate dominance hierarchy: the carbonaria allele shows complete dominance over the insularia and typical alleles, and

Using Different Examples of Natural Selection When Teaching Biology

There are usually only two or three examples of natural selection for my high school biology students to read about in their textbooks. Despite the fact that this phenomenon is responsible for the existence of virtually all morphological, physiological and many behavioral characteristics of living organisms, authors feel limited to discussions of a few classic examples: Darwin's finches, the peppered moth (Biston betularia) and antibiotic/pesticide resistance. Fortunately, there are numerous alternative examples we can choose to address this crucial topic (Endler 1986). I have brought other examples of natural selection to the attention of my classes. These have been used to explain not only the existence and impact of natural selection, but also the methods by which the information came to light-the people, hypotheses and research techniques that contributed to the discovery of how natural selection operates. Teachers can use this technique with virtually any topic they teach by using original articles and helping students understand how the information was pieced together. The study of natural selection is a particularly rewarding area to delve into when giving examples of how research is done since it tends to quench a powerful thirst my students have for proof that this process really exists and can be readily observed to be occurring, not simply inferred from the fossil record and the large number of existing species. In addition, the studies involve populations and their dynamics, topics that generally attract my students' attention. Finally, these examples may be pre-

Let's Not Throw the Baby Out with the Bathwater: A Comment on Management for MHC Diversity in Captive Populations

Genetic management of captive populations focuses on the design of breeding programs that minimize loss of genetic diversity (Rails & Ballou 1986). Because severe spatial and economic constraints limit the population sizes that can be maintained in most breeding programs, we agree with Hughes' (1991) assertion that breeding plans which focus strictly on the maintenance of heterozygosity will, nevertheless, lose a substantial proportion of the rare alleles (see also Allendorf 1986; Fuerst & Maruyama 1986; Nei et al. 1975). However, we disagree strongly with Hughes' assumption that most loci loss of diversity should not be a cause for concern, because the of genetic polymorphisms are selectively neutral. Based on this questionable assumption, Hughes proposes that we should breed individuals in captive populations to maintain allelic diversity for the subset of genes that is known to be under balancing selection, e.g., the major histocompatibility complex (MHC) of vertebrates. We do not dispute the role that MHC diversity plays in the ability of vertebrates to respond to a broad variety of infectious agents; however, Hughes' willingness to discount the role of diversity at the vast majority of other loci is comparable to throwing the baby out with the bathwater. Hughes' assertion that most polymorphism is neutral is questionable. For example, 15 years of genetic surveys and debates have not resulted in a consensus on the adaptive significance versus neutrality of allozyme polymorphisms (Kimura 1983; Lewontin 1974). Yet, careful physiological studies have revealed substantial evidence for an adaptive role of several biochemical polymorphisms, such as aminopeptidase-I in the mussel Mytilus edulis (Koehn et al. 1983), and several enzymes in Drosophila (Zera et al. 1985). Furthermore, while the adaptive significance of many allozyme variants may be unknown, there are other types of genetic polymorphisms which appear to have fitness consequences. For example, many visible polymorphisms, such as melanism in the moth Biston betularia and color spot intensity in the guppy Poecilia reticulata, are known to have strong effects on fitness (Endler 1980; Kettlewell 1973). A comprehensive review of evidence for adaptive polymorphisms in nature is provided by Endler (1986). Apparently Hughes also discounts variation in continuous traits, such as fecundity, growth rate, and foraging behavior. Though it is difficult to determine the adaptive value of quantitative variation at any point in time, most evolutionary biologists agree that such variation provides the basis for rapid responses to physical and biotic challenges (Fisher 1930). Thus, we do not see the immediate health of captive populations as the only issue at stake in captive breeding. Maintaining evolution-

Genetic manipulation for the control of Lymantria dispar

Gene manipulation on the Goldschmidt theory is not likely to be successful in the control of the gypsy moth, Lymantria dispar (L.), because the great excess of males described by Goldschmidt in a particular race cross is not due to sex reversal but to the Haldane effect, and the males in this cross are fully fertile. Genetic engineering holds out most promise for suppression of the moth using a spray containing the baculovirus Autografia califnica ‘engineered’ to contain a hormone gene which causes the pest caterpillar to stop eating. The virus can also be ‘engineered’ to be specific for L. dispar and to destroy itself after it has been used. There are marked racial differences in L. dispar but we have not encountered phenotypic polymorphism such as occurs in Biston betularia L. An advantage could be taken of lack of polymorphism by decreasing atmospheric pollution so as to lighten the bark colour of trees and to render the male gypsy moths on the barks of the trees more visible to predators. In the genus Orgyia, the Japanese female O. thyellina attracts male O. antiqua better than does the female O. antiqua. The relevance of this finding to an improved ‘disparlure’ against L. dispar is discussed.

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.

The reliability of estimates of migration in the peppered moth Biston betularia and some implications for selection-migration models

Migration of adult males is one of the important variables involved in the mathematical models of industrial melanism in Biston betularia. Values for this variable are based on data from a capture-recapture performed by Bishop (1972) using both local and bred moths which were at least one night old at release. We carried out an experiment to compare the rate of recapture close to the point of release for moths allowed to fly away immediately after their emergence around dusk and those which were at least one night old at release. Unheld moths were less likely to be recaptured suggesting that males have an initial dispersal phase on their first night which results in a higher rate of emigration than on subsequent nights. Such a phase would have been largely missed in Bishop's experiment. The implications of this type of behaviour pattern for the models of spatial variation based on a selection-migration balance are discussed.

Biston betularia (the peppered moth) in West Kirby, Wirral, 1959-1989: updating the decline in f. carbonaria

Since 1985 the fall in carbonaria has continued and in 1989 it reached 29.6%. It is surmised that carbonaria will be down to mutant values by about the year 2010.

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.

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.

Background selection by the peppered moth (Biston betularia Linn.): individual differences

The hypothesis that dimorphically coloured, cryptic moths select appropriate rest sites by comparing their body scales to substrate reflectance was tested using typical and melanic morphs of the peppered moth, Biston betularia (L.). Experiments designed to block the individual's inspection of its inherited colour phenotype do not support Kettlewell's contrast/conflict (self-inspection) hypothesis. Instead, tracking of marked moths over successive days revealed individual differences in rest-site selection which were not related to treatments, experience (imprinting), nor closely to a moth's inherited colour pattern. Differences between family broods indicate that some genetic bias in background selection exists. The production of artificially selected lines with consistent but opposing preferences will allow us to investigate the co-evolution of pattern and behaviour.

Behavioural studies on the peppered moth Biston betularia and a discussion of the role of pollution and lichens in industrial melanism

We examined the resting behaviour during pairing and egg-laying of bred female Biston betularia (L.) after they were set free at wooded sites in Somerset and Cardiff. Moths were not released immediately on emergence but were held for three nights to overcome an initial period of flight activity. Females (N= 257) were placed on trunks, and on large and small branches of trees, especially oaks, over periods of several weeks in 1984, 1985 and 1986. Releases were not made within 50 m of any known survivor. One hundred and thirty-one pairings were observed. We also examined oviposition behaviour in a cage experiment using different types of branches. Our observations support Mikkola's earlier conclusion from cage experiments with male moths that the species rests predominantly on branches and shows an appropriately specialized resting attitude, demonstrated here in a series of photographs. Many moths will rest underneath, or on the side of, narrow branches in the canopy. Once released females had settled and paired they only moved quite short distances, but positioning and egg-laying were profoundly influenced by the presence of foliose lichens. Females of all phenotypes show a strong preference to oviposit beneath a thallus of foliose lichens. Their tendency to rest against or close to the lichen during the day could markedly influence their crypsis. In the absence of foliose lichens, eggs are laid in cracks in the bark. The survivorship of released females both in different pairing combinations and during their whole reproductive life-span is analysed. These preliminary data suggest that bird predation can give rise to differential mortality of different pairing combinations and of the phenotypes. This technique provides a powerful method of measuring the relative crypsis and differential mortality of phenotypes with living females in natural resting sites. The significance of our observations on resting behaviour is discussed with regard to the role of air pollution and epiphytes in industrial melanism. Particular attention is given to the causal mechanisms underlying recent declines in the frequency of carbonaria melanics in parts of Britain. One important factor is the new growth made by trees since the marked reduction in particulate air pollution in the 1960s. It is emphasized that we need to know much more about the interactions between pollution, epiphytes and resting backgrounds, especially in the canopy, before we can be confident of our understanding of the evolution of industrial melanism.