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 and non-industrial melanism in the peppered moth, Bistort betularia (L.)

Abstract. 1. Estimates of the relative crypsis of the melanic and typical morphs of B.betularia have been made at fifty-two sites in southern England and south Wales and these estimates were compared with melanic frequencies in samples from these sites.
2. The decrease from east to west in the frequency of the melanic form, carbonaria , and increase in the frequency of a second melanic form, insularia , across the southern part of England and Wales is largely independent of changes in smoke concentration, sulphur dioxide concentration or relative crypsis.
3. When all the available information on the distribution of the melanics of B.betularia is considered, sulphur dioxide concentration is correlated with the geographic variation in carbonaria frequency. This, together with evidence of the close relationship between carbonaria crypsis and sulphur dioxide levels, indicates that outside southern England and south Wales, either selective predation, or some direct selective effect of pollutants, is of major importance in determining the variation in carbonaria frequency.
4. Some features of the pattern of the spread of carbonaria in England and Wales during the last century give reasons for expecting non-industrial selective factors to be of greater importance in determining the distribution of melanics of B.betularia in southern England and south Wales than in the rest of Britain.     

The peppered moth and industrial melanism: evolution of a natural selection case study

From the outset multiple causes have been suggested for changes in melanic gene frequency in the peppered moth Biston betularia and other industrial melanic moths. These have included higher intrinsic fitness of melanic forms and selective predation for camouflage. The possible existence and origin of heterozygote advantage has been debated. From the 1950s, as a result of experimental evidence, selective predation became the favoured explanation and is undoubtedly the major factor driving the frequency change. However, modelling and monitoring of declining melanic frequencies since the 1970s indicate either that migration rates are much higher than existing direct estimates suggested or else, or in addition, non-visual selection has a role. Recent molecular work on genetics has revealed that the melanic (carbonaria) allele had a single origin in Britain, and that the locus is orthologous to a major wing patterning locus in Heliconius butterflies. New methods of analysis should supply further information on the melanic system and on migration that will complete our understanding of this important example of rapid evolution.     

Recent history of melanism in American peppered moths

Industrial melanism in peppered moths has been studied most intensively in Britain. The first melanic phenotype (effectively solid black) was recorded near Manchester in 1848. By 1895 about 98% of the specimens near Manchester were melanic, and this once rare phenotype had spread across regions of the country blackened by industrial soot. In rural, unpolluted regions, well away from industrial centers, the pale phenotype (peppered with white and black scales) remained the predominant form. During the latter half of the 20th century, following legislation designed to improve air quality, melanics began to decline in frequency and are now rare where once they had been common. Similar evolutionary changes have occurred elsewhere, but records from outside Britain are fragmentary. We have extended previous surveys of American peppered moth populations and present a composite picture of the recent decline in melanism in northern industrial states-Michigan and Pennsylvania-where melanic phenotypes decreased from more than 90% in 1959 to 6% by 2001. We contrast these changes to the near absence of melanism in a southern state-Virginia-during that same period. As in Britain, the decline in melanism in American peppered moths followed clean air legislation.     

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.     

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.     

Cryptic designs on the peppered moth

In a provocative recent book, Jonathan Wells (2000) decries what he discerns as a systematic pattern in how introductory biology textbooks "blatantly misrepresent" ten routinely cited examples offered as evidence for evolution. Each of these examples, according to Wells, is fraught with interpretive problems and, as such, textbooks that continue to use them should at the very least be accompanied by warning labels. The following essay critiques his reasoning with reference to one of these examples, the phenomenon of industrial melanism. After criticizing Wells's specific argument, the essay draws several conclusions about the nature of science lost in his account.     

Linkage map of the peppered moth,Biston betularia (Lepidoptera,Geometridae): a model of industrial melanism

We have constructed a linkage map for the peppered moth (Biston betularia), the classical ecological genetics model of industrial melanism, aimed both at localizing the network of loci controlling melanism and making inferences about chromosome dynamics. The linkage map, which is based primarily on amplified fragment length polymorphisms (AFLPs) and genes, consists of 31 linkage groups (LGs; consistent with the karyotype). Comparison with the evolutionarily distant Bombyx mori suggests that the gene content of chromosomes is highly conserved. Gene order is conserved on the autosomes, but noticeably less so on the Z chromosome, as confirmed by physical mapping using bacterial artificial chromosome fluorescence in situ hybridization (BAC-FISH). Synteny mapping identified three pairs of B. betularia LGs (11/29, 23/30 and 24/31) as being orthologous to three B. mori chromosomes (11, 23 and 24, respectively). A similar finding in an outgroup moth (Plutella xylostella) indicates that the B. mori karyotype (n=28) is a phylogenetically derived state resulting from three chromosome fusions. As with other Lepidoptera, the B. betularia W chromosome consists largely of repetitive sequence, but exceptionally we found a W homolog of a Z-linked gene (laminin A), possibly resulting from ectopic recombination between the sex chromosomes. The B. betularia linkage map, featuring the network of known melanization genes, serves as a resource for melanism research in Lepidoptera. Moreover, its close resemblance to the ancestral lepidopteran karyotype (n=31) makes it a useful reference point for reconstructing chromosome dynamic events and ancestral genome architectures. Our study highlights the unusual evolutionary stability of lepidopteran autosomes; in contrast, higher rates of intrachromosomal rearrangements support a special role of the Z chromosome in adaptive evolution and speciation.     

Evolution in reverse: clean air and the peppered moth

Between 1848 and 1895 the melanic form f carbonaria of the peppered moth increased in Manchester from 0 to 98%. The reverse process is now occurring in one locality in Memyside where a year-to-year survey has shown that the pale form f. typica has increased from 6 to 30% between 1959 and 1984. Supporting information also comes from two studies in N Wales. The Clean Air Acts and the consequent decline in air pollution levels are probably responsible but there are many ill–understood problems, not the least being how, and the extent to which, non-visual selection operates.     

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.     

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.     

A bird’s eye view of the peppered moth

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.     

Gypsy moth parasitoids in the declining outbreak in Lithuania

A 3 year study was conducted on the parasitoids of gypsy moth larvae in two reducing outbreak areas in Lithuania. Overall parasitism of 25.0 ± 2.0% in the first post-culmination year was significantly lower than the 36.3 ± 1.4 and 35.2 ± 1.4% parasitism in the two subsequent years. When analysed in terms of the life stage at which the host was collected, the total parasitism over 3 years was constantly increasing from 3.1 ± 0.8 in the first to 72.5 ± 2.9% in the sixth instar. Parasetigena silvestris R.-D. dominated causing 48.7 ± 1.5% parasitism and 16.7 ± 0.6% larval mortality preferably in late instars. Phobocampe disparis Vier. contributed to 21.9 ± 1.2% parasitism and 7.5 ± 0.5% mortality recovering from early instar larvae. Meteorus pulchricornis Wes. parasitized 4.3 ± 0.6% gypsy moth larvae causing 1.5 ± 0.2% mortality and a few Apanteles species provided 2.8 ± 0.6% parasitism and 1.0 ± 0.2% mortality. The gypsy moth in Lithuania was reported to act as host for Rogas sp. (Hym., Braconidae) and Siphona boreata Mes. (Dipt., Tachinidae).     

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.     

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.     

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.     

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.     

A reversible color polyphenism in American peppered moth (Biston betularia cognataria) caterpillars

Insect body color polyphenisms enhance survival by producing crypsis in diverse backgrounds. While color polyphenisms are often indirectly induced by temperature, rearing density, or diet, insects can benefit from immediate crypsis if they evolve polyphenisms directly induced by exposure to the background color, hence immediately deriving protection from predation. Here, we examine such a directly induced color polyphenism in caterpillars of the geometrid peppered moth (Biston betularia). This larval color polyphenism is unrelated to the genetic polymorphism for melanic phenotypes in adult moths. B. betularia caterpillars are generalist feeders and develop body colors that closely match the brown or green twigs of their host plant. We expand on previous studies examining the proximal cues that stimulate color development. Under controlled rearing conditions, we manipulated diets and background reflectance, using both natural and artificial twigs, and show that visual experience has a much stronger effect than does diet in promoting precise color matching. Their induced body color was not a simple response to reflectance or light intensity but instead specifically matched the wavelength of light to which they were exposed. We also show that the potential to change color is retained until the final (sixth) larval instar. Given their broad host range, this directly induced color polyphenism likely provides the caterpillars with strong protection from bird predation.     

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.     

Evolutionary dynamics in structured populations

Evolutionary dynamics shape the living world around us. At the centre of every evolutionary process is a population of reproducing individuals. The structure of that population affects evolutionary dynamics. The individuals can be molecules, cells, viruses, multicellular organisms or humans. Whenever the fitness of individuals depends on the relative abundance of phenotypes in the population, we are in the realm of evolutionary game theory. Evolutionary game theory is a general approach that can describe the competition of species in an ecosystem, the interaction between hosts and parasites, between viruses and cells, and also the spread of ideas and behaviours in the human population. In this perspective, we review the recent advances in evolutionary game dynamics with a particular emphasis on stochastic approaches in finite sized and structured populations. We give simple, fundamental laws that determine how natural selection chooses between competing strategies. We study the well-mixed population, evolutionary graph theory, games in phenotype space and evolutionary set theory. We apply these results to the evolution of cooperation. The mechanism that leads to the evolution of cooperation in these settings could be called ‘spatial selection’: cooperators prevail against defectors by clustering in physical or other spaces.