Peppered moth evolution

The evolution of the peppered moth is an evolutionary instance of directional colour change in the moth population as a consequence of air pollution during the Industrial Revolution in England in the 19th century. The frequency of dark-coloured moths increased at that time, an example of industrial melanism. Later, when pollution was reduced in response to clean air legislation, the light-coloured form again predominated. Industrial melanism in the peppered moth was an early test of Charles Darwin's natural selection in action, and it remains a classic example in the teaching of evolution. In 1978, Sewall Wright described it as "the clearest case in which a conspicuous evolutionary process has actually been observed."

The dark-coloured or melanic form of the peppered moth (var. carbonaria) was rare, though a specimen had been collected by 1811. After field collection in 1848 from Manchester, an industrial city in England, the frequency of the variety was found to have increased drastically. By the end of the 19th century it almost completely outnumbered the original light-coloured type (var. typica), with a record of 98% in 1895. The evolutionary importance of the moth was only speculated upon during Darwin's lifetime. It was 14 years after Darwin's death, in 1896, that J. W. Tutt presented it as a case of natural selection. Because of this, the idea spread widely, and more people came to believe in Darwin's theory.

Bernard Kettlewell was the first to investigate the evolutionary mechanism behind peppered moth adaptation, between 1953 and 1956. He found that a light-coloured body was an effective camouflage in a clean environment, such as in rural Dorset, while the dark colour was beneficial in a polluted environment like industrial Birmingham. This selective survival was due to birds, which easily caught dark moths on clean trees and white moths on trees darkened with soot. The story, supported by Kettlewell's experiment, became the canonical example of Darwinian evolution and evidence for natural selection used in standard textbooks.

However, failure to replicate the experiment and Theodore David Sargent's criticism of Kettlewell's methods in the late 1960s led to general skepticism. When Judith Hooper's Of Moths and Men was published in 2002, Kettlewell's story was more sternly attacked, and accused of fraud. The criticism became a major argument for creationists. Michael Majerus was the principal defender of Kettlewell's original experiment. His seven-year experiment beginning in 2001, the most elaborate of its kind in population biology, the results of which were published posthumously in 2012, vindicated Kettlewell's work in great detail. This restored peppered moth evolution as "the most direct evidence [of evolution]", and "one of the clearest and most easily understood examples of Darwinian evolution in action".

Origin and evolution

Before the Industrial Revolution, the black form of the peppered moth was rare. The first black specimen (of unknown origin) was collected before 1811, and kept in the University of Oxford. The first live specimen was caught by R. S. Edleston in Manchester, England in 1848, but he reported this only 16 years later in 1864, in The Entomologist. Edleston notes that by 1864 it was the more common type of moth in his garden in Manchester. The light-bodied moths were able to blend in with the light-coloured lichens and tree bark, and the less common black moths were more likely to be eaten by birds. As a result of the common light-coloured lichens and English trees, therefore, the light-coloured moths were much more effective at hiding from predators, and the frequency of the dark allele was very low, at about 0.01%.

During the early decades of the Industrial Revolution in England, the countryside between London and Manchester became blanketed with soot from the new coal-burning factories. Many of the light-bodied lichens died from sulphur dioxide emissions, and the trees became darkened. This led to an increase in bird predation for light-coloured moths, as they no longer blended in as well in their polluted ecosystem: indeed, their bodies now dramatically contrasted with the colour of the bark. Dark-coloured moths, on the other hand, were camouflaged very well by the blackened trees.Miller, Ken (1999). The Peppered Moth: An Update The population of dark-coloured moth rapidly increased. By the mid-19th century, the number of dark-coloured moths had risen noticeably, and by 1895, the percentage of dark-coloured moths in Manchester was reported at 98%, a dramatic change (of almost 100 times) from the original frequency. This effect of industrialization in body colour led to the coining of the term "industrial melanism".

The implication that industrial melanism could be evidence supporting Charles Darwin's theory of natural selection was noticed during his lifetime. Albert Brydges Farn (1841–1921), a British entomologist, wrote to Darwin on 18 November 1878 to discuss his observation of colour variations in the Annulet moth (then Gnophos obscurata, now Charissa obscurata). He noted the existence of dark moths in peat in the New Forest, brown moths on clay and red soil in Herefordshire, and white moths on chalk cliffs in Lewes, and suggested that this variation was an example of "survival of the fittest". He told Darwin that he had found dark moths on a chalk slope where the foliage had been blackened by smoke from lime kilns, and he had also heard that white moths had become less common at Lewes after lime kilns had been in operation for a few years. Darwin does not seem to have responded to this information, possibly because he thought natural selection would be a much slower process. A scientific explanation of moth coloration was only published in 1896, 14 years after Darwin's death, when J. W. Tutt explicitly linked peppered moth melanism to natural selection.

Rise and fall of phenotype frequency

Melanism has been observed in both European and North American peppered moth populations. Information about the rise in frequency is scarce. Much more is known about the subsequent fall in phenotype frequency, as it has been measured by lepidopterists using moth traps.

Steward compiled data for the first recordings of the peppered moth by locality, and deduced that the carbonaria morph was the result of a single mutation that subsequently spread. By 1895, it had reached a reported frequency of 98% in Manchester.

From around 1962 to the present, the phenotype frequency of carbonaria has steadily fallen in line with cleaner air around industrial cities. Its decline has been measured more accurately than its rise, through more rigorous scientific studies. Notably, Kettlewell conducted a national survey in 1956, Bruce Grant conducted a similar one in early 1996, and L.M. Cook in 2003.

Similar results were found in North America. Melanic forms have not been found in Japan. It is believed that this is because peppered moths in Japan do not inhabit industrialised regions.

Genetics

Tutt was the first to propose the "differential bird predation hypothesis" in 1896, as a mechanism of natural selection. The melanic morphs were better camouflaged against the bark of trees without foliose lichen, whereas the typica morphs were better camouflaged against trees with lichens. As a result, birds would find and eat those morphs that were not camouflaged with increased frequency.

In 1924, J.B.S. Haldane calculated, using a simple general selection model, the selective advantage necessary for the recorded natural evolution of peppered moths, based on the assumption that in 1848 the frequency of dark-coloured moths was 2%, and by 1895 it was 95%. The dark-coloured, or melanic, form would have had to be 50% more fit than the typical, light-coloured form. Even taking into consideration possible errors in the model, this reasonably excluded the stochastic process of genetic drift, because the changes were too fast.Haldane, J.B.S. (1924). A Mathematical Theory of Natural and Artificial Selection. Haldane's statistical analysis of selection for the melanic variant in peppered moths became a well known part of his effort to demonstrate that mathematical models that combined natural selection with Mendelian genetics could explain evolution – an effort that played a key role in the foundation of the discipline of population genetics, and the beginnings of the modern synthesis of evolutionary theory with genetics.

The peppered moth Biston betularia is also a model of parallel evolution in the incidence of melanism in the British form (f. carbonaria) and the American form (f. swettaria) as they are indistinguishable in appearance. Genetic analysis indicates that both phenotypes are inherited as autosomal dominants. Cross hybridizations indicate that the phenotypes are produced by alleles at a single locus.

The gene for carbonaria in B. betularia was thought to be in a region of chromosome 17. It was later concluded that the gene could not be in that region, because none of the genes in the chromosome coded for either wing pattern or melanisation. The region that was used to find it was the first intron of the orthologue of the cortex gene in Drosophila. Through elimination of candidates within the region based on rarity, a 21,925 base pair insert remained. The insert, labelled carb-TE, is a class II transposable element that has an approximately 9-kb non-repetitive sequence tandemly repeated two and one third times. There are 6 base pairs of inverted repeats and duplicated 4 base pairs at the target site not present in typica moths. Carb-TE has higher expression during the stage of rapid wing disc morphogenesis. The mechanism of how the gene increases expression, and whether it is the only gene involved, is still not known.

Alternative hypotheses

Several alternative hypotheses to natural selection as the driving force of evolution were proposed during the 1920s and 1930s. Random mutation, migration, and genetic drift were also seen as major forces of evolution.

P. A. Riley proposed an additional selective factor, where heavy metal chelation by melanin would supposedly protect peppered moths against the toxic effects of heavy metals associated with industrialisation. This selective advantage would supplement the major selective mechanism of differential bird predation.

Phenotypic induction

In 1920, John William Heslop-Harrison rejected Tutt's differential bird predation hypothesis, on the basis that he did not believe that birds ate moths. Instead he proposed that pollutants could cause changes to the soma and germ plasm of the organism. In 1925, K. Hasebroek made an early attempt to prove this hypothesis, exposing pupae to pollutant gases, namely hydrogen sulfide (H2S), ammonia (NH3), and "pyredin". He used eight species in his studies, four of which were species of butterfly that did not exhibit melanism.

In 1926 and 1928, Heslop-Harrison suggested that the increase of melanic moths in industrialised regions was due to "mutation pressure", not to selection by predators which he regarded as negligible. Salts of lead and manganese were present in the airborne pollutant particles, and he suggested that these caused the mutation of genes for melanin production but of no others. He used Selenia bilunaria and Tephrosia bistortata as material. The larvae were fed with leaves that had incorporated these salts: melanics subsequently appeared. A similar experiment in 1932 by McKenney Hughes failed to replicate these results; the statistician and geneticist Ronald Fisher showed that Heslop-Harrison's controls were inadequate, and that Hughes's findings made the 6% mutation rate required by Heslop-Harrison "improbable".

Kettlewell's experiment