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Industrial Melanism and Peppered Moths (Biston Betularia (L.))

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Industrial Melanism and Peppered Moths (Biston Betularia (L.)) Biological Journal ofthe Linnean Soczep (1990), 39; 301-322. With 4 figures Industrial melanism and peppered moths (Bistom betularia (L.)) Downloaded from https://academic.oup.com/biolinnean/article/39/4/301/2654253 by guest on 29 September 2021 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: Peppered moth - microevolution natural selection - bird prrdation - air pollution. CONTENTS Introduction ................... 30 1 Observations and interpretations .............. 302 Genetics ...................304 Geographical distribution ............... 305 Natural selection, etc ................ 308 Behaviour. ..................309 Multiple factor analysis and models ............. 312 Acknowledgements ................. 314 References. ...................314 Appendix A: Tutt (1896) on peppered moth melanism ......... 317 Appendix B: Suggestions for further work ............ 318 Appendix C: History of peppered moth melanism work ......... 319 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 30 I 0024-4066/90/040301+ 22 $03.00/0 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 Downloaded from https://academic.oup.com/biolinnean/article/39/4/301/2654253 by guest on 29 September 2021 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, 1955~~1956a, 1958, 1959, 1965a, 196513; Kettlewell & Conn, 1977), and largely summarized in his definitive book The Evolution of 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. In 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 MOTHS 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 Tutt (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. The 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 Downloaded from https://academic.oup.com/biolinnean/article/39/4/301/2654253 by guest on 29 September 2021 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. The 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 an 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). *In 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 at all improbable that the establishing of a new variety at the expense of an older one in a relatively short space of time is continually
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