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The Quarterly Review of Biology Volume 78, No. 4 December 2003 The Quarterly Review of Biology THE RISE AND FALL OF THE CARBONARIA FORM OF THE PEPPERED MOTH Laurence M. Cook The Manchester Museum, University of Manchester Manchester M13 9PL, United Kingdom e-mail: [email protected] keywords peppered moth, Biston betularia, melanism, selection, predation, Kettlewell abstract 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 carbon- aria 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. ISTON BETULARIA (L.) has been called marks on a white background. Harris noted B the peppered moth at least since the that the larvae come in a variety of colors time of Moses Harris (1766), because typically from black to olive and that the moths are the wings and body are sprinkled with black “sometimes found sitting against the bark.” The Quarterly Review of Biology, December 2003, Vol. 78, No. 4 Copyright ᭧ 2003 by The University of Chicago. All rights reserved. 0033-5770/2003/7804-0001$15.00 399 400 THE QUARTERLY REVIEW OF BIOLOGY Volume 78 Since he mentions larval but not adult varia- urban environment. Pollutant gases declined tion it is unlikely that black forms were known too, but less dramatically and they were more to lepidopterists in his time. There were one widely dispersed. or two black individuals in collections by the The change in frequency of melanic forms beginning of the 19th century (Ford 1975; of moths in the 19th century was brought to Berry 1990), but they were not reported in the attention of the scientific community by the literature until the second half of the cen- William Bateson in relation to his dispute tury (Edelston 1864; Chappell 1886). The with the biometricians over the evolutionary darkest melanic was named doubledayaria by significance of distinct variants (see e.g., Prov- Millie`re (1872), later replaced in common ine 1971). Bateson (1900) published a “mem- usage by carbonaria ( Jordan 1869). The sev- orandum” from the Royal Society’s Evolution eral intermediate forms received the varietal Committee, asking entomologists for infor- name insularia (Thierry-Mieg 1886). The mation. The results were published (Barrett material for these descriptions came from 1901; Doncaster 1906) and discussed by Bate- northern England (see Cook and Muggleton son (1913). Melanism in the peppered moth 2003). was soon shown to be genetic and dominant Increase in melanics among moths fol- in effect (e.g., Bowater 1914). First sightings lowed the onset of industrialization, with its of carbonaria were from industrial Lancashire accompanying pollutants. London had suf- and Yorkshire (1848 to 1860), and progres- fered serious atmospheric pollution since the sively later from points north and south, Middle Ages, but developments in the indus- reaching London in 1897. There was much trial north of England were on a new scale. contemporary interest in the phenomenon, In the 17th century, spinning and weaving of and the pattern of spread suggests a single linen, cotton, and wool took place in hill val- source of origin (Steward 1977a). leys of Lancashire and Yorkshire, first as cot- A massive and widespread increase in the tage occupations and then in water-powered frequency of melanics had evidently taken mills. Cities such as Manchester and Leeds place, but the evidence was fragmentary and were manufacturing, finishing, and distribu- anecdotal. Haldane (1924, 1932) used it as an tion centers. In time the whole complex example of strong selection and examined became driven by coal power. The population mean selection per generation for periods of of Manchester was 24,000 in 1770. In 1800 it several generations (in Europe there is one was three times larger, and by 1850 over 10 generation per year). Work by H B D Kettle- times larger. Coal was used in the home as well showed that by the 1950s a large area of well as to drive machines, so smoke and sulfur England had carbonaria frequencies over and nitrogen gases became appallingly 90%. The frequency started to drop again in intense. Contemporary accounts record the the early 1970s. darkness of the skies and blackness of the It is intended here to present information buildings; attempts to control pollution were on this decline in melanic frequency and to largely ignored. Towns were not completely discuss the probable magnitude and type of devoid of plants and animals, however. Trans- selection involved. One aim is to draw port required horses; cows for milk were kept together and assess a range of data, some of in cities. Quantities of hay and grain were it from rather inaccessible sources. The story brought in, which would support populations was interesting at the start of the 20th century of small birds. Although dense, pollution was and is still so now. However, another reason highly localized and surrounding areas still for a review is the recent tendency in several retained their rural character. Smoke pollu- quarters to level charges of ignorance or tion continued in the growing conurbations deceit at researchers in the field. Part of the of the 20th century, and it was only in the attack comes from the antievolution lobby, 1960s, when coal as a fuel was replaced by oil e.g., Wells (2000), who writes of moves to “rid and electricity, that a significant drop textbooks of this fraud” (for a specific rebut- occurred. Smoke abatement legislation and tal of his claims see Rudge 2002). A book extensive rebuilding again transformed the review by Coyne (1998) gave much satisfac- December 2003CARBONARIA FORM OF THE PEPPERED MOTH 401 tion to creationists, and is frequently quoted 1a represents the data from 1952 to 1970. The on the web in their material on evolution and most notable feature is the cline running education (e.g., by J D Morris of the Institute from the north of Wales to the southeast of for Creation Research and by the Biblical England, which separates a region of low car- Creation Society; but see Rudge 2000). Other bonaria frequency west from the high fre- attacks are more mysterious. Although they quency areas of the east. Northern industrial are “certain that this phenomenon is a prod- England, including parts that are not urban- uct of selection,” Sargent, Millar, and Lam- ized, had a uniform frequency over 90%. This bert (1998) claim that almost everything continued southwards, dropping to 70% to about the melanism studies carried out so far 80% in the London area but remaining high is, possibly, wrong. In advance publicity for in rural eastern parts. The cline was steepest her book, Hooper (2002) contended that in the north, close to the Welsh/English bor- Kettlewell, “a deluded bumbling scientist,” der. A more detailed map given by Bishop et fraudulently arranged his evidence to satisfy al. (1978a) has the contours displaced some- an equally dissimulating E B Ford (but see what to the east because it is based on a more Coyne 2002; Grant 2002; Rudge 2003). No restricted set of values (the full data for this one determined to find fault will be swayed region are in Clarke and Sheppard 1963, by the presentation of evidence here, but 1966; Bishop 1972; Bailey et al. 1973; Whittle hopefully it will be useful in discussion of the et al. 1976; and the microfiche in Bishop et subject when a calmer atmosphere prevails. al. 1978a). During this period, melanic morph frequencies were positively associated Surveys in Britain with atmospheric sulfur dioxide concentra- tion rather than with smoke (Kettlewell 1973; H B D Kettlewell coordinated three surveys Lees et al. 1973; Bishop et al. 1975). of morph frequencies over the country, from A survey carried out in the 1980s used 1952 to 1956, from 1957 to 1964, and from information provided by students of the 1965 to 1970 (Kettlewell 1958, 1965, 1973). Open University (Cook et al. 1986). Each had They are usually taken to represent the stable a standard collecting trap to sample from pattern at the middle of the century (e.g., in their home location; all accepted records pie diagrams by Kettlewell 1973; Lees 1981; being verified as the correct species and Majerus 1998). In Biston betularia there are morphs. Small individual samples were several alleles intermediate in expression and obtained (often fewer than 10 individuals), dominance between the carbonaria and typi- but they were widely dispersed.
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