L. M. Cook

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.

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 todays 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.

Citizen Science Reveals Unexpected Continental-Scale Evolutionary Change in a Model Organism

Organisms provide some of the most sensitive indicators of climate change and evolutionary responses are becoming apparent in species with short generation times. Large datasets on genetic polymorphism that can provide an historical benchmark against which to test for recent evolutionary responses are very rare, but an exception is found in the brown-lipped banded snail (Cepaea nemoralis). This species is sensitive to its thermal environment and exhibits several polymorphisms of shell colour and banding pattern affecting shell albedo in the majority of populations within its native range in Europe. We tested for evolutionary changes in shell albedo that might have been driven by the warming of the climate in Europe over the last half century by compiling an historical dataset for 6,515 native populations of C. nemoralis and comparing this with new data on nearly 3,000 populations. The new data were sampled mainly in 2009 through the Evolution MegaLab, a citizen science project that engaged thousands of volunteers in 15 countries throughout Europe in the biggest such exercise ever undertaken. A known geographic cline in the frequency of the colour phenotype with the highest albedo (yellow) was shown to have persisted and a difference in colour frequency between woodland and more open habitats was confirmed, but there was no general increase in the frequency of yellow shells. This may have been because snails adapted to a warming climate through behavioural thermoregulation. By contrast, we detected an unexpected decrease in the frequency of Unbanded shells and an increase in the Mid-banded morph. Neither of these evolutionary changes appears to be a direct response to climate change, indicating that the influence of other selective agents, possibly related to changing predation pressure and habitat change with effects on micro-climate.

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.

The genetics of Cepaea nemoralis

THE genetics of the polymorphic snail Cepaea nemoralis is now relatively well known. Much recent work has been designed to investigate the polymorphism and at the beginning of the century the species was used to study heredity by Arnold Lang (1912 and earlier). Breeding of C. nemoralis was begun by Mr A. W. Stelfox in 1909 and has been continued until the present time. The results of some early experiments were reported in 1917 (Stelfox, 1918) and one mating was discussed by Fisher and Diver (i 934) in connection with an observation of their own. Since then very extensive studies by other authors, notably Lamotte (ii, 5954) and Cain et al. (Cain and Sheppard, 5952, 1957; Cain, King and Sheppard, 5960), have established or verified the principal properties of the system, rendering a full account of Stelfoxs work unnecessary. Mr Stelfox has, however, very kindly allowed me to study the results of matings set up to investigate band modifying and band pigment reducing factors, which add considerably to present knowledge. The conclusions are reported here, together with an account of the evidence for the inheritance of shell size.

Selection and gene flow on a diminishing cline of melanic peppered moths

Historical datasets documenting changes to gene frequency clines are extremely rare but provide a powerful means of assessing the strength and relative roles of natural selection and gene flow. In 19th century Britain, blackening of the environment by the coal-fired manufacturing industry gave rise to a steep cline in the frequency of the black (carbonaria) morph of the peppered moth (Biston betularia) across northwest England and north Wales. The carbonaria morph has declined across the region following 1960s legislation to improve air quality, but the cline had not been comprehensively described since the early 1970s. We have quantified changes to the cline as of 2002, equivalent to an interval of 30 generations, and find that a cline still exists but that it is much shallower and shifted eastward. Joint estimation of the dominant fitness cost of carbonaria and dispersal parameters consistent with the observed cline change indicate that selection against carbonaria is very strong across the landscape (s ≈ 0.2), and that dispersal is much greater than previously assumed. The high dispersal estimate is further supported by the weak pattern of genetic isolation by distance at microsatellite loci, and it implies that in addition to adult dispersal, wind-dispersed first instar larvae also contribute to lifetime dispersal. The historical perspective afforded by this study of cline reversal provides new insight into the factors contributing to gene frequency change in this species, and it serves to illustrate that, even under conditions of high dispersal and strong reverse selection acting against it, complete erosion of an established cline requires many generations.

Fossil evidence of recent human impact on the land snail fauna of Madeira

The Madeiran islands, located at 33?N in the eastern Atlantic, were colonized early in the 15th century, and perhaps up to a century earlier. The woodland and scrub cover was rapidly reduced and the amount of grassland and dis- turbed ground increased. The effect on the land snail popu- lation has been assessed by analysis of fossil assemblages from a deposit in eastern Madeira. Dates were obtained by measurement of amino acid epimer ratios (D-alloisoleucine/L- isoleucine) of individual shells, calibrated against radiocarbon- dated samples. Because this method allows dating of individual shells, it was possible to reconstruct the chronology of various species from mixed-age assemblages. It also per- mits dating of shells too young for radiocarbon dating (post- AD 1650). Fifteen land snail assemblages were analysed from deposits of post-settlement age (c. 420-50 yr BP). Of the thirty-four species of land snails present in the samples, nine have become extinct over the period. In contrast, only five species became extinct on the island during the previous c. 300,000 years. The majority of the extinctions have occurred within the last two centuries, as a result of habitat destruction. A major decline in the abundance of woodland species took place during the 20th century. The extinction of the endemic Caseolus bowdichianus, abundant in middle Holocene de- posits, occurred about a century after colonization of the island. Theba pisana, a snail of similar size and shape, was introduced around the time of colonization, and is now abun- dant in grassy areas. Two endemic grassland species, Discula polymorpha and Heterostoma paupercula, have also become more abundant and thus apparently benefited from the arrival of man.

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 Quaternary eolian sequence of Madeira: stratigraphy, chronology, and paleoenvironmental interpretation

A thick (ca. 40 m) sequence of coastal eolian sediments occurs on a narrow peninsula on the eastern end of the island of Madeira, located in the Eastern Atlantic at 33°N latitude. The sediments consist of black volcanic sands (with or without bioclasts) as well as clay units up to 2 m thick. A series of inceptisols (Eutrochrepts) and one alfisol (a Hapludalf) are developed in these sediments. Land snail shells and secondary carbonates, in the form of well-developed rhizoliths, calcretes, fissure-fills, and soil nodules, are present in abundance. The chronology of the sequence was determined by 14C and UTh analyses of land snail shells and secondary carbonates and amino acid epimerization analysis of land snail shells. All sediments, including the clay units, are originally of eolian origin, derived from the beach to the south of the deposit, but some have been redeposited by colluviation. Temporal variation in the lithology of the sediments relates to variations in sea-level, with black sands being deposited during lower sea level stands and clays at the lowest. It is suggested that fine marine sediments, exposed during low sea-level stands, may also be the dominant source of silty or clayey units in other coastal eolian deposits in the subtropical Atlantic and Mediterranean. The sequence spans from 200,000–300,000 years ago up to the 20th century. Sedimentation was discontinuous and often rapid; erosional hiatuses are present. During the Holocene, eolian sands started accumulating at 8200 yr B.P. during a transgressive phase and stopped at 4500 yr B.P. as sea level approached its present height. Colluviation increased dramatically following the first human settlement of the island in the 15th century and continued up to the 20th century, as dated by amino acid epimerization analysis of land snails. Earlier periods of colluviation were identified from the age distribution of land snail shells redeposited in younger colluvium. Paleoenvironmental reconstruction was based mainly on soil and sediment features (including rhizolith morphology) and land snail faunas but also on stable isotope variations (13C, 18O) in land snails and secondary carbonates, pollen (generally not well preserved), and phytoliths. Most of the portion of the Middle Pleistocene represented in the sequence was characterized by moderately dry conditions, in comparison to the late Pleistocene and Holocene. During the last interglacial, relatively wet conditions occurred, wetter than during the Holocene interglacial. Moderately moist conditions were present during the accumulation of the thick unit dating to ca. 80,000 yr B.P. As sea level fell subsequent to this period, conditions appear to have become drier. Starting ca. 50,000–55,000 yr B.P., conditions were especially wet, but prior to the last glacial maximum, markedly arid conditions ensued. Toward the end of the last glacial, wet conditions returned and produced the best-developed soil preserved in the sequence. Moderately moist conditions occurred during the early to middle Holocene but apparently become slightly drier after 4500 yr B.P. The impact of human settlement can be seen in the loss of woody vegetation and enhanced gullying and colluviation during the last ca. 500 years.

Land Snails of Eastern Madeira: Speciation, Persistence and Colonization

The Madeiran archipelago has an exceptionally rich land snail fauna (over 250 taxa), consisting mostly of endemic species with affinities with pre-Pleistocene Europe. Two surveys have been done to examine the distribution of species on the main island of the group, Madeira. The first shows that there is a faunal discontinuity between the eastern peninsula and the rest of the island. The second analyses the relation of the peninsula to the rest of Madeira. The peninsula has several distinctive species of its own. It also includes species usually from damp woodland, which appear to have a relict distribution there, and taxa nearly confined to it on Madeira but abundant on the Deserta islands and Porto Santo. Examination of a fossil sequence shows that damper conditions have occurred on the peninsula in the past. Variation in Discula polymorpha Heterostoma, Steenbergia spp. and Amphorella spp. may be interpreted as showing local adaptations that perhaps indicate parapatric evolution. The general pattern of distribution and the geological history of the islands suggests, however, that the present distributions result mostly from allopatric speciation in a geologically unstable region. As a whole, the archipelago is very species rich, but individual samples show low diversity. The possible contribution of interspecies competition to this pattern is considered.