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Viewpoint A Peppered Icon Enters the Genomic Era Chris D. Jiggins I n any field of scientific endeavor, there are certain ideas or examples that achieve iconic status, perhaps way beyond their individual importance. In evolutionary biology, iconic status has certainly been achieved by the humble peppered moth, Biston betularia. It is an unlikely candidate for celebrity status; it is a speckled black and white moth, common in northern temperate regions of Europe and North America. Like many species, its wing patterns impart an uncanny ability to blend into the background when it rests on mottled tree trunks. What has made this species famous, however, is a remarkably rapid evolutionary change in its coloration following the British Industrial Revolution, from the typical peppered form, typica, to a dark melanic form, carbonaria. A single genetic locus controls the switch from the typical to the melanic form, so this represented a simple evolutionary change at a single gene (Kettlewell 1973). Recent work has uncovered the genetic locus that controls this dramatic change in appearance, offering new insights into its evolutionary history (van’t Hof et al. 2011). Similar changes have been observed in many moth species, but what gained the peppered moth its iconic status was evidence that linked the undisputed evolutionary change that had occurred in the population to a causal mechanism—namely, natural selection by bird predators. A series of simple but compelling release-and-recapture experiments were carried out by Bernard Kettlewell in the 1950s that showed that dark moths had reduced survival in rural Dorset (an unpolluted area), whereas in polluted Manchester, the pattern was reversed, with the typical peppered form showing lower survival (Kettlewell 1973). These field studies were combined with caged-bird experiments showing attack patterns consistent with the survival patterns www.biosciencemag.org seen in the field. In combination with striking photographs of moths resting on lichen-covered and sooty tree trunks (the dark moths are alarmingly conspicuous on the former), this seemed to be one of the best documented examples of recent evolutionary change and became a textbook case of natural selection in action. Textbook examples deserve scrutiny every few years, if only to ensure that the original evidence holds up. The peppered moth came under such scrutiny about 10 years ago. In a book on melanism, Michael Majerus highlighted some aspects of Kettlewell’s experiments that were potentially unrealistic (Majerus 1998). The moths were placed on tree trunks, rather than under branches where they were thought to rest. The moth densities tested were unrealistically high. The different morphs were released at unnatural frequencies. Subsequently, Kettlewell has even been accused of fraud, although such accusations seem entirely unfounded (Hooper 2002). In the 10 years between the publication of his book and his tragic death in 2009, Majerus worked to rebut criticisms of Kettlewell’s experiments. He documented natural resting places of wild moths and showed that a significant proportion do indeed rest on tree trunks. More importantly, he also carried out a long-term experiment near Cambridge, United Kingdom, in which moths were allowed to choose their own resting sites and were then observed during daylight hours for direct evidence of predation. In an experiment that took six years, involved nearly 5000 moths and countless hours of observation, differential predation was observed and was, furthermore, strong enough to explain the natural observed rate of decline in the carbonaria morph during the experiment. Sadly, Majerus died before these results were published. However, he presented the data at the European Society of Evolutionary Biology meeting in Uppsala in 2007, and it is to be hoped that these valuable experiments will eventually be published. Clean-air legislation in the United Kingdom has led to a welcome return to mottled soot-free tree trunks and a steady decline in frequency of the carbonaria morph. Indeed, it is now so rare in most parts of the United Kingdom that field studies of natural selection will soon no longer be possible. However, just as one era is ending, the study of B. betularia has entered a new genomic era. The genetic locus that controls the carbonaria morph has recently been identified through genetic linkage mapping and gene-cloning techniques (van’t Hof et al. 2011). A sequence comparison of typica and carbonaria moths identified a unique sequence signature in all carbonaria individuals across a relatively broad region of the genome. This result confirms the hypothesis that the form has a single origin in the United Kingdom, which was already strongly implied by the geographic spread of carbonaria morphs after the first specimen was collected near Manchester in 1848. The genetic signature associated with typica forms is more complex, as would be expected if this were the ancestral, older form. These new population genetic data therefore provide strong support for the classic story, whereby a novel mutation arose once and spread rapidly by strong natural selection. So far, the broad genome region controlling carbonaria has been identified, but the actual gene or mutation responsible has not. Nonetheless, the data offer a couple of intriguing insights into the genetic mechanism underlying the change. First, the region identified does not contain any genes known to be involved in pigment production. In particular, studies of fruit flies with different patterns of wing and body spots September 2011 / Vol. 61 No. 9 • BioScience 655 Viewpoint have repeatedly shown the involvement of a handful of pigment-synthesis genes in evolutionary change (Wittkopp et al. 2003). These genes have helpful names, such as ebony, yellow, and tan, that reflect the colorful (well, mainly grayscale) effects of their laboratory mutants. However, none of these genes were found at the carbonaria locus (van’t Hof et al. 2011). It seems likely that carbonaria is in fact a gene located upstream—a regulatory locus rather than a pigmentation gene. This hypothesis gains further support from another remarkable observation. The locus of the carbonaria morph corresponds closely to a genome region already identified in our studies of butterflies. This locus controls yellow and white pattern elements in several species of mimetic tropical butterflies in the genus Heliconius (Joron et al. 2006). The same locus has since also been implicated in another genus of butterflies, Bicyclus, as containing genes that have major mutational effects in wing patterns—notably, a mutant called Bigeye (Beldade et al. 2009). This result is surprising: Butterfly wing eyespots, yellow bands, and overall melanization in a moth would not seem to be homologous patterns. Furthermore, these species are separated by more than 100 million years of evolution. The implication that there is a common mechanism of genetic control in these divergent lineages would seem to suggest an ancient shared patterning system in the Macrolepidoptera. So after a period in which the peppered moth seemed to have lost its iconic status, it should now be returned to its rightful place in the evolutionary textbooks. Kettlewell’s experiments have been vindicated. And genetic data provide a novel line of support for the original hypothesis of a single mutational origin for the dark carbonaria form. Of course, as is always the case in biology, there are surprises, and the study of a recent evolutionary change in response to industrialization has provided evidence for an ancient shared patterning system dating back to the early diversification of the Lepidoptera. The elucidation of the molecular mechanisms underlying this patterning system will provide an exciting challenge for the next few years. References cited Beldade P, Saenko SV, Pul N, Long AD. 2009. A gene-based linkage map for Bicyclus anynana butterflies allows for a more comprehensive analysis of synteny with the lepidopteran reference genomre. PLoS Genetics 5: e1000366. Hooper J. 2002. Of Moths and Men: An Evolutionary Tale—The Untold Story of Science and the Peppered Moth. Norton. Joron M, et al. 2006. A conserved supergene locus controls colour pattern diversity in Heliconius butterflies. PLoS Biology 4: e303. Kettlewell B. 1973. The Evolution of Melanism: The Study of Recurring Necessity, with Special Reference to Industrial Melanism in the Lepidoptera. Blackwell. Majerus MEN. 1998. Melanism: Evolution in Action. Oxford University Press. Van’t Hof AE, Edmonds N, Dalíková M, Marek F, Saccheri IJ. 2011, Industrial melanism in British peppered moths has a singular and recent mutational origin. Science 332: 958–960. Wittkopp PJ, Carroll SB, Kopp A. 2003. Evolution in black and white: Genetic control of pigment patterns in Drosophila. Trends in Genetics 19: 495–504. Chris D. Jiggins ([email protected]) is affiliated with the Department of Zoology at the University of Cambridge, England. doi:10.1525/bio.2011.61.9.3 Enter the Faces of Biology Photo Contest Communicate Your Research Through Imagery The Grand Prize Winner will have his/her winning photo featured on the cover of BioScience, and will receive $250 and a one year membership in AIBS. The contest ends on September 30, 2011. To enter, visit http://www.aibs.org/public-programs/photocontest.html 656 BioScience • September 2011 / Vol. 61 No. 9 www.biosciencemag.org