Journal Article

The industrial melanism mutation in British peppered moths is a transposable element

Campagne, Pascal, Rigden, Daniel J., Lingley, Jessica, Yung, Carl J., Hall, Neil, Darby, Alistair C., Saccheri, Ilik J., Hof, Arjen E. van’t, Quail, Michael A.

2016

Overview

The mutation responsible for the black carbonaria morph of the peppered moth is identified as a transposable element within the cortex gene. The look of Lepidoptera driven by cortex The darkening of the peppered moth Biston betularia , the phenomenon known as industrial melanism, is a textbook example of evolutionary biology in action. However, the genetic background of the black or c arbonaria variants has remained unclear. Building on their earlier work that isolated the gene responsible to within a roughly 400-kilobase region containing 13 genes, Ilik Saccheri and colleagues have identified the melanism-causing event as the insertion of a class II transposable element into the first intron of a gene called cortex . Statistical inference indicates that the polymorphism occurred around 1819, when the Industrial Revolution was well under way. In a separate study, Nicola Nadeau et al . report that colour patterning in butterflies of the genus Heliconius is also mediated by expression of the cortex gene, apparently co-opted to control the rate of scale cell development, on which colour depends. Taken together, these two papers suggest that cortex , conserved widely within Lepidoptera, is a major target for natural selection acting on colour and pattern variation. Discovering the mutational events that fuel adaptation to environmental change remains an important challenge for evolutionary biology. The classroom example of a visible evolutionary response is industrial melanism in the peppered moth ( Biston betularia ): the replacement, during the Industrial Revolution, of the common pale typica form by a previously unknown black ( carbonaria ) form, driven by the interaction between bird predation and coal pollution 1 . The carbonaria locus has been coarsely localized to a 200-kilobase region, but the specific identity and nature of the sequence difference controlling the carbonaria – typica polymorphism, and the gene it influences, are unknown 2 . Here we show that the mutation event giving rise to industrial melanism in Britain was the insertion of a large, tandemly repeated, transposable element into the first intron of the gene cortex . Statistical inference based on the distribution of recombined carbonaria haplotypes indicates that this transposition event occurred around 1819, consistent with the historical record. We have begun to dissect the mode of action of the carbonaria transposable element by showing that it increases the abundance of a cortex transcript, the protein product of which plays an important role in cell-cycle regulation, during early wing disc development. Our findings fill a substantial knowledge gap in the iconic example of microevolutionary change, adding a further layer of insight into the mechanism of adaptation in response to natural selection. The discovery that the mutation itself is a transposable element will stimulate further debate about the importance of ‘jumping genes’ as a source of major phenotypic novelty 3 .

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 38 / 45/23 / 631/181/2474 / 631/208/199 / Adaptation / Adaptation, Physiological - genetics / Alleles / Amino acids / Animals / Artificial chromosomes / Biological Evolution / Biological research / Butterflies & moths / Cell Cycle - genetics / Cell division / Color / DNA Transposable Elements - genetics / Environmental aspects / Environmental changes / Evolution & development / Gene mutation / Genes / Genes, Insect - genetics / Genetic aspects / Haplotypes / Haplotypes - genetics / Humanities and Social Sciences / Identification and classification / Introns - genetics / letter / Male / Melanism (Evolutionary adaptation) / Melanosis - genetics / Melanosis - veterinary / Mode of action / Moths / Moths - cytology / Moths - genetics / Moths - physiology / multidisciplinary / Mutagenesis, Insertional - genetics / Mutation / Mutation - genetics / Phenotype / Pigmentation - genetics / Pigmentation - physiology / Science / Selection, Genetic - genetics / United Kingdom / Wings, Animal - growth & development / Wings, Animal - physiology