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

Abstract

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. 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. 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.

Genetic and epigenetic variation in Spartina alterniflora following the Deepwater Horizon oil spill

“…A classic example is the rapid phenotypic change experienced by the peppered moth as a result of coal pollution (Kettlewell, 1958), which was recently explained by the activity of transposable elements that alter its development (van't Hof et al., 2016). Several studies also describe molecular differentiation in marine organisms across the eastern coast of the United States in response to aquatic pollution (Chapman et al., 2011; Whitehead et al., 2012; Williams & Oleksiak, 2008).…”

Signatures of positive selection and local adaptation to urbanization in white‐footed mice (Peromyscus leucopus)

“…Past urban evolutionary studies often focus solely on phenotypic (Yeh 2004; Partecke et al 2006; Cheptou et al 2008; Thompson et al 2016) or genetic (Wandeler et al 2003; Noël & Lapointe 2010; Mueller et al 2013; Lourenco et al 2017) differences between populations in and outside of cities. However, researchers are beginning to examine both the genotype and phenotype in parallel instances of urban evolution (Whitehead et al 2010; Wirgin et al 2011; Hof et al 2016), which is key to understanding how urbanization affects the evolution of species. In the future, the gene annotations for our predicted outlier genes can help determine which phenotypic traits to measure in urban P. leucopus populations.…”

“…Urban adaptation has also been confirmed in the well-known peppered moth ( Biston betularia ) system. Recent evidence suggests that the industrial melanism trait in this species is linked to an insertion of a transposable element in the cortex gene in the early 1800s that spread throughout the population in response to industrial airborne pollution (Hof et al 2016). The study of additional systems will likely identify a complex array of adaptive evolutionary responses in cities (Whitehead et al 2017).…”

The Genomic Basis of Color Pattern Polymorphism in the Harlequin Ladybird

“…A common example in natural populations of insects is the occurrence of different color patterns, which has motivated a rich body of ecological and genetic research [1, 2, 3, 4, 5, 6]. The occurrence of dark, i.e., melanic, forms displaying discrete color patterns is found across multiple taxa, but the underlying genomic basis remains poorly characterized.…”