New insight into the genetic basis of industrial melanism

The evolution of coloration in peppered moths during the industrial revolution is one of the most well known examples of natural selection in action. Part of the appeal of the system is the apparent simplicity. The once-abundant light colored morph (typica) dominated in the early 1800’s. However, by 1900 nearly all individuals were black (carbonaria). As early as 1896 it was hypothesized that this drastic change in coloration was driven by an increase of soot produced from the smoke stacks of factories built in the 1800s. It was thought that predation by birds resulted in high mortality in the typica morphs, which would stand out on black, sooty backgrounds. Predation on white typica morphs would then increase the proportion of carbonaria morphs that could match the color of their background and… poof! Evolution.

© wikipedia

Examples of carbonaria (left) and typica (right) morphs. © wikipedia

Oddly, no one actually tested this predation hypothesis until Bernard Kettlewell in the 1950’s (link). He performed some fairly simple aviary experiments, mark recapture experiments, and observations of predation events. These results convincingly demonstrated how predation can result in drastic phenotypic changes over quite short time periods (~50 years). It should be noted that there have been some significant criticisms of this system ranging from accusations of poor experimental design to outright fraud. However, these criticisms haven’t held up with time. Michael Majerus did much to refute these criticisms, including redoing Kettlewell’s experiment (Cook et al., 2012, published posthumously) and writing numerous reviews on the subject (Majerus 2009); his work is worth the read.
While this system is well known, the genetic basis of industrial melanism (i.e., increasing pigmentation in response to a darkening environment with industrialization) has remained elusive. Recently, however, Arjen van’t Hof and co-authors have found that a transposable element in the first intron of the gene cortex is responsible for dark coloration.
Previous work had localized the cabonaria locus to a ~400 kb region. Using fine-scale association mapping, the authors narrowed this region down to 100 kb, all of which resides within the cortex gene. The authors thought that, because the causal carbonaria haplotype must have arisen on a typica background, they only had to identify the variant specific to carbonaria to find the causal polymorphism. They compared one carbonaria to three typica individuals to identify the first set of carbonaria specific polymorphisms; these 87 polymorphisms were considered melanization candidates. By screening more and more typica individuals, they were eventually able to find all but one polymorphism in typica individuals. This remaining polymorphism that is unique to carbonaria is the causative variant.
The authors next took advantage of the decay of the carbaonaria haplotype block to date the age of the polymorphism. This method found that the mutation likely arose around 1819, a date that makes sense given the first sighting of a carbonaria phenotype in the 1840’s (see figure for maximum likelihood distribution of mutation dates).
Probability distribution for date of carbonara mutation. From van't Hof et al., 2016

Probability distribution for date of carbonara mutation. From van’t Hof et al., 2016

The causative polymorphism, a 21.9 kb transposable element, actually increases the abundance of cortex transcripts. However, how cortex causes melanism is still unresolved. Interestingly, parallel findings in Heliconius butterflies also implicate the cortex gene in generating coloration (link).
It is always exciting to see a study find the causative variant for an adaptive phenotype. At the same time, it reminds me how hard it is to actually identify these variants. Even for a trait where only one allele of large effect is involved, finding that variant is a tremendous undertaking (this trait might not actually be only 1 gene: 5 out of 110 carbonaria morphs were missing the variant, which suggests there is some other basis for dark coloration…). Most traits, however, are coded in many alleles—sometimes hundreds—which makes finding their underlying genetic bases difficult.
van’t Hof et al. have provided a nice study identifying the genetic basis of industrial melanism. Hopefully there will be some insight soon as to the mechanisms for how cortex is involved in melanism!
Cook, L.M., Grant, B.S., Saccheri, I.J. and Mallet, J., 2012. Selective bird predation on the peppered moth: the last experiment of Michael Majerus.Biology Letters, p.rsbl20111136.
Kettlewell, H.B.D., 1955. Selection experiments on industrial melanism in the Lepidoptera. Heredity, 9, pp.323-342.
Majerus, M.E., 2009. Industrial melanism in the peppered moth, Biston betularia: an excellent teaching example of Darwinian evolution in action.Evolution: Education and Outreach, 2(1), pp.63-74.
van’t Hof, A.E., Campagne, P., Rigden, D.J., Yung, C.J., Lingley, J., Quail, M.A., Hall, N., Darby, A.C. and Saccheri, I.J., 2016. The industrial melanism mutation in British peppered moths is a transposable element. Nature534(7605), pp.102-105.

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