Mechanism of adaptation to environmental change: parallel evolution of melanism in the peppered moth

Lead Research Organisation: University of Liverpool
Department Name: Institute of Integrative Biology

Abstract

The genetic raw material that allows a population to respond adaptively to environmental change must come from one of three different sources: 1) genetic variation already present in the population; 2) immigration from another population that has the necessary genetic variation; or 3) spontaneous mutation within the population that produces a beneficial trait. Because a novel phenotypic trait may be produced through a variety of alternative genetic and developmental pathways, adaptive responses to the same environmental change in different populations could involve the same or different genetic changes. Furthermore, the idea that many adaptations are controlled by a restricted subset of genetic master switches or 'hotspots' implies that the origin of phenotypic novelty is to some extent predictable. This overall process influences the likelihood of a novel trait appearing in a population and therefore on the rate of adaptation. However, there are very few well worked examples of mutational origins and the existence of genomic hotspots for adaptation in natural populations.
This research aims to expand our understanding of these phenomena in the context of industrial melanism in the peppered moth. This species provides excellent material for studying the mechanism of adaptation. It is widely known that in 19th century Britain till the 1970s, a black coloured variety of this moth, which had never been seen before, replaced the light coloured 'typical' form. The reason for this is that high levels of coal soot in the air caused darkening of the surfaces which peppered moths rest on during the day-time. This made the typical form much more visible than the black form to bird predators, and so the genetic variants producing the typical form rapidly declined. What is less well known is that essentially the same change happened at around the same time in the peppered moth populations of mainland Europe and eastern North America. Were these parallel changes in the separate populations made possible by the same mutation spreading around the world or by different, home-grown, mutations? If there were different mutations, did they occur in the same or different genes?
For the British peppered moth population, recent genetic studies have shown that all black peppered moths (called carbonaria) are descended from just one mutant ancestor from the 19th century. Surprisingly, the obscure chromosomal region where the carbonaria gene was found turns out to also control very different colour patterns in butterflies, which hints at a deeply conserved mechanism, perhaps a hotspot. Our objective is to similarly discover the original genetic source of the black peppered moths in mainland Europe and in N America. Preliminary evidence already suggests that they are different from the UK carbonaria and also that they may be much older. This latter possibility is significant because it would mean that, in some populations, the genetic variation for the black form existed before industrialisation.
We will take three complementary approaches to this problem: 1) Use parent-offspring families to work out whether the chromosomal regions controlling the black morphs are the same or different between populations. 2) Compare DNA sequence variation associated with black and typical moths in population samples, including early 20th century museum specimens through to modern day specimens. This will tell us if the black moths in Europe and N America come from different ancestors, and whether these ancestors came into being relatively recently, or have a much more ancient history. 3) Measure the activity of the genes that we find during the critical period of melanin production, shortly before the adult moth emerges from the pupa. The findings of this research will add significantly to our understanding of how natural populations adapt to rapid environmental change, which is important to anticipating the consequences of human activity.

Planned Impact

Parallel evolution raises several deep and important general questions about the mechanism of adaptation. The proposed research is aimed at revealing the details of this mechanism in a biological system that is familiar to a wide audience. The intra-specific level of enquiry and contemporary nature of the material lets us get close to the evolutionary process itself. These features lend themselves to effective dissemination of the research to a broad target audience, including professional biologists, school teachers/pupils, university students, the general public, and environmental policy makers.

There is also an international dimension to the beneficiaries. Because peppered moth industrial melanism has been most actively studied in Britain, the vast majority of biology textbooks refer only to this example, even in countries such as USA and several in western/central Europe, that experienced their own industrial melanisation. This ongoing situation has led to the perception that the changes to the British population were a special case. By uncovering the story behind the non-British melanic populations this research will broaden appreciation of the worldwide scale of the phenomenon.

Through its prominent use as an example in science education, peppered moth industrial melanism has come under attack by anti-science forces, particularly in USA. In this context I have had contact with the National Centre for Science Education, whose mission is to defend the teaching of evolution in schools. Simplified descriptions of multiple origins of the same trait in the same species will provide an added layer of evidence (against intelligent design) for science teachers.

The story of melanism in the peppered moth, which has mostly been told by British scientists, is part of the evolutionary biology canon and a landmark of the scientific intellectual tradition. There is no doubt, therefore, that by adding a new dimension to the existing body of classical work accumulated over nearly a century, this research will make a lasting contribution to the cultural heritage of the UK and the international community.

At least two museums (Cardiff Museum and Cambridge Museum of Zoology) will benefit directly from the proposed research through professionally designed and produced exhibits which will integrate the new results into the classic industrial melanism story. In the medium term (within 3-5 years), the results should also start to find their way into undergraduate, and possibly also secondary school, textbooks.
 
Description Linkage mapping studies have established that melanism in continental European (EU) and North American (NA) peppered moths is controlled by the same genetic region as in British carbonaria, but that the mutational origins are different.
Extensive population samples collected in EU and NA (contemporary and museum).
Contrary to the widely held assumption, in EU multiple haplotypes are associated with the same melanic phenotype, suggesting either that they pre-date the industrial revolution or that mutation rate is high.
Exploitation Route Identify the specific functional sequence mutations in EU and NA haplotypes, as has been done for the British carbonaria haplotype.
Sectors Education,Culture, Heritage, Museums and Collections

URL http://planetearth.nerc.ac.uk/multimedia/story.aspx?id=1743&cookieConsent=A
 
Description Recurrent adaptation to industrial pollution: ancestral diversity and ecological succession
Amount £647,487 (GBP)
Funding ID NE/T000597/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 07/2019 
End 07/2022
 
Title Sequence and genotype information 
Description Gene sequences have been submitted to GenBank, and polymorphic markers/genotypes to Dryad. 
Type Of Material Database/Collection of data 
Year Produced 2013 
Provided To Others? Yes  
Impact Provide a gene reference and linkage map for other Lepidoptera. Provide mutant and wild-type core haplotype sequences. 
URL https://www.ncbi.nlm.nih.gov/gquery/?term=KT182637
 
Description Bruce Grant 
Organisation College of William & Mary
Country United States 
Sector Academic/University 
PI Contribution Expertise and intellectual input, and virgin peppered moth material for crosses
Collaborator Contribution Prof Bruce Grant produced genetic crosses that allowed us to map the locus controlling melanism in north American peppered moths
Impact Melanism maps to the same region as in UK peppered moths. Results not yet published.
Start Year 2010
 
Description Frantisek Marec lab, Ceske Budejovice, Czech Republic 
Organisation Academy of Sciences of the Czech Republic
Country Czech Republic 
Sector Academic/University 
PI Contribution Population genetics/bioinformatics expertise; mapping studies; population samples
Collaborator Contribution Molecular cytogenetics and assistance in sampling peppered moths in Czech Republic
Impact Van't Hof et al Science 2011; Van't Hof et al Heredity 2012.
Start Year 2008
 
Description Josef Settele, UFZ 
Organisation Helmholtz Association of German Research Centres
Department Helmholtz Centre for Environmental Research - UFZ
Country Germany 
Sector Academic/University 
PI Contribution Expertise and intellectual input
Collaborator Contribution Provided accommodation and research facilities to allow sampling of peppered moths in eastern Germany
Impact We found high frequencies of melanic moths associated with historical and current coal mining areas in eastern Germany. Genetic analysis suggests that this phenotype has evolved through different mutations, some of which occur sympatrically in the present day. Published outputs are in preparation.
Start Year 2013
 
Description Laszlo Rakosy 
Organisation Babes-Bolyai University
Country Romania 
Sector Academic/University 
PI Contribution Conducting field surveys of peppered moth melanism in Romania.
Collaborator Contribution Hosting field surveys of peppered moth melanism in Romania.
Impact Preliminary survey suggests that factors additional to (historical) atmospheric coal pollution may maintain high frequencies of peppered moth melanism.
Start Year 2016
 
Description Lawrence Gall 
Organisation Peabody Museum of Natural History
Country United States 
Sector Academic/University 
PI Contribution Expertise and intellectual input
Collaborator Contribution Lepidoptera collections database and permission to sample legs from large numbers of specimens over several days
Impact Discovery that melanism in North American peppered moths is due to different mutational events than in Britain or continental Europe, although the appearance of the phenotype is the same. Further work is needed before published outputs can be produced.
Start Year 2012
 
Description Wouter Dekoninck 
Organisation Royal Belgian Institute of Natural Sciences
Country Belgium 
Sector Learned Society 
PI Contribution Expertise and intellectual input
Collaborator Contribution Access to peppered moth specimens and assistance in sampling legs for genetic studies.
Impact No outputs as yet
Start Year 2013
 
Description BBC video 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Video interview describing the recent discovery of the molecular identity of the mutation that gave rise to industrial melanism in British peppered moths
Year(s) Of Engagement Activity 2016
URL http://www.bbc.co.uk/news/science-environment-36424768
 
Description Biology of Butterflies (Turku) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other academic audiences (collaborators, peers etc.)
Results and Impact Talk sparked questions and discussion afterwards

Much excitement over the discovery of the carbonaria mutation.
Year(s) Of Engagement Activity 2014
 
Description Manchester Museum 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Presentation on the the genetics of industrial melanism as part of Manchester Museum "Climate Control" exhibition, attended by approximately 50 members of the general public.
Year(s) Of Engagement Activity 2016
 
Description RES graduate forum 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Postgraduate students
Results and Impact Presentation at the Royal Entomological Society Graduate Forum meeting in Sheffield
Year(s) Of Engagement Activity 2016
 
Description Secondary School outreach talk 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? Yes
Geographic Reach Local
Primary Audience Schools
Results and Impact Talk sparked questions and discussion afterwards.

Pupils wanted to know more ab0ut the system.
Year(s) Of Engagement Activity 2014