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Understanding the genetic control of a complex polymorphism

Reference	BB/V01451X/1
Principal Investigator / Supervisor	Professor Chris Jiggins
Co-Investigators / Co-Supervisors
Institution	University of Cambridge
Department	Zoology
Funding type	Research
Value (£)	577,276
Status	Current
Type	Research Grant
Start date	01/03/2022
End date	28/02/2025
Duration	36 months

Abstract

An of current interest in evolutionary biology is the genetic control of complex polymorphisms. In some species, inversion polymorphism maintains tight linkage between genes controlling complex phenotypes. Here we study a system in which a complex polymorphism involving multiple traits is apparently not associated with any inversion or structural rearrangement, and only shows a narrow associated genomic region. One major goal will be to determine whether complex traits are controlled as pleiotropic effects of the 'colour' locus, or whether they have a more complex genetic architecture. The yellow/white polymorphism in male Arctia plantaginis has been localised to a handful of candidate genes. We will use RNAseq and CRISPR-generated gene knockouts to identify the causal gene at this locus. We will then use QTL mapping to explore the genetic basis for other traits including flight behaviour, immune response, pheromone and defensive chemistry known to differ between yellow and white males, to determine whether they are pleiotropic effects of the same locus. We will then use quantitative genetic approaches to identify loci underlying continuous variation in phenotype, specifically exploring a genetic trade-off between colouration in larval and adult females. This will use the animal model approach in large pedigrees of individuals already available from 10 years of laboratory breeding. We will take advantage of haplotagging for the large-pedigree and QTL mapping. This requires very low sequencing coverage for pedigree analysis Using the same sequencing approach, we will explore patterns of genetic variation in natural populations, testing for signatures of balancing selection in the site frequency spectrum and for linkage disequilibrium between loci. We will also use haplotagging data to explore structural variation around loci under selection.

Summary

Animals are hugely varied in their colouration, which can be adapted for a multiplicity of functions including camouflage, warning, sexual signals and thermoregulation. Stable polymorphisms in colouration offer an opportunity to study evolutionary processes including natural selection, gene flow and genetic drift acting in the wild. In some cases, variation in colour is an external indicator of differences between individuals in their physiology, behaviour and other complex traits. Such genetic correlations among colouration and other traits can be important for the maintenance of variation within populations. In some cases, such correlations are due to multiple genes in tight linkage, so-called supergenes, but in other cases complex polymorphisms seem to have a very simple genetic basis. Here we will study genetic correlations in the wood tiger moth, Arctia plantaginis. Males have either yellow or white hindwings, but these morphs also differ in behaviour, pheromones, immune responses and defensive chemistry. In contrast, females show continuous variation in hindwing colour, which is negatively correlated with larval warning colour. The system has many advantages for genetic analysis, being tractable to rear in large numbers and well-studied in the wild. Preliminary work on the male polymorphism has identified a narrow genomic region that controls morph differences, containing just six genes. Here we will identify the gene responsible for the yellow/white polymorphism using gene expression and gene knockdown experiments. Next, we will test whether the complex traits that differ between morphs vary as pleiotropic effects of the major yellow/white locus, or whether they represent variation at other loci perhaps maintained in linkage disequilibrium. We will also explore the genetic architecture of trade-offs in adult and larval colour traits that show more continuous variation. Here, we will take advantage of large pedigrees that are already available for genetic analysis. Additional breeding and phenotyping of families will be carried out with our Co-I Johanna Mappes in Finland. Finally, we will take advantage of large numbers of wild caught individuals already available to study patterns of genetic variation in the wild. In particular, we will test for signatures of balancing selection at loci controlling polymorphic and variable colour phenotypes. We will also test for patterns of association (linkage disequilibrium) between loci controlling multiple traits. In summary, this project offers an exciting opportunity to develop a new evolutionary genetic system. The wood tiger moth is already well studied in the field and laboratory. We know a great deal about its interaction with predators and with the biotic environment, as well as its behaviour and eco-physiology. However, despite many advantages for genetic analysis including ease of rearing in large numbers and relatively small genome, little genetic analysis has been carried out to date. Here we will explore the genetic basis for key traits in this system and explore the action of natural selection in wild populations at a genetic level. This project has the potential for developing an exciting new text-book example, in which evolutionary forces can be studied through from genotype to phenotype to fitness in the wild.

Committee	Research Committee C (Genes, development and STEM approaches to biology)
Research Topics	X – not assigned to a current Research Topic
Research Priority	X – Research Priority information not available
Research Initiative	X - not in an Initiative
Funding Scheme	X – not Funded via a specific Funding Scheme

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