The evolutionary genetics of sexually selected plumage colour traits in the galliform birds

Extravagant male plumage traits in birds are a classic example of sexual selection. However we know very little about the units that selection is acting upon, the genes themselves – what are they and how are they influenced by sexual selection? In this study I focused on in the evolution and genetics of colouration the galliform birds. Several novel loci were used to create a well resolved phylogeny of this group. This was then used to investigate and reconstruct the evolution of sexual plumage dichromatism. Four pigmentation genes were sequenced in an array of galliform species. A measure of the rate of evolutionary change (dN/dS) at these loci was then compared between lineages with different strengths of sexual selection, using sexual dichromatism as the main index of sexual selection. I found evidence for sexual selection acting at the MC1R locus, in the form of a robust correlation between dN/dS and sexual plumage dichromatism that was not found at any of the other loci. I then went on to investigate the evolution and population genetics of MC1R in the grouse, focusing on the strongly dichromatic black grouse and the relatively monochromatic red grouse. I found some evidence for an adaptive change at this locus between these species. Finally I used a candidate gene approach to investigate the role of several genes in avian pigmentation using the Japanese quail (Coturnix japonica) as a model system. I found evidence that the avian agouti gene is involved in dorso-ventral pigmentation patterning and a regulatory mutation at this locus that produces a yellow phenotype. In addition point mutations at MC1R and TYRP1 were found to be responsible for producing pigmentation variants. I then compared the expression of several of these candidate genes in male and female common pheasants (Phasianus colchicus) and found lower TYRP1 expression in males. Knowledge of the genetic basis of secondary sexual traits and the action of sexual selection at this level could have important implications for our understanding of the process of sexual selection as a whole.This work was funded by the Natural Environment Research Council under the Environmental Genomics programme [grant number NER/T/S/2002/00020]

How do predators generalize warning signals in simple and complex prey communities? Insights from a videogame

The persistence of distinct warning signals within and between sympatric mimetic communities is a puzzling evolutionary question because selection favours convergence of colour patterns among toxic species. Such convergence is partly shaped by predators' reaction to similar but not identical stimulus (i.e. generalization behaviour), and generalization by predators is likely to be shaped by the diversity of local prey. However, studying generalization behaviour is generally limited to simple variations of prey colour patterns. Here, we used a computer game played by humans as surrogate predators to investigate generalization behaviours in simple (4 morphs) and complex (10 morphs) communities of unprofitable (associated with a penalty) and profitable butterflies. Colour patterns used in the game are observed in the natural populations of unprofitable butterfly species such as Heliconius numata. Analyses of 449 game participants' behaviours show that players avoided unprofitable prey more readily in simple than in complex communities. However, generalization was observed only in players that faced complex communities, enhancing the protection of profitable prey that looked similar to at least one unprofitable morph. Additionally, similarity among unprofitable prey also reduced attack rates only in complex communities. These results are consistent with previous studies using avian predators but artificial colour patterns and suggest that mimicry is more likely to evolve in complex communities where increases in similarity are more likely to be advantageous

Altitude and life-history shape the evolution of Heliconius wings.

Phenotypic divergence between closely related species has long interested biologists. Taxa that inhabit a range of environments and have diverse natural histories can help understand how selection drives phenotypic divergence. In butterflies, wing color patterns have been extensively studied but diversity in wing shape and size is less well understood. Here, we assess the relative importance of phylogenetic relatedness, natural history, and habitat on shaping wing morphology in a large dataset of over 3500 individuals, representing 13 Heliconius species from across the Neotropics. We find that both larval and adult behavioral ecology correlate with patterns of wing sexual dimorphism and adult size. Species with solitary larvae have larger adult males, in contrast to gregarious Heliconius species, and indeed most Lepidoptera, where females are larger. Species in the pupal-mating clade are smaller than those in the adult-mating clade. Interestingly, we find that high-altitude species tend to have rounder wings and, in one of the two major Heliconius clades, are also bigger than their lowland relatives. Furthermore, within two widespread species, we find that high-altitude populations also have rounder wings. Thus, we reveal novel adaptive wing morphological divergence among Heliconius species beyond that imposed by natural selection on aposematic wing coloration

Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling.

An important goal in evolutionary biology is to understand the genetic changes underlying novel morphological structures. We investigated the origins of a complex wing pattern found among Amazonian Heliconius butterflies. Genome sequence data from 142 individuals across 17 species identified narrow regions associated with two distinct red colour pattern elements, dennis and ray. We hypothesise that these modules in non-coding sequence represent distinct cis-regulatory loci that control expression of the transcription factor optix, which in turn controls red pattern variation across Heliconius. Phylogenetic analysis of the two elements demonstrated that they have distinct evolutionary histories and that novel adaptive morphological variation was created by shuffling these cis-regulatory modules through recombination between divergent lineages. In addition, recombination of modules into different combinations within species further contributes to diversity. Analysis of the timing of diversification in these two regions supports the hypothesis of introgression moving regulatory modules between species, rather than shared ancestral variation. The dennis phenotype introgressed into Heliconius melpomene at about the same time that ray originated in this group, while ray introgressed back into H. elevatus much more recently. We show that shuffling of existing enhancer elements both within and between species provides a mechanism for rapid diversification and generation of novel morphological combinations during adaptive radiation.This work was funded by BBSRC grant H01439X/1, ERC grant MimEvol and ANR grant HybEvol to MJ.This is the final version of the article. It was first available from PLOS via http://dx.doi.org/10.1371/journal.pbio.100235

Selective sweeps on novel and introgressed variation shape mimicry loci in a butterfly adaptive radiation.

Natural selection leaves distinct signatures in the genome that can reveal the targets and history of adaptive evolution. By analysing high-coverage genome sequence data from 4 major colour pattern loci sampled from nearly 600 individuals in 53 populations, we show pervasive selection on wing patterns in the Heliconius adaptive radiation. The strongest signatures correspond to loci with the greatest phenotypic effects, consistent with visual selection by predators, and are found in colour patterns with geographically restricted distributions. These recent sweeps are similar between co-mimics and indicate colour pattern turn-over events despite strong stabilising selection. Using simulations, we compare sweep signatures expected under classic hard sweeps with those resulting from adaptive introgression, an important aspect of mimicry evolution in Heliconius butterflies. Simulated recipient populations show a distinct 'volcano' pattern with peaks of increased genetic diversity around the selected target, characteristic of sweeps of introgressed variation and consistent with diversity patterns found in some populations. Our genomic data reveal a surprisingly dynamic history of colour pattern selection and co-evolution in this adaptive radiation

Limited genetic parallels underlie convergent evolution of quantitative pattern variation in mimetic butterflies

Mimetic systems allow us to address the question of whether the same genes control similar phenotypes in different species. Although widespread parallels have been found for major effect loci, much less is known about genes that control quantitative trait variation. In this study, we identify and compare the loci that control subtle changes in the size and shape of forewing pattern elements in twoHeliconiusbutterfly co-mimics. We use quantitative trait locus (QTL) analysis with a multivariate phenotyping approach to map the variation in red pattern elements across the whole forewing surface ofHeliconius eratoandHeliconius melpomene. These results are compared with a QTL analysis of univariate trait changes, and show that our resolution for identifying small effect loci is somewhat improved with the multivariate approach, but also that different loci are detected with these different approaches. QTL likely corresponding to the known patterning geneoptixwere found in both species but otherwise, a remarkably low level of genetic parallelism was found. This lack of similarity indicates that the genetic basis of convergent traits may not be as predictable as assumed from studies that focus solely on Mendelian traits.Peer reviewe

ARIA-EAACI statement on asthma and COVID-19 (June 2, 2020)

Non peer reviewe