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Jiggins, C.

Publications and source records attributed to Jiggins, C..

9 recordsLinked to original sources

Toxin structure shapes palatability in a chemically defended butterfly

The toxicity of chemical defences is well studied, but the potential contribution of compound structure to predator deterrence remains largely unexplored. Whether predation acts more strongly on toxicity or unpalatability remains largely untested, partly because few systems allow toxin structure to vary independently of quantity. Heliconius sara larvae provide such a system: those reared on Passiflora auriculata sequester cyclopentenyl cyanogenic glucosides (CGs), while those reared on P. biflora biosynthesise comparable quantities of aliphatic CGs. Using two invertebrate predators, Camponotus floridanus ants and Hierodula membranacea mantids, we tested whether this structural difference affects palatability independent of toxicity. Mantids rejected larvae with cyclopentenyl CGs more often than larvae with aliphatic CGs, despite no detectable difference in total CG content. This pattern was mirrored in extract-based assays with ants, independently of cyanide release: extracts with cyclopentenyl CGs remained deterrent, while extracts with aliphatic CGs did not differ in deterrence from water. Live larvae, by contrast, elicited similar responses from ants regardless of CG structure. These results show that variation in toxin structure can strongly affect palatability, with some compounds conferring greater protection than others. This demonstrates the importance of chemical structural diversity in the evolution of chemical defences.

evolutionary biology↗

Genetic parallelism underpins convergent mimicry coloration across Lepidoptera

Convergent evolution, the repeated evolution of similar phenotypes in response to the same selective pressures across multiple lineages, is widespread in nature. The extent to which the same genetic mechanisms contribute to convergent evolution could reveal whether the pathway towards these optimal endpoints is flexible or constrained to follow a particular route. Although mimicry of aposematic colour patterns is well known in Lepidoptera, our knowledge of the genetic basis of these convergent patterns is mostly restricted to a few closely-related species. Here we study the genetic basis of mimicry across seven species of Ithomiini and Heliconius butterflies and a day-flying Chetone moth, representing lineages that diverged between [~]1-120 Mya, each presenting similar colour pattern switches. In all the butterfly species, the genetic variants most strongly associated with convergent colour pattern switches are similarly located in non-coding regions near the genes ivory and optix. Colour pattern variation in the moth is associated with a [~]1 Mb inversion around ivory paralleling the supergene architecture of the co-mimic Heliconius numata. In contrast to previous studies in Heliconius, there is limited evidence of alleles shared by means of hybridization in convergence among closely-related ithomiine species. Repeated parallel evolution of regulatory switches via reuse of the same two genes suggests that convergent colour pattern evolution is highly constrained, even across large evolutionary timescales.

evolutionary biology↗

Phylogeny not mimicry drives chemical variation in tropical aposematic butterflies

Chemical signals serve a vast array of functions for both intra- and interspecific communication and defence. Chemically defended, aposematic insects will advertise their noxiousness to predators with warning signals and it has been suggested that volatile compounds shared between species could send a common signal to deter avian predators, similar to colour pattern mimicry. This is exemplified in the bright, mimetic warning colours of toxic heliconiine and ithomiine butterflies. Besides defence, males in these groups also use chemicals to communicate with potential female mates and male competitors. Here, we characterise chemical profiles of male Heliconiini and Ithomiini species from a range of mimicry rings. We find that chemical distances between species are not associated with mimicry and instead show a strong phylogenetic signal. In addition, we show that the distribution of specific shared compounds does not correlate with mimicry. We propose chemical signals in these groups are primarily used for intraspecific communication and highlight the potential selective mechanisms driving chemical profile evolution, such as selection for species-specific pheromone concentrations and collective male deterrent compounds. Our findings imply that chemical profile variation among butterfly species is the product of shared ancestry. However, more research is required on the behavioural significance of compounds among butterflies and predator perception of olfactory warning signals to identify which selective pressures are exerted on specific chemical traits.

evolutionary biology↗

Pollen-feeding delays reproductive senescence and maintains toxicity of Heliconius butterflies

Dietary shifts may act to ease energetic constraints and allow organisms to optimise life-history traits. Heliconius butterflies differ from other nectar-feeders due to their unique ability to digest pollen, which provides a reliable source of amino acids to adults. Pollen-feeding has been associated with prolonged adult lifespan and increased fertility, yet there is a lack of empirical data demonstrating how pollen consumption influences key fitness traits, including chemical defences and adult body weight, as well as fertility over their elongated lifespan. Here, we investigated the effect of pollen-feeding on fertility, weight and chemical defences, as well as offspring defences, controlling for butterfly age and sex. Recently emerged Heliconius erato butterflies of similar size were fed for 14 or 45 days on one of three diets: sugar solution only, or sugar solution replenished with either amino acid supplement or pollen. At the end of the experiment, oviposition assays were performed to evaluate fertility, and afterwards all butterflies and eggs were weighed and used for quantification of cyanogenic glucosides (CG). We found that there is an age-specific and sex-specific effect of pollen-feeding on butterfly weight, with both the sugar-only and amino-acid supplement diets reducing the weight of old females (45d), but not young females (14d) or males of any age. Females fed only sugar significantly reduced their egg-laying through adulthood, whereas females that had access to pollen maintained their fertility. Diet had a significant effect on the maintenance of the chemical defence of females, but not males. Curiously, even though females that have access to pollen were heavier, more toxic and laid more eggs, this did not translate into improvements in offspring defences, as eggs from butterflies of all ages and diet treatments had similar CG content. Our results emphasise the importance of controlling for age-specific and sex-specific effects in studies of life-history evolution and demonstrate that dietary novelty can relax energetic constraints.

evolutionary biology↗

The evolution of novel biotic interactions at ecological margins in response to climate change involves alleles from across the geographical range of the UK Brown Argus butterfly

Understanding the rate and extent to which populations can adapt to novel environments at their ecological margins is fundamental to predicting the persistence of biological communities during ongoing and rapid global change. Recent range expansion in response to climate change in the UK butterfly Aricia agestis is associated with the evolution of novel interactions with a larval food plant, and the loss of its ability to use its ancestral larval host species. Using ddRAD analysis of 61210 variable SNPs from 261 females from throughout the UK range of this species, we identify genomic regions at multiple chromosomes that are associated with these evolutionary responses, and their association with demographic history and ecological variation. Gene flow appears widespread throughout the range, despite the apparently fragmented nature of the habitats used by this species. Patterns of haplotype variation between selected and neutral genomic regions suggest that evolution associated with climate adaptation is polygenic, resulting from the independent spread of existing alleles throughout the established range of this species, rather than the colonisation of pre-adapted genotypes from coastal populations. These data suggest that rapid responses to climate change do not depend on the availability of pre-adapted genotypes. Instead, the evolution of novel forms of biotic interaction in Aricia agestis has occurred during range expansion, through the assembly of novel genotypes from alleles from multiple localities.

evolutionary biology↗

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 known and diverse, natural histories, can help understand how different selection pressures shape diverging traits. In butterflies, wing colour patterns have been extensively studied, whereas wing shape diversity is less well understood despite its importance for flight. Here we study a measure of wing shape, aspect ratio, and wing size in a large dataset of over 3200 individuals, representing 13 Heliconius species, from across the Neotropics. We assess the relative importance of phylogenetic relatedness, natural history and habitat in determining wing shape and size. We find that both larval and adult behavioural ecology affect patterns of adult size dimorphisms. On one hand, species with solitary larvae have larger adult males, in contrast to gregarious Heliconius species, and indeed most Lepidoptera. On the other hand, species in the pupal-mating clade are smaller overall than those in the adult-mating clade. Interestingly, while controlling for phylogeny, sex ratios and allometry, we find that species inhabiting higher altitudes have rounder wings and, in one of the two major Heliconius clades, are also bigger in size than their lowland relatives. Thus, we reveal novel adaptive wing morphological divergence among Heliconius species beyond that imposed by natural selection on aposematic wing colouration. Our study highlights the value of phylogenetic comparative methods in study systems that have diverse and well-studied natural histories to disentangle the selection pressures shaping adaptive phenotypes.

evolutionary biology↗

Recombination rate variation shapes barriers to introgression across butterfly genomes

Hybridisation and introgression can dramatically alter the relationships among groups of species, leading to phylogenetic discordance across the genome and between populations. Introgression can also erode species differences over time, but selection against introgression at certain loci acts to maintain post-mating species barriers. Theory predicts that species barriers made up of many loci throughout the genome should lead to a broad correlation between introgression and recombination rate, which determines the extent to which selection on deleterious foreign alleles will affect neutral alleles at physically linked loci. Here we describe the variation in genealogical relationships across the genome among three species of Heliconius butterflies: H. melpomene, H. cydno and H. timareta, using whole genomes of 92 individuals, and ask whether this variation can be explained by heterogeneous barriers to introgression. We find that species relationships vary predictably at the chromosomal scale. By quantifying recombination rate and admixture proportions, we then show that rates of introgression are predicted by variation in recombination rate. This implies that species barriers are highly polygenic, with selection acting against introgressed alleles across most of the genome. In addition, long chromosomes, which have lower recombination rates, produce stronger barriers on average than short chromosomes. Finally, we find a consistent difference between two species pairs on either side of the Andes, which suggests differences in the architecture of the species barriers. Our findings illustrate how the combined effects of hybridisation, recombination and natural selection, acting at multitudes of loci over long periods, can dramatically sculpt the phylogenetic relationships among species.

evolutionary biology↗

Genetic dissection of assortative mating behavior

The evolution of new species is made easier when traits under divergent ecological selection are also mating cues. Such ecological mating cues are now considered more common than previously thought, but we still know little about the genetic changes underlying their evolution, or more generally about the genetic basis for assortative mating behaviors. The warning patterns of Heliconius melpomene and H. cydno are under disruptive selection due to increased predation of non-mimetic hybrids, and are used during mate recognition. We carried out a genome-wide quantitative trait locus (QTL) analysis of preference behaviors between these species and showed that divergent male preference has a simple genetic basis. Three QTLs each explain a large proportion of the differences in preference behavior observed between the parental species. Two of these QTLs are on chromosomes with major color pattern genes, including one that is tightly associated with the gene optix. Different loci influence different aspects of attraction, suggesting that behavioral isolation in Heliconius involves the evolution of independently segregating modules, similar to those for the corresponding wing pattern cues. Hybridization and subsequent sharing of wing pattern loci has played an important role during adaptation and speciation in Heliconius butterflies. The existence of large effect preference loci could similarly assist the evolution of novel behavioral phenotypes through recombination and introgression, and should facilitate rapid speciation.

evolutionary biology↗

Patternize: An R Package For Quantifying Color Pattern Variation

O_LIThe use of image data to quantify, study and compare variation in the colors and patterns of organisms requires the alignment of images to establish homology, followed by color-based segmentation of images. Here we describe an R package for image alignment and segmentation that has applications to quantify color patterns in a wide range of organisms.\nC_LIO_LIpatternize is an R package that quantifies variation in color patterns obtained from image data. patternize first defines homology between pattern positions across specimens either through manually placed homologous landmarks or automated image registration. Pattern identification is performed by categorizing the distribution of colors using an RGB threshold, k-means clustering or watershed transformation.\nC_LIO_LIWe demonstrate that patternize can be used for quantification of the color patterns in a variety of organisms by analyzing image data for butterflies, guppies, spiders and salamanders. Image data can be compared between sets of specimens, visualized as heatmaps and analyzed using principal component analysis (PCA).\nC_LIO_LIpatternize has potential applications for fine scale quantification of color pattern phenotypes in population comparisons, genetic association studies and investigating the basis of color pattern variation across a wide range of organisms.\nC_LI

bioinformatics↗