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1. Cortex cis-regulatory switches establish scale colour identity and pattern diversity in Heliconius

   https://doi.org/10.7554/eLife.68549  

   Livraghi, Luca ; Hanly, Joseph J ; Van Bellghem, Steven M ; Montejo-Kovacevich, Gabriela ; van der Heijden, Eva SM ; Loh, Ling Sheng ; Ren, Anna ; Warren, Ian A ; Lewis, James J ; Concha, Carolina ; et al ( July 2021 , eLife)

   null (Ed.)

   Heliconius butterflies have bright patterns on their wings that tell potential predators that they are toxic. As a result, predators learn to avoid eating them. Over time, unrelated species of butterflies have evolved similar patterns to avoid predation through a process known as Müllerian mimicry. Worldwide, there are over 180,000 species of butterflies and moths, most of which have different wing patterns. How do genes create this pattern diversity? And do butterflies use similar genes to create similar wing patterns? One of the genes involved in creating wing patterns is called cortex . This gene has a large region of DNA around it that does not code for proteins, but instead, controls whether cortex is on or off in different parts of the wing. Changes in this non-coding region can act like switches, turning regions of the wing into different colours and creating complex patterns, but it is unclear how these switches have evolved. Butterfly wings get their colour from tiny structures called scales, which each have their own unique set of pigments. In Heliconius butterflies, there are three types of scales: yellow/white scales, black scales, and red/orange/brown scales. Livraghi et al. used a DNA editing technique called CRISPR to find out whether the cortex gene affects scale type. First, Livraghi et al. confirmed that deleting cortex turned black and red scales yellow. Next, they used the same technique to manipulate the non-coding DNA around the cortex gene to see the effect on the wing pattern. This manipulation turned a black-winged butterfly into a butterfly with a yellow wing band, a pattern that occurs naturally in Heliconius butterflies. The next step was to find the mutation responsible for the appearance of yellow wing bands in nature. It turns out that a bit of extra genetic code, derived from so-called ‘jumping genes’, had inserted itself into the non-coding DNA around the cortex gene, ‘flipping’ the switch and leading to the appearance of the yellow scales. Genetic information contains the instructions to generate shape and form in most organisms. These instructions evolve over millions of years, creating everything from bacteria to blue whales. Butterfly wings are visual evidence of evolution, but the way their genes create new patterns isn't specific to butterflies. Understanding wing patterns can help researchers to learn how genetic switches control diversity across other species too. 

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2. A large deletion at the cortex locus eliminates butterfly wing patterning

   https://doi.org/10.1093/g3journal/jkac021  

   Hanly, Joseph J. ; Livraghi, Luca ; Heryanto, Christa ; McMillan, W. Owen ; Jiggins, Chris D. ; Gilbert, Lawrence E. ; Martin, Arnaud ; Oliver, ed., B. ( January 2022 , G3 Genes|Genomes|Genetics)

   As the genetic basis of natural and domesticated variation has been described in recent years, a number of hotspot genes have been repeatedly identified as the targets of selection, Heliconius butterflies display a spectacular diversity of pattern variants in the wild and the genetic basis of these patterns has been well-described. Here, we sought to identify the mechanism behind an unusual pattern variant that is instead found in captivity, the ivory mutant, in which all scales on both the wings and body become white or yellow. Using a combination of autozygosity mapping and coverage analysis from 37 captive individuals, we identify a 78-kb deletion at the cortex wing patterning locus, a gene which has been associated with wing pattern evolution in H. melpomene and 10 divergent lepidopteran species. This deletion is undetected among 458 wild Heliconius genomes samples, and its dosage explains both homozygous and heterozygous ivory phenotypes found in captivity. The deletion spans a large 5′ region of the cortex gene that includes a facultative 5′UTR exon detected in larval wing disk transcriptomes. CRISPR mutagenesis of this exon replicates the wing phenotypes from coding knock-outs of cortex, consistent with a functional role of ivory-deleted elements in establishing scale color fate. Population demographics reveal that the stock giving rise to the ivory mutant has a mixed origin from across the wild range of H. melpomene, and supports a scenario where the ivory mutation occurred after the introduction of cortex haplotypes from Ecuador. Homozygotes for the ivory deletion are inviable while heterozygotes are the targets of artificial selection, joining 40 other examples of allelic variants that provide heterozygous advantage in animal populations under artificial selection by fanciers and breeders. Finally, our results highlight the promise of autozygosity and association mapping for identifying the genetic basis of aberrant mutations in captive insect populations.

    

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3. The roles of hybridization and habitat fragmentation in the evolution of Brazil’s enigmatic longwing butterflies, Heliconius nattereri and H. hermathena

   https://doi.org/10.1186/s12915-020-00797-1  

   Massardo, Darli ; VanKuren, Nicholas W. ; Nallu, Sumitha ; Ramos, Renato R. ; Ribeiro, Pedro G. ; Silva-Brandão, Karina L. ; Brandão, Marcelo M. ; Lion, Marília B. ; Freitas, André V. ; Cardoso, Márcio Z. ; et al ( December 2020 , BMC Biology)

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   Abstract Background Heliconius butterflies are widely distributed across the Neotropics and have evolved a stunning array of wing color patterns that mediate Müllerian mimicry and mating behavior. Their rapid radiation has been strongly influenced by hybridization, which has created new species and allowed sharing of color patterning alleles between mimetic species pairs. While these processes have frequently been observed in widespread species with contiguous distributions, many Heliconius species inhabit patchy or rare habitats that may strongly influence the origin and spread of species and color patterns. Here, we assess the effects of historical population fragmentation and unique biology on the origins, genetic health, and color pattern evolution of two rare and sparsely distributed Brazilian butterflies, Heliconius hermathena and Heliconius nattereri . Results We assembled genomes and re-sequenced whole genomes of eight H. nattereri and 71 H. hermathena individuals. These species harbor little genetic diversity, skewed site frequency spectra, and high deleterious mutation loads consistent with recent population bottlenecks. Heliconius hermathena consists of discrete, strongly isolated populations that likely arose from a single population that dispersed after the last glacial maximum. Despite having a unique color pattern combination that suggested a hybrid origin, we found no genome-wide evidence that H. hermathena is a hybrid species. However, H. hermathena mimicry evolved via introgression, from co-mimetic Heliconius erato , of a small genomic region upstream of the color patterning gene cortex . Conclusions Heliconius hermathena and H. nattereri population fragmentation, potentially driven by historical climate change and recent deforestation, has significantly reduced the genetic health of these rare species. Our results contribute to a growing body of evidence that introgression of color patterning alleles between co-mimetic species appears to be a general feature of Heliconius evolution. 

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4. A shared genetic basis of mimicry across swallowtail butterflies points to ancestral co-option of doublesex

   https://doi.org/10.1038/s41467-019-13859-y  

   Palmer, Daniela H. ; Kronforst, Marcus R. ( January 2020 , Nature Communications)

   Uncovering whether convergent adaptations share a genetic basis is consequential for understanding the evolution of phenotypic diversity. This information can help us understand the extent to which shared ancestry or independent evolution shape adaptive phenotypes. In this study, we first ask whether the same genes underlie polymorphic mimicry inPapilioswallowtail butterflies. By comparing signatures of genetic variation between polymorphic and monomorphic species, we then investigate how ancestral variation, hybridization, and independent evolution contributed to wing pattern diversity in this group. We report that a single gene,doublesex (dsx), controls mimicry across multiple taxa, but with species-specific patterns of genetic differentiation and linkage disequilibrium. In contrast to widespread examples of phenotypic evolution driven by introgression, our analyses reveal distinct mimicry alleles. We conclude that mimicry evolution in this group was likely facilitated by ancestral polymorphism resulting from early co-option ofdsxas a mimicry locus, and that evolutionary turnover ofdsxalleles may underlie the wing pattern diversity of extant polymorphic and monomorphic lineages.

    

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5. Divergence of chemosensing during the early stages of speciation

   https://doi.org/10.1073/pnas.1921318117  

   van Schooten, Bas ; Meléndez-Rosa, Jesyka ; Van Belleghem, Steven M. ; Jiggins, Chris D. ; Tan, John D. ; McMillan, W. Owen ; Papa, Riccardo ( July 2020 , Proceedings of the National Academy of Sciences)

   Chemosensory communication is essential to insect biology, playing indispensable roles during mate-finding, foraging, and oviposition behaviors. These traits are particularly important during speciation, where chemical perception may serve to establish species barriers. However, identifying genes associated with such complex behavioral traits remains a significant challenge. Through a combination of transcriptomic and genomic approaches, we characterize the genetic architecture of chemoperception and the role of chemosensing during speciation for a young species pair of Heliconius butterflies, Heliconius melpomene and Heliconius cydno . We provide a detailed description of chemosensory gene-expression profiles as they relate to sensory tissue (antennae, legs, and mouthparts), sex (male and female), and life stage (unmated and mated female butterflies). Our results untangle the potential role of chemical communication in establishing barriers during speciation and identify strong candidate genes for mate and host plant choice behaviors. Of the 252 chemosensory genes, HmOBP20 (involved in volatile detection) and HmGr56 (a putative synephrine-related receptor) emerge as strong candidates for divergence in pheromone detection and host plant discrimination, respectively. These two genes are not physically linked to wing-color pattern loci or other genomic regions associated with visual mate preference. Altogether, our results provide evidence for chemosensory divergence between H. melpomene and H. cydno , two rarely hybridizing butterflies with distinct mate and host plant preferences, a finding that supports a polygenic architecture of species boundaries. 

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