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1.
Proc Natl Acad Sci U S A ; 121(36): e2403326121, 2024 Sep 03.
Artigo em Inglês | MEDLINE | ID: mdl-39213180

RESUMO

Evolutionary variation in the wing pigmentation of butterflies and moths offers striking examples of adaptation by crypsis and mimicry. The cortex locus has been independently mapped as the locus controlling color polymorphisms in 15 lepidopteran species, suggesting that it acts as a genomic hotspot for the diversification of wing patterns, but functional validation through protein-coding knockouts has proven difficult to obtain. Our study unveils the role of a long noncoding RNA (lncRNA) which we name ivory, transcribed from the cortex locus, in modulating color patterning in butterflies. Strikingly, ivory expression prefigures most melanic patterns during pupal development, suggesting an early developmental role in specifying scale identity. To test this, we generated CRISPR mosaic knock-outs in five nymphalid butterfly species and show that ivory mutagenesis yields transformations of dark pigmented scales into white or light-colored scales. Genotyping of Vanessa cardui germline mutants associates these phenotypes to small on-target deletions at the conserved first exon of ivory. In contrast, cortex germline mutant butterflies with confirmed null alleles lack any wing phenotype and exclude a color patterning role for this adjacent gene. Overall, these results show that a lncRNA gene acts as a master switch of color pattern specification and played key roles in the adaptive diversification of wing patterns in butterflies.


Assuntos
Borboletas , Pigmentação , RNA Longo não Codificante , Asas de Animais , Animais , Borboletas/genética , Pigmentação/genética , Asas de Animais/anatomia & histologia , Asas de Animais/crescimento & desenvolvimento , RNA Longo não Codificante/genética , Fenótipo , Adaptação Fisiológica/genética
2.
Elife ; 122024 Jan 23.
Artigo em Inglês | MEDLINE | ID: mdl-38261357

RESUMO

Hox gene clusters encode transcription factors that drive regional specialization during animal development: for example the Hox factor Ubx is expressed in the insect metathoracic (T3) wing appendages and differentiates them from T2 mesothoracic identities. Hox transcriptional regulation requires silencing activities that prevent spurious activation and regulatory crosstalks in the wrong tissues, but this has seldom been studied in insects other than Drosophila, which shows a derived Hox dislocation into two genomic clusters that disjoined Antennapedia (Antp) and Ultrabithorax (Ubx). Here, we investigated how Ubx is restricted to the hindwing in butterflies, amidst a contiguous Hox cluster. By analysing Hi-C and ATAC-seq data in the butterfly Junonia coenia, we show that a Topologically Associated Domain (TAD) maintains a hindwing-enriched profile of chromatin opening around Ubx. This TAD is bordered by a Boundary Element (BE) that separates it from a region of joined wing activity around the Antp locus. CRISPR mutational perturbation of this BE releases ectopic Ubx expression in forewings, inducing homeotic clones with hindwing identities. Further mutational interrogation of two non-coding RNA encoding regions and one putative cis-regulatory module within the Ubx TAD cause rare homeotic transformations in both directions, indicating the presence of both activating and repressing chromatin features. We also describe a series of spontaneous forewing homeotic phenotypes obtained in Heliconius butterflies, and discuss their possible mutational basis. By leveraging the extensive wing specialization found in butterflies, our initial exploration of Ubx regulation demonstrates the existence of silencing and insulating sequences that prevent its spurious expression in forewings.


Assuntos
Borboletas , Proteínas de Homeodomínio , Fatores de Transcrição , Animais , Borboletas/genética , Cromatina , Células Clonais , Repetições Palindrômicas Curtas Agrupadas e Regularmente Espaçadas , Reações Cruzadas , Proteínas de Homeodomínio/genética , Fatores de Transcrição/genética , Proteínas de Insetos/genética
3.
Artigo em Inglês | MEDLINE | ID: mdl-37948150

RESUMO

Quantification and reduction of uncertainty in deep-learning techniques have received much attention but ignored how to characterize the imprecision caused by such uncertainty. In some tasks, we prefer to obtain an imprecise result rather than being willing or unable to bear the cost of an error. For this purpose, we investigate the representation of imprecision in deep-learning (RIDL) techniques based on the theory of belief functions (TBF). First, the labels of some training images are reconstructed using the learning mechanism of neural networks to characterize the imprecision in the training set. In the process, a label assignment rule is proposed to reassign one or more labels to each training image. Once an image is assigned with multiple labels, it indicates that the image may be in an overlapping region of different categories from the feature perspective or the original label is wrong. Second, those images with multiple labels are rechecked. As a result, the imprecision (multiple labels) caused by the original labeling errors will be corrected, while the imprecision caused by insufficient knowledge is retained. Images with multiple labels are called imprecise ones, and they are considered to belong to meta-categories, the union of some specific categories. Third, the deep network model is retrained based on the reconstructed training set, and the test images are then classified. Finally, some test images that specific categories cannot distinguish will be assigned to meta-categories to characterize the imprecision in the results. Experiments based on some remarkable networks have shown that RIDL can improve accuracy (AC) and reasonably represent imprecision both in the training and testing sets.

4.
Evolution ; 77(12): 2619-2630, 2023 Dec 02.
Artigo em Inglês | MEDLINE | ID: mdl-37797261

RESUMO

Iridescent ultraviolet (IUV) patterns on pierid butterfly wings are phenotypic adaptations commonly used as sexual signals, generated by scales with ultrastructural modifications. Pierid IUV patterns are sexually dichromatic, with reduced size in females, where conspicuous sexual signaling balances courtship against ecological predation. There have been no phylogenetic reconstructions of IUV within Pieridae and little morphological characterization of phenotypic diversity. Our genus-wide characterization of IUV revealed the uniform similarity of stacked lamellar ridges on the dorsal surface of cover scales. We tested a hypothesis of single versus multiple origins by reconstructing a phylogeny of 534 species (~43.2% described species), with all genera represented, and a trait matrix of 734 species (~59.4%) screened for IUV. A single, early dimorphic origin of IUV followed by several losses and gains received strong support, concluding that IUV patterns and structural coloration are old traits. Collectively, these results support the homology of IUV scales and patterns that diversified within several lineages, suggesting an interplay between female-mediated sexual selection and ecological predatory selection.


Assuntos
Borboletas , Animais , Feminino , Borboletas/genética , Borboletas/anatomia & histologia , Filogenia , Asas de Animais/anatomia & histologia , Seleção Sexual , Fenótipo
5.
Nat Commun ; 14(1): 5620, 2023 09 12.
Artigo em Inglês | MEDLINE | ID: mdl-37699868

RESUMO

Heliconius butterflies, a speciose genus of Müllerian mimics, represent a classic example of an adaptive radiation that includes a range of derived dietary, life history, physiological and neural traits. However, key lineages within the genus, and across the broader Heliconiini tribe, lack genomic resources, limiting our understanding of how adaptive and neutral processes shaped genome evolution during their radiation. Here, we generate highly contiguous genome assemblies for nine Heliconiini, 29 additional reference-assembled genomes, and improve 10 existing assemblies. Altogether, we provide a dataset of annotated genomes for a total of 63 species, including 58 species within the Heliconiini tribe. We use this extensive dataset to generate a robust and dated heliconiine phylogeny, describe major patterns of introgression, explore the evolution of genome architecture, and the genomic basis of key innovations in this enigmatic group, including an assessment of the evolution of putative regulatory regions at the Heliconius stem. Our work illustrates how the increased resolution provided by such dense genomic sampling improves our power to generate and test gene-phenotype hypotheses, and precisely characterize how genomes evolve.


Assuntos
Borboletas , Animais , Tamanho do Genoma , Borboletas/genética , Genômica , Fenótipo , Filogenia
6.
Development ; 150(18)2023 Sep 15.
Artigo em Inglês | MEDLINE | ID: mdl-37602496

RESUMO

Butterfly color patterns provide visible and biodiverse phenotypic readouts of the patterning processes. Although the secreted ligand WntA has been shown to instruct the color pattern formation in butterflies, its mode of reception remains elusive. Butterfly genomes encode four homologs of the Frizzled-family of Wnt receptors. Here, we show that CRISPR mosaic knockouts of frizzled2 (fz2) phenocopy the color pattern effects of WntA loss of function in multiple nymphalids. Whereas WntA mosaic clones result in intermediate patterns of reduced size, fz2 clones are cell-autonomous, consistent with a morphogen function. Shifts in expression of WntA and fz2 in WntA crispant pupae show that they are under positive and negative feedback, respectively. Fz1 is required for Wnt-independent planar cell polarity in the wing epithelium. Fz3 and Fz4 show phenotypes consistent with Wnt competitive-antagonist functions in vein formation (Fz3 and Fz4), wing margin specification (Fz3), and color patterning in the Discalis and Marginal Band Systems (Fz4). Overall, these data show that the WntA/Frizzled2 morphogen-receptor pair forms a signaling axis that instructs butterfly color patterning and shed light on the functional diversity of insect Frizzled receptors.


Assuntos
Borboletas , Pigmentação , Animais , Pigmentação/genética , Borboletas/genética , Borboletas/metabolismo , Transdução de Sinais/genética , Receptores Frizzled/genética , Receptores Frizzled/metabolismo , Asas de Animais/metabolismo
7.
Cell Rep ; 42(8): 112820, 2023 08 29.
Artigo em Inglês | MEDLINE | ID: mdl-37481719

RESUMO

Continuous color polymorphisms can serve as a tractable model for the genetic and developmental architecture of traits. Here we investigated continuous color variation in Colias eurytheme and Colias philodice, two species of sulphur butterflies that hybridize in sympatry. Using quantitative trait locus (QTL) analysis and high-throughput color quantification, we found two interacting large-effect loci affecting orange-to-yellow chromaticity. Knockouts of red Malpighian tubules (red), likely involved in endosomal maturation, result in depigmented wing scales. Additionally, the transcription factor bric-a-brac can act as a modulator of orange pigmentation. We also describe the QTL architecture of other continuously varying traits, together supporting a large-X effect model where the genetic control of species-defining traits is enriched on sex chromosomes. This study sheds light on the range of possible genetic architectures that can underpin a continuously varying trait and illustrates the power of using automated measurement to score phenotypes that are not always conspicuous to the human eye.


Assuntos
Borboletas , Animais , Humanos , Borboletas/genética , Simpatria , Pigmentação/genética , Locos de Características Quantitativas/genética , Polimorfismo Genético , Asas de Animais
8.
Biol Rev Camb Philos Soc ; 98(4): 1250-1277, 2023 08.
Artigo em Inglês | MEDLINE | ID: mdl-37017088

RESUMO

Vertebrate pigmentation patterns are amongst the best characterised model systems for studying the genetic basis of adaptive evolution. The wealth of available data on the genetic basis for pigmentation evolution allows for analysis of trends and quantitative testing of evolutionary hypotheses. We employed Gephebase, a database of genetic variants associated with natural and domesticated trait variation, to examine trends in how cis-regulatory and coding mutations contribute to vertebrate pigmentation phenotypes, as well as factors that favour one mutation type over the other. We found that studies with lower ascertainment bias identified higher proportions of cis-regulatory mutations, and that cis-regulatory mutations were more common amongst animals harbouring a higher number of pigment cell classes. We classified pigmentation traits firstly according to their physiological basis and secondly according to whether they affect colour or pattern, and identified that carotenoid-based pigmentation and variation in pattern boundaries are preferentially associated with cis-regulatory change. We also classified genes according to their developmental, cellular, and molecular functions. We found a greater proportion of cis-regulatory mutations in genes implicated in upstream developmental processes compared to those involved in downstream cellular functions, and that ligands were associated with a higher proportion of cis-regulatory mutations than their respective receptors. Based on these trends, we discuss future directions for research in vertebrate pigmentation evolution.


Assuntos
Loci Gênicos , Vertebrados , Animais , Vertebrados/genética , Mutação , Pigmentação/genética , Fenótipo
9.
Sci Adv ; 9(12): eabq3713, 2023 03 22.
Artigo em Inglês | MEDLINE | ID: mdl-36947619

RESUMO

Understanding the evolutionary origins and factors maintaining alternative life history strategies (ALHS) within species is a major goal of evolutionary research. While alternative alleles causing discrete ALHS are expected to purge or fix over time, one-third of the ~90 species of Colias butterflies are polymorphic for a female-limited ALHS called Alba. Whether Alba arose once, evolved in parallel, or has been exchanged among taxa is currently unknown. Using comparative genome-wide association study (GWAS) and population genomic analyses, we placed the genetic basis of Alba in time-calibrated phylogenomic framework, revealing that Alba evolved once near the base of the genus and has been subsequently maintained via introgression and balancing selection. CRISPR-Cas9 mutagenesis was then used to verify a putative cis-regulatory region of Alba, which we identified using phylogenetic foot printing. We hypothesize that this cis-regulatory region acts as a modular enhancer for the induction of the Alba ALHS, which has likely facilitated its long evolutionary persistence.


Assuntos
Borboletas , Características de História de Vida , Animais , Feminino , Filogenia , Borboletas/genética , Estudo de Associação Genômica Ampla , Evolução Biológica
10.
Science ; 378(6617): 304-308, 2022 10 21.
Artigo em Inglês | MEDLINE | ID: mdl-36264807

RESUMO

Butterfly wing patterns derive from a deeply conserved developmental ground plan yet are diverse and evolve rapidly. It is poorly understood how gene regulatory architectures can accommodate both deep homology and adaptive change. To address this, we characterized the cis-regulatory evolution of the color pattern gene WntA in nymphalid butterflies. Comparative assay for transposase-accessible chromatin using sequencing (ATAC-seq) and in vivo deletions spanning 46 cis-regulatory elements across five species revealed deep homology of ground plan-determining sequences, except in monarch butterflies. Furthermore, noncoding deletions displayed both positive and negative regulatory effects that were often broad in nature. Our results provide little support for models predicting rapid enhancer turnover and suggest that deeply ancestral, multifunctional noncoding elements can underlie rapidly evolving trait systems.


Assuntos
Padronização Corporal , Borboletas , Elementos Facilitadores Genéticos , Regulação da Expressão Gênica no Desenvolvimento , Pigmentação , Asas de Animais , Animais , Borboletas/genética , Borboletas/crescimento & desenvolvimento , Pigmentação/genética , Asas de Animais/anatomia & histologia , Asas de Animais/crescimento & desenvolvimento , Padronização Corporal/genética , Loci Gênicos
11.
Biochem Mol Biol Educ ; 50(6): 605-619, 2022 11.
Artigo em Inglês | MEDLINE | ID: mdl-36054482

RESUMO

CRISPR is a technique increasingly used in the laboratory for both fundamental and applied research. We designed and implemented a lab experience for undergraduates to carry out CRISPR technology in the lab, and knockout the wing patterning genes optix and WntA in Vanessa cardui butterflies. Students obtained spectacular phenotypic mutants of butterfly wings color and patterns, awakening curiosity about how genomes encode morphology. In addition, students successfully used molecular techniques to genotype and screen wild-type caterpillar larvae and butterflies for CRISPR edits in genes. Student feedback suggests that they experienced a meaningful process of scientific inquiry by carrying out the whole CRISPR workflow process, from the design and delivery of CRISPR components through microinjection of butterfly eggs, the rearing of live animals through their complete life cycle, and molecular and phenotypic analyses of the resulting mutants. We discuss our experience using CRISP genome editing experiments in butterflies to expose students to hands-on research experiences probing gene-to-phenotype relationships in a charismatic and live organism.


Assuntos
Borboletas , Animais , Humanos , Borboletas/genética , Repetições Palindrômicas Curtas Agrupadas e Regularmente Espaçadas/genética , Pigmentação/genética , Asas de Animais/anatomia & histologia , Asas de Animais/fisiologia , Estudantes
12.
iScience ; 25(8): 104749, 2022 Aug 19.
Artigo em Inglês | MEDLINE | ID: mdl-35874096

RESUMO

[This corrects the article DOI: 10.1016/j.isci.2022.103885.].

13.
iScience ; 25(3): 103885, 2022 Mar 18.
Artigo em Inglês | MEDLINE | ID: mdl-35243245

RESUMO

The pantry moth Plodia interpunctella is a worldwide pest of stored food products and a promising laboratory model system for lepidopteran functional genomics. Here we describe efficient methods for precise genome editing in this insect. A spontaneous recessive white-eyed phenotype maps to a frameshift deletion (c.737delC) in the white gene. CRISPR NHEJ mutagenesis of white replicates this phenotype with high rates of somatic biallelic knockout. G0 individuals with mutant clones on both eyes produced 100% mutant progeny, making white an ideal marker for co-conversion when targeting other genes. CRISPR HDR experiments corrected c.737delC and reverted white eyes to a pigmented state in 37% of G0 mosaic adults. These repaired alleles showed practical rates of germline transmission in backcrosses, demonstrating the potential of the technique for precise genome editing. Plodia offers a promising avenue for research in this taxon because of its lab-ready features, egg injectability, and editability.

14.
J Exp Zool B Mol Dev Evol ; 338(6): 382-387, 2022 09.
Artigo em Inglês | MEDLINE | ID: mdl-35189035

RESUMO

Classical Drosophila eye color mutations have unearthed a toolkit of genes that have permitted candidate gene studies of the outstanding diversity of coloration patterns in other insects. The gene underlying the eye color phenotypes of the red Malphigian tubules (red) fly mutant was mapped to a LysM domain gene of unknown molecular function. Here, we used RNAi to test the role of a red ortholog in the pigmentation of the milkweed bug Oncopeltus fasciatus, and contrast its effect with the ommochrome biosynthetic pathway gene vermilion (ver). Pigmentation was reduced in the cuticle of embryonic legs and first instar abdomens following parental RNAi against red, but not against ver, likely reflecting an effect on pterin biogenesis. Nymphal RNAi of red and ver both resulted in adult eye depigmentation, consistent with an effect on ommochrome content. These results suggest red loss-of-function impacts biochemically distinct types of pigments, and we discuss its putative role in the biogenesis of lysosome-related organelles such as ommochromasomes and pterinosomes.


Assuntos
Heterópteros , Pigmentação , Animais , Drosophila/genética , Heterópteros/genética , Fenótipo , Pigmentação/genética , Interferência de RNA
15.
G3 (Bethesda) ; 12(4)2022 04 04.
Artigo em Inglês | MEDLINE | ID: mdl-35099556

RESUMO

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.


Assuntos
Borboletas , Animais , Borboletas/genética , Genoma , Fenótipo , Pigmentação/genética , Asas de Animais
16.
Proc Natl Acad Sci U S A ; 119(3)2022 01 18.
Artigo em Inglês | MEDLINE | ID: mdl-35012980

RESUMO

Mating cues evolve rapidly and can contribute to species formation and maintenance. However, little is known about how sexual signals diverge and how this variation integrates with other barrier loci to shape the genomic landscape of reproductive isolation. Here, we elucidate the genetic basis of ultraviolet (UV) iridescence, a courtship signal that differentiates the males of Colias eurytheme butterflies from a sister species, allowing females to avoid costly heterospecific matings. Anthropogenic range expansion of the two incipient species established a large zone of secondary contact across the eastern United States with strong signatures of genomic admixtures spanning all autosomes. In contrast, Z chromosomes are highly differentiated between the two species, supporting a disproportionate role of sex chromosomes in speciation known as the large-X (or large-Z) effect. Within this chromosome-wide reproductive barrier, linkage mapping indicates that cis-regulatory variation of bric a brac (bab) underlies the male UV-iridescence polymorphism between the two species. Bab is expressed in all non-UV scales, and butterflies of either species or sex acquire widespread ectopic iridescence following its CRISPR knockout, demonstrating that Bab functions as a suppressor of UV-scale differentiation that potentiates mating cue divergence. These results highlight how a genetic switch can regulate a premating signal and integrate with other reproductive barriers during intermediate phases of speciation.


Assuntos
Borboletas/genética , Borboletas/efeitos da radiação , Genes de Troca , Iridescência/genética , Enxofre/química , Raios Ultravioleta , Animais , Sistemas CRISPR-Cas/genética , Cromossomos/genética , Genes de Insetos , Loci Gênicos , Proteínas de Insetos/genética , Proteínas de Insetos/metabolismo , Iridescência/efeitos da radiação , Masculino , Comportamento Sexual Animal/fisiologia , Especificidade da Espécie , Simpatria/genética , Asas de Animais/metabolismo
17.
Front Genome Ed ; 4: 1074888, 2022.
Artigo em Inglês | MEDLINE | ID: mdl-36620082

RESUMO

While piggyBac transposon-based transgenesis is widely used in various emerging model organisms, its relatively low transposition rate in butterflies and moths has hindered its use for routine genetic transformation in Lepidoptera. Here, we tested the suitability of a codon-optimized hyperactive piggyBac transposase (hyPBase) in mRNA form to deliver and integrate transgenic cassettes into the genome of the pantry moth Plodia interpunctella. Co-injection of hyPBase mRNA with donor plasmids successfully integrated 1.5-4.4 kb expression cassettes driving the fluorescent markers EGFP, DsRed, or EYFP in eyes and glia with the 3xP3 promoter. Somatic integration and expression of the transgene in the G0 injected generation was detectable from 72-h embryos and onward in larvae, pupae and adults carrying a recessive white-eyed mutation. Overall, 2.5% of injected eggs survived into transgene-bearing adults with mosaic fluorescence. Subsequent outcrossing of fluorescent G0 founders transmitted single-insertion copies of 3xP3::EGFP and 3xP3::EYFP and generated stable isogenic lines. Random in-crossing of a small cohort of G0 founders expressing 3xP3::DsRed yielded a stable transgenic line segregating for more than one transgene insertion site. We discuss how hyPBase can be used to generate stable transgenic resources in Plodia and other moths.

18.
Mol Biol Evol ; 38(11): 5021-5033, 2021 10 27.
Artigo em Inglês | MEDLINE | ID: mdl-34323995

RESUMO

Sexually dimorphic development is responsible for some of the most remarkable phenotypic variation found in nature. Alternative splicing of the transcription factor gene doublesex (dsx) is a highly conserved developmental switch controlling the expression of sex-specific pathways. Here, we leverage sex-specific differences in butterfly wing color pattern to characterize the genetic basis of sexually dimorphic development. We use RNA-seq, immunolocalization, and motif binding site analysis to test specific predictions about the role of dsx in the development of structurally based ultraviolet (UV) wing patterns in Zerene cesonia (Southern Dogface). Unexpectedly, we discover a novel duplication of dsx that shows a sex-specific burst of expression associated with the sexually dimorphic UV coloration. The derived copy consists of a single exon that encodes a DNA binding but no protein-binding domain and has experienced rapid amino-acid divergence. We propose the novel dsx paralog may suppress UV scale differentiation in females, which is supported by an excess of Dsx-binding sites at cytoskeletal and chitin-related genes with sex-biased expression. These findings illustrate the molecular flexibility of the dsx gene in mediating the differentiation of secondary sexual characteristics.


Assuntos
Borboletas , Proteínas de Drosophila , Processamento Alternativo , Animais , Sítios de Ligação , Borboletas/genética , Borboletas/metabolismo , Proteínas de Drosophila/genética , Feminino , Masculino , Caracteres Sexuais , Asas de Animais
19.
Elife ; 102021 07 19.
Artigo em Inglês | MEDLINE | ID: mdl-34280087

RESUMO

In Heliconius butterflies, wing colour pattern diversity and scale types are controlled by a few genes of large effect that regulate colour pattern switches between morphs and species across a large mimetic radiation. One of these genes, cortex, has been repeatedly associated with colour pattern evolution in butterflies. Here we carried out CRISPR knockouts in multiple Heliconius species and show that cortex is a major determinant of scale cell identity. Chromatin accessibility profiling and introgression scans identified cis-regulatory regions associated with discrete phenotypic switches. CRISPR perturbation of these regions in black hindwing genotypes recreated a yellow bar, revealing their spatially limited activity. In the H. melpomene/timareta lineage, the candidate CRE from yellow-barred phenotype morphs is interrupted by a transposable element, suggesting that cis-regulatory structural variation underlies these mimetic adaptations. Our work shows that cortex functionally controls scale colour fate and that its cis-regulatory regions control a phenotypic switch in a modular and pattern-specific fashion.


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.


Assuntos
Borboletas/genética , Pigmentos Biológicos/genética , Asas de Animais/fisiologia , Animais , Repetições Palindrômicas Curtas Agrupadas e Regularmente Espaçadas , Cor , Fenótipo
20.
J Exp Zool B Mol Dev Evol ; 336(6): 470-481, 2021 09.
Artigo em Inglês | MEDLINE | ID: mdl-34010515

RESUMO

Wnt ligands are key signaling molecules in animals, but little is known about the evolutionary dynamics and mode of action of the WntA orthologs, which are not present in the vertebrates or in Drosophila. Here we show that the WntA subfamily evolved at the base of the Bilateria + Cnidaria clade, and conserved the thumb region and Ser209 acylation site present in most other Wnts, suggesting WntA requires the core Wnt secretory pathway. WntA proteins are distinguishable from other Wnts by a synapomorphic Iso/Val/Ala216 amino-acid residue that replaces the otherwise ubiquitous Thr216 position. WntA embryonic expression is conserved between beetles and butterflies, suggesting functionality, but the WntA gene was lost three times within arthropods, in podoplean copepods, in the cyclorrhaphan fly radiation, and in ensiferan crickets and katydids. Finally, CRISPR mosaic knockouts (KOs) of porcupine and wntless phenocopied the pattern-specific effects of WntA KOs in the wings of Vanessa cardui butterflies. These results highlight the molecular conservation of the WntA protein across invertebrates, and imply it functions as a typical Wnt ligand that is acylated and secreted through the Porcupine/Wntless secretory pathway.


Assuntos
Evolução Biológica , Borboletas/genética , Proteínas Wnt/genética , Via de Sinalização Wnt , Animais , Borboletas/crescimento & desenvolvimento , Proteína 9 Associada à CRISPR , Sistemas CRISPR-Cas , Ligantes , Filogenia , Asas de Animais/crescimento & desenvolvimento
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