The evolution and diversification of oakleaf butterflies

Cell, Journal Year: 2022, Volume and Issue: 185(17), P. 3138 - 3152.e20

Published: Aug. 1, 2022

Language: Английский

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High level of novelty under the hood of convergent evolution

Science, Journal Year: 2023, Volume and Issue: 379(6636), P. 1043 - 1049

Published: March 10, 2023

Little is known about the extent to which species use homologous regulatory architectures achieve phenotypic convergence. By characterizing chromatin accessibility and gene expression in developing wing tissues, we compared architecture of convergence between a pair mimetic butterfly species. Although handful color pattern genes are be involved their convergence, our data suggest that different mutational paths underlie integration these into development. This supported by large fraction accessible being exclusive each species, including de novo lineage-specific evolution modular optix enhancer. These findings may explained high level developmental drift evolutionary contingency occurs during independent mimicry.

Language: Английский

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

eLife, Journal Year: 2021, Volume and Issue: 10

Published: July 19, 2021

In Heliconius butterflies, wing colour pattern diversity and scale types are controlled by a few genes of large effect that regulate switches between morphs species across mimetic radiation. One these genes, cortex, has been repeatedly associated with evolution in butterflies. Here we carried out CRISPR knockouts multiple show cortex is major determinant cell identity. Chromatin accessibility profiling introgression scans identified cis-regulatory regions discrete phenotypic switches. perturbation black hindwing genotypes recreated yellow bar, revealing their spatially limited activity. the H. melpomene/timareta lineage, candidate CRE from yellow-barred phenotype interrupted transposable element, suggesting structural variation underlies adaptations. Our work shows functionally controls fate its control switch modular pattern-specific fashion.Heliconius butterflies have bright patterns on wings tell potential predators they toxic. As result, learn to avoid eating them. Over time, unrelated evolved similar predation through process known as Müllerian mimicry. Worldwide, there over 180,000 moths, most which different patterns. How do create this diversity? And use patterns? involved creating called cortex. This gene region DNA around it does not code for proteins, but instead, whether or off parts wing. Changes non-coding can act like switches, turning into colours complex patterns, unclear how evolved. Butterfly get tiny structures scales, each own unique set pigments. three scales: yellow/white red/orange/brown scales. Livraghi et al. used editing technique find affects type. First, confirmed deleting turned red scales yellow. Next, same manipulate see pattern. manipulation black-winged butterfly band, occurs naturally The next step was mutation responsible appearance bands nature. It turns bit extra genetic code, derived so-called ‘jumping genes’, had inserted itself gene, ‘flipping’ leading Genetic information contains instructions generate shape form organisms. These evolve millions years, everything bacteria blue whales. visual evidence evolution, way new isn't specific Understanding help researchers other too.

Language: Английский

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Association mapping of colour variation in a butterfly provides evidence that a supergene locks together a cluster of adaptive loci

Philosophical Transactions of the Royal Society B Biological Sciences, Journal Year: 2022, Volume and Issue: 377(1856)

Published: June 13, 2022

Supergenes are genetic architectures associated with discrete and concerted variation in multiple traits. It has long been suggested that supergenes control these complex polymorphisms by suppressing recombination between sets of coadapted genes. However, because suppression hinders the dissociation individual effects genes within supergenes, there is still little evidence evolve tightening linkage Here, combining a landmark-free phenotyping algorithm multivariate genome-wide association studies, we dissected basis wing pattern butterfly Heliconius numata . We show supergene controlling striking polymorphism displayed this species contains several independent loci different features patterns. The three chromosomal inversions suppress loci, supporting hypothesis they may have evolved captured beneficial combinations alleles. Some are, however, colour variations only subset morphs where phenotype controlled derived inversion forms, indicating were recruited after formation inversions. Our study shows clusters adaptive general form via evolution rearrangements co-adapted but also subsequent recruitment linked mutations. This article part theme issue ‘Genomic architecture supergenes: causes evolutionary consequences’.

Language: Английский

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A micro-RNA is the effector gene of a classic evolutionary hotspot locus

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: Feb. 12, 2024

In Lepidoptera (butterflies and moths), a genomic region around the gene cortex is hotspot locus, repeatedly used to generate intraspecific melanic wing color polymorphisms across 100-million-years of evolution. However, identity effector regulating within this locus remains unknown. Here, we show that none four candidate protein-coding genes including cortex, serve as major effectors. Instead, micro-RNA (miRNA), mir-193, serves three deeply diverged lineages butterflies, its function conserved in Drosophila. Lepidoptera, mir-193 derived from gigantic long non-coding RNA, ivory, it functions by directly repressing multiple pigmentation genes. We miRNA can drive repeated instances adaptive evolution animals.

Language: Английский

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A long noncoding RNA at the cortex locus controls adaptive coloration in butterflies

Proceedings of the National Academy of Sciences, Journal Year: 2024, Volume and Issue: 121(36)

Published: Aug. 30, 2024

Evolutionary variation in the wing pigmentation of butterflies and moths offers striking examples adaptation by crypsis mimicry. The

Language: Английский

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Antennapedia and optix regulate metallic silver wing scale development and cell shape in Bicyclus anynana butterflies

Cell Reports, Journal Year: 2022, Volume and Issue: 40(1), P. 111052 - 111052

Published: July 1, 2022

Butterfly wing scales can develop intricate cuticular nanostructures that produce silver colors, but the underlying genetic and physical basis of such colors is mostly unexplored. Here, we characterize different types wild-type in Bicyclus anynana butterflies show varying thickness air layer between two laminas most important for producing silvery broadband reflectance. We then address function five genes—apterous A, Ultrabithorax, doublesex, Antennapedia, optix—in scale development by examining crispants with either ectopic gains or losses scales. Simultaneous transformations three parameters—loss upper lamina, increased lower lamina thickness, pigmentation—occur when become brown vice versa silver. Antennapedia optix are high-level regulators determine cell shape both sexes. Moreover, involved determining ridge crossrib orientation.

Language: Английский

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Functional genomic tools for emerging model species

Trends in Ecology & Evolution, Journal Year: 2022, Volume and Issue: 37(12), P. 1104 - 1115

Published: July 30, 2022

Understanding the molecular mechanisms underlying phenotypic evolution is a central goal in evolutionary biology.Unfortunately, causal associations between candidate loci and phenotype are rarely established because majority of never validated with functional tools.We describe latest developments use tools, particularly RNAi clustered regularly interspaced palindromic repeats (CRISPR)-Cas, to establish links genotype phenotype, discuss some methodological challenges when applying these tools that unique emerging model organisms.Specifically, we highlight significant issue current studies ecology biology date recapitulate ecologically relevant variation, suggest gene editing species should make more HDR pathway obtain insights thereby deeper understanding genetic basis traits. Most field aiming connect validate identified using tools. Recent RNA interference (RNAi) (CRISPR)-Cas genome have dramatically increased feasibility validation. However, methods come specific applied organisms, including limited spatial control silencing, low knock-in efficiencies, throughput Moreover, many do not this limits their scope for into processes. We therefore argue by allelic replacement through homology-directed repair (HDR) would greatly benefit evolution. A fundamental aim identify genomic variation underlies micro- macroevolutionary dynamics [1.Vitti J.J. et al.Detecting natural selection data.Annu. Rev. Genet. 2013; 47: 97-120Crossref PubMed Scopus (397) Google Scholar]. In present post-genomic era, diverse datasets routinely used purpose organisms (see Glossary), ranging from genome-wide population data various association approaches differential expression analysis chromatin accessibility assays [2.Jamann T.M. al.QTL mapping high-throughput sequencing.in: Alonso J.M. Stepanova A.N. Plant Functional Genomics: Methods Protocols. Springer, 2015: 257-285Crossref (20) Scholar,3.van der Burg K.R.L. al.Genomic architecture genetically assimilated seasonal color pattern.Science. 2020; 370: 721-725Crossref (24) Although such advancing our genotype–phenotype relationships traits involved adaptation speciation [3.van Scholar,4.Pardo-Diaz C. al.Towards identification adaptive evolution.Methods Ecol. Evol. 2015; 6: 445-464Crossref (93) Scholar], they also clear limitations, most obvious being lack ability rigorous inferences phenotypes genes or loci. manipulating function, as (CRISPR)–CRISPR-associated protein (Cas), recent years made it possible link organisms. review address growing need inferences, practical aspects validation future role CRISPR-Cas technologies evolution, strong emphasis on challenge importance establishing ecological relevance Rather than investing validation, genomics hasinstead predominantly resulted an increase sample sizes individuals, populations, quest speciation. The result ever-increasing number that, after identifying (e.g., tests selection, allele-frequency patterns, mapping, linkage analysis, transcriptomic studies), at length potential implications. These all inherent (reviewed [5.Schielzeth H. al.Success failure replication associations: How does help outbred populations?.Mol. Resour. 2018; 18: 739-754Crossref (19) Scholar, 6.Liu Y. al.On dependency cellular levels mRNA abundance.Cell. 2016; 165: 535-550Abstract Full Text PDF (1576) 7.Schielzeth Husby A. Challenges prospects quantitative trait standing populations.Ann. N. Acad. Sci. 2014; 1320: 35-57Crossref (41) 8.Wellenreuther M. Hansson B. Detecting polygenic evolution: problems, pitfalls, promises.Trends TIG. 32: 155-164Abstract (84) Scholar]), but common them limitation phenotype. Drawing conclusions body evidence challenging, interpretations be considered carefully attempting understand relationship. Given circumstances, raise two worth considering investigating First, although acknowledge implementation even desirable instances, wish stress absence proper allowing avoiding language. Imprecise language degrades insights, impedes how world works, bloats false positive results [9.Siddiq M.A. al.Experimental test refutation classic case Drosophila melanogaster.Nat. 2017; 1: 25Crossref (21) Second, relying upon existing annotations without perpetuates bias. Consider hypothetical scenario, wherein intersection SNP trait, where variants associated near coding sequences several differentially expressed genes. resulting list assessed, hypotheses formed based sequence element annotations, which turn overwhelmingly closest organism melanogaster insects, mouse Mus musculus mammals, zebrafish Danio rerio fish, Saccharomyces cerevisiae yeast, Arabidopsis thaliana plants, so on). note duality approach: seems sound way forward homologous share functions over deep time, approach necessary no other possible, comes risk erroneous inferences. Model only important unknown function [10.Wu al.CRISPR/Cas9 mediated resource kinase phosphatase Drosophila.Sci. Rep. 10: 7383Crossref (3) Scholar] certainly change time orthologous [11.Verster A.J. al.Comparative screens elegans briggsae reveal impact developmental system drift function.PLoS 10e1004077Crossref Thus, solely annotation can restrict detect lineage-specific genes, moonlighting proteins, cases co-option evolved shape interest, especially subsequent changes alter biological [12.Tomczak al.Interpretation experiments Gene Ontology its annotations.Sci. 8: 5115Crossref (66) Equally problematic, selecting generates ascertainment bias assigned almost always avoided, though species-specific clearly magnitude problem huge ramifications vast – Homo sapiens <10% been focus >90% published papers [13.Stoeger T. al.Large-scale investigation reasons why potentially ignored.PLoS Biol. 16e2006643Crossref (125) bias, well aforementioned issues, demonstrate empowerment able functionally irrespective whether annotations. study van al. exemplifies issues elegance, authors investigated assimilation plasticity butterfly wing coloration, arriving 13 intersecting (GWAS) RNA-seq time-series results. They then manipulate four Knockout (KO) first choice, locus annotated wing-pattern (cortex), predictably affected color. Of one had effect (Dscam3) whereas did (trehalase). Finally, KO uncharacterized unannotated demonstrated causally coloration plasticity, was named herfst. Had chosen cortex, novel missed, (the metabolic trehalase) has unpredicted patterning. conducted neuronal Dscam3 patterning might generated line inquiry fact lacks support, trehalase possibly discounted. discovery herfst provides knowledge allows reanalysis previous work. With components types will synergistically improve across broader taxonomical range interest field. Establishing necessity stepwise process requires determination effort. amenable manipulation, others accomplished scale months, led impressive proliferation insightful knockdown techniques explore candidates were previously association-based [14.Klaassen al.CRISPR mutagenesis confirms oca2 melanin pigmentation Astyanax mexicanus.Dev. 441: 313-318Crossref (59) 15.Li X. al.Outbred sequencing CRISPR/Cas9 butterflies.Nat. Commun. 8212Crossref (133) 16.Mazo-Vargas al.Macroevolutionary shifts WntA potentiate diversity.Proc. Natl. U. S. 114: 10701-10706Crossref (99) 17.Santos M.E. al.Taxon-restricted origin access new environment.Science. 358: 386-390Crossref (56) 18.Woronik al.A transposable insertion alternative life history strategy.Nat. 2019; 5757Crossref (28) 19.Wucherpfennig J.I. al.Efficient CRISPR-Cas9 major sticklebacks.Evol. Res. 20: 107-132PubMed 20.Zhang L. al.Single master regulatory coordinates development iridescence.Proc. 10707-10712Crossref (97) taxonomically diverse, confirming butterflies [15.Li Scholar,16.Mazo-Vargas Scholar,20.Zhang albinism cave fish describing habitats water striders [17.Santos findings benefits bringing realm possibility behind processes documented populations difficult include phenomena migration [21.Zhan al.The genetics monarch warning colouration.Nature. 514: 317-321Crossref (186) exaggeration [22.Toubiana W. Khila Fluctuating strength intense male competition underlie strider's weapon.Proc. 28620182400PubMed innovations [23.Wagner G.P. Lynch V.J. Evolutionary novelties.Curr. 2010; R48-R52Abstract (184) polyphenisms [24.Casasa al.Nutrition-responsive insect polyphenism.Nat. 4: 970-978Crossref (17) name few. technique artificially downregulate assess level. downregulation occurs temporarily usually referred reduces rather eliminates production, opposed KO. largely relies proteins endogenous small pathways microRNA, interfering RNA, Piwi-interacting RNA) eukaryotic lineages [25.Shabalina S.A. Koonin E.V. Origins interference.Trends 2008; 23: 578-587Abstract (364) taxa highly divergent complex [26.Chapman E.J. Carrington J.C. Specialization pathways.Nat. 2007; 884-896Crossref (557) exogenously induced follow simplified conserved mechanism (Box 1) makes (although there notable exceptions; e.g., Lepidoptera [27.Terenius O. al.RNA Lepidoptera: overview successful unsuccessful implications experimental design.J. Insect Physiol. 2012; 57: 231-245Crossref (639) Scholar]).Box 1The nature enables sequence-specific knockdownsThe discovered plants Caenorhabditis [78.Fire al.Potent double-stranded elegans.Nature. 1998; 391: 806-811Crossref (12060) Scholar,79.Hamilton Baulcombe D.C. antisense posttranscriptional silencing plants.Science. 1999; 286: 950-952Crossref (2373) researchers observed reduction introduced (dsRNA) (asRNA) cells whole Research different systems since elucidated [80.Wilson R.C. Doudna J.A. Molecular interference.Annu. Biophys. 42: 217-239Crossref (732) core initiated cleavage dsRNA endonuclease Dicer smaller 20–25 nt fragments [81.Bernstein E. al.Role bidentate ribonuclease initiation step interference.Nature. 2001; 409: 363-366Crossref (3854) From fragments, strands associate Argonaut family and, together additional factors, form RNA-induced (RISC) [82.Hammond S.M. al.An RNA-directed nuclease mediates post-transcriptional cells.Nature. 2000; 404: 293-296Crossref (2443) Based RISC recognizes binds molecules interferes direct endonucleolytic cleavage, translational repression, directing formation heterochromatin corresponding [45.Podolska K. Svoboda P. Targeting living mammals interference.Brief. Funct. Genomics. 2011; 238-247Crossref (12) Scholar].The dependent transport cytosol described above initiated. groups efficient, vertebrates, cell membranes occur easily. cases, introduction aided exogenous agents viral vectors electroporation, delivering vehicle cationic lipids microinjection, solution injected directly tissue. This method efficient transport, systemic RNAi. strategy can, large extent, guided nearest organism. Apart generally broad applicability taxa, advantages stages tissue localization, both minimize negative pleiotropic effects. Further, tuned controlling dose completely ablated [28.Killiny al.Double-stranded uptake topical application, five CYP4 suppresses insecticide resistance Diaphorina citri.PLoS One. 9e110536Crossref (116) Scholar,29.Refki P.N. al.Emergence sensitivity Hox morphological trait.Dev. 392: 441-453Crossref (27) thus enabling survival phenotyping infer function. For example, insulin receptor polyphenism revealed [30.Xu H.J. al.Two receptors determine morphs planthoppers.Nature. 519: 464-467Crossref (308) alleles cause embryonic lethality homozygous state [31.Zhao al.Mutations NlInR1 affect normal growth lifespan brown planthopper Nilaparvata lugens.Insect Biochem. Mol. 115103246Crossref [32.Zhang C.-X. al.Molecular polymorphism insects.Annu. Entomol. 64: 297-314Crossref (64) studied classical large-scale normally [33.Liu al.Whole-animal screen identifies networks regulating germline stem Drosophila.Nat. 7: 12149Crossref Scholar,34.Wang G. al.RNAi tuning, microfluidic screening, recombineering improved production cerevisiae.Proc. 116: 9324-9332Crossref (37) tens [35.Toubiana factor BMP11 required exaggerated weapon fighting behavior strider.PLoS 2021; 19e3001157Crossref (6) Efficient rely overcoming hurdle organism, done time-consuming microinjections, targeting modest set (less ~50) achievable microinjection Scholar,35.Toubiana Some feeding [36.Feng D. Interference ingested dsRNA-expressing bacteria shell biosynthesis Crassostrea gigas.Mar. Biotechnol. 21: 526-536Crossref (23) Scholar,37.Whyard al.Ingested RNAs act insecticides.Insect 2009; 39: 824-832Crossref (456) time-efficient knockdowns [38.Forsthoefel D.J. reveals intestinal regulators branching morphogenesis, differentiation, planarians.Dev. Cell. 691-704Abstract (94) addition RNAi, application insects [39.Wang al.Second-generation supply effective targets pest control.PLoS 6e18644Google underutilized screens. One obstacle efficiency delivery within treated individual varies [40.Vogel insects: protecting beneficials pests.Front. 9: 1912Crossref (107) generating necessitates larger sizes. Another drawback lacking administration difficult. vertebrates resort via [41.Schepers Practice: Principles, Basics, Silencing elegans, Drosophila, Mammals. John Wiley & Sons,

Language: Английский

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A long non-coding RNA at thecortexlocus controls adaptive colouration in butterflies

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: Feb. 12, 2024

Abstract Evolutionary variation in the wing pigmentation of butterflies and moths offers striking examples adaptation by crypsis mimicry. The cortex locus has been independently mapped as controlling colour polymorphisms 14 lepidopteran species, suggesting it acts a genomic hotspot for diversification patterns, but functional validation through protein-coding knockouts proven difficult to obtain. Our study unveils role novel long non-coding RNA (lncRNA) which we name ivory , transcribed from locus, modulating patterning butterflies. Strikingly, expression prefigures most melanic patterns during pupal development, an early developmental specifying scale identity. To test this, generated CRISPR mosaic knock-outs five nymphalid butterfly species show that mutagenesis yields transformations dark pigmented scales into white or light-coloured scales. Genotyping Vanessa cardui germline mutants associates these phenotypes small on-target deletions at conserved first exon . In contrast, mutant with confirmed null alleles lack any phenotype, exclude this adjacent gene. Overall, results lncRNA master switch pattern specification, played key roles adaptive Significance statement Deciphering genetic underpinnings is fundamental comprehensive understanding evolutionary processes. Long RNAs (lncRNAs) represent emerging category modulators within genome, yet they have overlooked source phenotypic diversity. study, unveil pivotal orchestrating transitions between light development. Remarkably, gene nested region known control multiple cases moths, including iconic natural selection. These findings highlight significant influence lncRNAs regulation, also underscore their potential players process itself.

Language: Английский

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TheivorylncRNA regulates seasonal color patterns in buckeye butterflies

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: Feb. 12, 2024

Abstract Long non-coding RNAs (lncRNAs) are transcribed elements increasingly recognized for their roles in regulating gene expression. Thus far, however, we have little understanding of how lncRNAs contribute to evolution and adaptation. Here show that a conserved lncRNA, ivory , is an important color patterning the buckeye butterfly Junonia coenia . overlaps with cortex locus linked multiple cases crypsis mimicry Lepidoptera. Along companion paper by Livraghi et. al., argue not pattern interest at this locus. In J. cluster cis -regulatory (CREs) first intron genetically associated natural variation seasonal plasticity, targeted deletions these CREs phenocopy phenotypes. Deletions different produce other distinct phenotypes as well, including loss melanic eyespot rings, positive negative changes overall wing pigmentation. We transcription factors Spineless, Bric-a-brac, Ftz-f1 bind promoter during development, suggesting they directly regulate This case study demonstrates -regulation single RNA can exert diverse nuanced effects on development patterns, modulating seasonally plastic patterns. Significance The genomic hosting has been numerous adaptation moths butterflies, crypsis, mimicry, polyphenism. butterflies actual evolutionarily long (lncRNA), dubbed Compared genes, stands out because highly nuanced, quantitative pigmentation be achieved manipulating adjacent sequences. highlights underlying morphological evolution, emphasizes importance considering transcripts comparative genomics.

Language: Английский

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