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A large deletion at the cortex locus eliminates butterfly wing patterning
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...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8982378/ https://www.ncbi.nlm.nih.gov/pubmed/35099556 http://dx.doi.org/10.1093/g3journal/jkac021 |
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author | Hanly, Joseph J Livraghi, Luca Heryanto, Christa McMillan, W Owen Jiggins, Chris D Gilbert, Lawrence E Martin, Arnaud |
author_facet | Hanly, Joseph J Livraghi, Luca Heryanto, Christa McMillan, W Owen Jiggins, Chris D Gilbert, Lawrence E Martin, Arnaud |
author_sort | Hanly, Joseph J |
collection | PubMed |
description | 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. |
format | Online Article Text |
id | pubmed-8982378 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-89823782022-04-05 A large deletion at the cortex locus eliminates butterfly wing patterning Hanly, Joseph J Livraghi, Luca Heryanto, Christa McMillan, W Owen Jiggins, Chris D Gilbert, Lawrence E Martin, Arnaud G3 (Bethesda) Investigation 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. Oxford University Press 2022-01-31 /pmc/articles/PMC8982378/ /pubmed/35099556 http://dx.doi.org/10.1093/g3journal/jkac021 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Genetics Society of America. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Investigation Hanly, Joseph J Livraghi, Luca Heryanto, Christa McMillan, W Owen Jiggins, Chris D Gilbert, Lawrence E Martin, Arnaud A large deletion at the cortex locus eliminates butterfly wing patterning |
title | A large deletion at the cortex locus eliminates butterfly wing patterning |
title_full | A large deletion at the cortex locus eliminates butterfly wing patterning |
title_fullStr | A large deletion at the cortex locus eliminates butterfly wing patterning |
title_full_unstemmed | A large deletion at the cortex locus eliminates butterfly wing patterning |
title_short | A large deletion at the cortex locus eliminates butterfly wing patterning |
title_sort | large deletion at the cortex locus eliminates butterfly wing patterning |
topic | Investigation |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8982378/ https://www.ncbi.nlm.nih.gov/pubmed/35099556 http://dx.doi.org/10.1093/g3journal/jkac021 |
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