Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene clade.
Wing patterning in Heliconius butterflies is a longstanding example of both Müllerian mimicry and phenotypic radiation under strong natural selection. The loci controlling such patterns are "hotspots" for adaptive evolution with great allelic diversity across different species in the genus...
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Public Library of Science (PLoS)
2010-02-01
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| Series: | PLoS Genetics |
| Online Access: | https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1000794&type=printable |
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| author | Simon W Baxter Nicola J Nadeau Luana S Maroja Paul Wilkinson Brian A Counterman Anna Dawson Margarita Beltran Silvia Perez-Espona Nicola Chamberlain Laura Ferguson Richard Clark Claire Davidson Rebecca Glithero James Mallet W Owen McMillan Marcus Kronforst Mathieu Joron Richard H Ffrench-Constant Chris D Jiggins |
| author_facet | Simon W Baxter Nicola J Nadeau Luana S Maroja Paul Wilkinson Brian A Counterman Anna Dawson Margarita Beltran Silvia Perez-Espona Nicola Chamberlain Laura Ferguson Richard Clark Claire Davidson Rebecca Glithero James Mallet W Owen McMillan Marcus Kronforst Mathieu Joron Richard H Ffrench-Constant Chris D Jiggins |
| author_sort | Simon W Baxter |
| collection | DOAJ |
| description | Wing patterning in Heliconius butterflies is a longstanding example of both Müllerian mimicry and phenotypic radiation under strong natural selection. The loci controlling such patterns are "hotspots" for adaptive evolution with great allelic diversity across different species in the genus. We characterise nucleotide variation, genotype-by-phenotype associations, linkage disequilibrium, and candidate gene expression at two loci and across multiple hybrid zones in Heliconius melpomene and relatives. Alleles at HmB control the presence or absence of the red forewing band, while alleles at HmYb control the yellow hindwing bar. Across HmYb two regions, separated by approximately 100 kb, show significant genotype-by-phenotype associations that are replicated across independent hybrid zones. In contrast, at HmB a single peak of association indicates the likely position of functional sites at three genes, encoding a kinesin, a G-protein coupled receptor, and an mRNA splicing factor. At both HmYb and HmB there is evidence for enhanced linkage disequilibrium (LD) between associated sites separated by up to 14 kb, suggesting that multiple sites are under selection. However, there was no evidence for reduced variation or deviations from neutrality that might indicate a recent selective sweep, consistent with these alleles being relatively old. Of the three genes showing an association with the HmB locus, the kinesin shows differences in wing disc expression between races that are replicated in the co-mimic, Heliconius erato, providing striking evidence for parallel changes in gene expression between Müllerian co-mimics. Wing patterning loci in Heliconius melpomene therefore show a haplotype structure maintained by selection, but no evidence for a recent selective sweep. The complex genetic pattern contrasts with the simple genetic basis of many adaptive traits studied previously, but may provide a better model for most adaptation in natural populations that has arisen over millions rather than tens of years. |
| format | Article |
| id | doaj-art-dcd4514d33c844caa953262a9e41357e |
| institution | OA Journals |
| issn | 1553-7390 1553-7404 |
| language | English |
| publishDate | 2010-02-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj-art-dcd4514d33c844caa953262a9e41357e2025-08-20T02:31:51ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042010-02-0162e100079410.1371/journal.pgen.1000794Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene clade.Simon W BaxterNicola J NadeauLuana S MarojaPaul WilkinsonBrian A CountermanAnna DawsonMargarita BeltranSilvia Perez-EsponaNicola ChamberlainLaura FergusonRichard ClarkClaire DavidsonRebecca GlitheroJames MalletW Owen McMillanMarcus KronforstMathieu JoronRichard H Ffrench-ConstantChris D JigginsWing patterning in Heliconius butterflies is a longstanding example of both Müllerian mimicry and phenotypic radiation under strong natural selection. The loci controlling such patterns are "hotspots" for adaptive evolution with great allelic diversity across different species in the genus. We characterise nucleotide variation, genotype-by-phenotype associations, linkage disequilibrium, and candidate gene expression at two loci and across multiple hybrid zones in Heliconius melpomene and relatives. Alleles at HmB control the presence or absence of the red forewing band, while alleles at HmYb control the yellow hindwing bar. Across HmYb two regions, separated by approximately 100 kb, show significant genotype-by-phenotype associations that are replicated across independent hybrid zones. In contrast, at HmB a single peak of association indicates the likely position of functional sites at three genes, encoding a kinesin, a G-protein coupled receptor, and an mRNA splicing factor. At both HmYb and HmB there is evidence for enhanced linkage disequilibrium (LD) between associated sites separated by up to 14 kb, suggesting that multiple sites are under selection. However, there was no evidence for reduced variation or deviations from neutrality that might indicate a recent selective sweep, consistent with these alleles being relatively old. Of the three genes showing an association with the HmB locus, the kinesin shows differences in wing disc expression between races that are replicated in the co-mimic, Heliconius erato, providing striking evidence for parallel changes in gene expression between Müllerian co-mimics. Wing patterning loci in Heliconius melpomene therefore show a haplotype structure maintained by selection, but no evidence for a recent selective sweep. The complex genetic pattern contrasts with the simple genetic basis of many adaptive traits studied previously, but may provide a better model for most adaptation in natural populations that has arisen over millions rather than tens of years.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1000794&type=printable |
| spellingShingle | Simon W Baxter Nicola J Nadeau Luana S Maroja Paul Wilkinson Brian A Counterman Anna Dawson Margarita Beltran Silvia Perez-Espona Nicola Chamberlain Laura Ferguson Richard Clark Claire Davidson Rebecca Glithero James Mallet W Owen McMillan Marcus Kronforst Mathieu Joron Richard H Ffrench-Constant Chris D Jiggins Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene clade. PLoS Genetics |
| title | Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene clade. |
| title_full | Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene clade. |
| title_fullStr | Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene clade. |
| title_full_unstemmed | Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene clade. |
| title_short | Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene clade. |
| title_sort | genomic hotspots for adaptation the population genetics of mullerian mimicry in the heliconius melpomene clade |
| url | https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1000794&type=printable |
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