RESUMEN
Supergenes are tight clusters of loci that facilitate the co-segregation of adaptive variation, providing integrated control of complex adaptive phenotypes. Polymorphic supergenes, in which specific combinations of traits are maintained within a single population, were first described for 'pin' and 'thrum' floral types in Primula and Fagopyrum, but classic examples are also found in insect mimicry and snail morphology. Understanding the evolutionary mechanisms that generate these co-adapted gene sets, as well as the mode of limiting the production of unfit recombinant forms, remains a substantial challenge. Here we show that individual wing-pattern morphs in the polymorphic mimetic butterfly Heliconius numata are associated with different genomic rearrangements at the supergene locus P. These rearrangements tighten the genetic linkage between at least two colour-pattern loci that are known to recombine in closely related species, with complete suppression of recombination being observed in experimental crosses across a 400-kilobase interval containing at least 18 genes. In natural populations, notable patterns of linkage disequilibrium (LD) are observed across the entire P region. The resulting divergent haplotype clades and inversion breakpoints are found in complete association with wing-pattern morphs. Our results indicate that allelic combinations at known wing-patterning loci have become locked together in a polymorphic rearrangement at the P locus, forming a supergene that acts as a simple switch between complex adaptive phenotypes found in sympatry. These findings highlight how genomic rearrangements can have a central role in the coexistence of adaptive phenotypes involving several genes acting in concert, by locally limiting recombination and gene flow.
Asunto(s)
Mariposas Diurnas/genética , Cromosomas de Insectos/genética , Reordenamiento Génico/genética , Genes de Insecto/genética , Imitación Molecular/genética , Polimorfismo Genético/genética , Alelos , Animales , Mariposas Diurnas/anatomía & histología , Mariposas Diurnas/fisiología , Paseo de Cromosoma , Ligamiento Genético/genética , Haplotipos/genética , Imitación Molecular/fisiología , Datos de Secuencia Molecular , Familia de Multigenes/genética , Fenotipo , Pigmentación/genética , Pigmentación/fisiología , Alas de Animales/anatomía & histología , Alas de Animales/metabolismo , Alas de Animales/fisiologíaRESUMEN
Convergent evolution provides a rare, natural experiment with which to test the predictability of adaptation at the molecular level. Little is known about the molecular basis of convergence over macro-evolutionary timescales. Here we use a combination of positional cloning, population genomic resequencing, association mapping and developmental data to demonstrate that positionally orthologous nucleotide variants in the upstream region of the same gene, WntA, are responsible for parallel mimetic variation in two butterfly lineages that diverged >65 million years ago. Furthermore, characterization of spatial patterns of WntA expression during development suggests that alternative regulatory mechanisms underlie wing pattern variation in each system. Taken together, our results reveal a strikingly predictable molecular basis for phenotypic convergence over deep evolutionary time.
Asunto(s)
Mariposas Diurnas/genética , Evolución Molecular , Regulación del Desarrollo de la Expresión Génica/genética , Genes de Insecto/genética , Pigmentación/genética , Homología de Secuencia de Ácido Nucleico , Alas de Animales/metabolismo , Proteínas Wnt/genética , Animales , Evolución Biológica , Variación Genética , Genoma , Fenotipo , Alas de Animales/crecimiento & desarrolloRESUMEN
Mimicry--whereby warning signals in different species evolve to look similar--has long served as a paradigm of convergent evolution. Little is known, however, about the genes that underlie the evolution of mimetic phenotypes or to what extent the same or different genes drive such convergence. Here, we characterize one of the major genes responsible for mimetic wing pattern evolution in Heliconius butterflies. Mapping, gene expression, and population genetic work all identify a single gene, optix, that controls extreme red wing pattern variation across multiple species of Heliconius. Our results show that the cis-regulatory evolution of a single transcription factor can repeatedly drive the convergent evolution of complex color patterns in distantly related species, thus blurring the distinction between convergence and homology.
Asunto(s)
Evolución Biológica , Mariposas Diurnas/genética , Genes de Insecto , Proteínas de Homeodominio/genética , Proteínas de Insectos/genética , Pigmentación/genética , Alas de Animales/anatomía & histología , Adaptación Biológica , Animales , Mariposas Diurnas/anatomía & histología , Mariposas Diurnas/crecimiento & desarrollo , Evolución Molecular , Perfilación de la Expresión Génica , Regulación del Desarrollo de la Expresión Génica , Variación Genética , Genoma de los Insectos , Desequilibrio de Ligamiento , Datos de Secuencia Molecular , Mariposas Nocturnas/genética , Fenotipo , Elementos Reguladores de la Transcripción , Selección Genética , Especificidad de la Especie , Factores de Transcripción/genética , Transcripción Genética , Alas de Animales/crecimiento & desarrolloRESUMEN
Ecological speciation occurs when ecologically based, divergent selection causes the evolution of reproductive isolation. There are many empirical examples of this process; however, there exists a poorly characterized stage during which the traits that distinguish species ecologically and reproductively segregate in a single population. By using a combination of genetic mapping, mate-choice experiments, field observations, and population genetics, we studied a butterfly population with a mimetic wing color polymorphism and found that the butterflies exhibited partial, color-based, assortative mate preference. These traits represent the divergent, ecologically based signal and preference components of sexual isolation that usually distinguish incipient and sibling species. The association between behavior and recognition trait in a single population may enhance the probability of speciation and provides an example of the missing link between an interbreeding population and isolated species.