Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry

CNRS UMR 7205, Muséum National d'Histoire Naturelle, CP50, 45 Rue Buffon, 75005 Paris, France.
Nature (Impact Factor: 42.35). 08/2011; 477(7363):203-6. DOI: 10.1038/nature10341
Source: PubMed

ABSTRACT 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.

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Available from: Paul Anthony Wilkinson, Aug 11, 2015
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    • "Butterfly wing patterns are a crucible of morphological diversity that provide an ideal template to study the mechanisms that drive pattern evolution (Beldade and Brakefield, 2002; Joron et al., 2006; Nijhout, 1991). Several recent studies have narrowed down the genetic basis of wing pattern variation to single genes, explaining phenotypic switches involved in adaptive mimicry and sexual selection (Gallant et al., 2014; Joron et al., 2011; Kunte et al., 2014; Martin et al., 2012; Reed et al., 2011). Importantly, some of these mechanisms of intraspecific variation also appear to act at deeper taxonomic scales, with the same genes repeatedly causing similar trait differences in convergent lineages (Gallant et al., 2014; Martin and Orgogozo, 2013; Martin et al., 2012; Papa et al., 2008; Reed et al., 2011). "
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    ABSTRACT: Most butterfly wing patterns are proposed to be derived from a set of conserved pattern elements known as symmetry systems. Symmetry systems are so-named because they are often associated with parallel color stripes mirrored around linear organizing centers that run between the anterior and posterior wing margins. Even though the symmetry systems are the most prominent and diverse wing pattern elements, their study has been confounded by a lack of knowledge regarding the molecular basis of their development, as well as the difficulty of drawing pattern homologies across species with highly derived wing patterns. Here we present the first molecular characterization of symmetry system development by showing that WntA expression is consistently associated with the major basal, discal, central, and external symmetry system patterns of nymphalid butterflies. Pharmacological manipulations of signaling gradients using heparin and dextran sulfate showed that pattern organizing centers correspond precisely with WntA, wingless, Wnt6, and Wnt10 expression patterns, thus suggesting a role for Wnt signaling in color pattern induction. Importantly, this model is supported by recent genetic and population genomic work identifying WntA as the causative locus underlying wing pattern variation within several butterfly species. By comparing the expression of WntA between nymphalid butterflies representing a range of prototypical symmetry systems, slightly deviated symmetry systems, and highly derived wing patterns, we were able to infer symmetry system homologies in several challenging cases. Our work illustrates how highly divergent morphologies can be derived from modifications to a common ground plan across both micro- and macro-evolutionary time scales.
    Developmental Biology 09/2014; 395(2). DOI:10.1016/j.ydbio.2014.08.031 · 3.64 Impact Factor
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    • "Warning coloration Divergence isolated to two genomic regions associated with color and pattern variation Joron et al. 2006, 2011; Reed et al. 2011 Baxter et al. 2010, Counterman et al. 2010, Heliconius Genome Consort. 2012, Nadeau et al. 2012 Lycaeides sp. "
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    ABSTRACT: Understanding speciation requires determining how inherent barriers to gene flow (reproductive isolation) evolve between populations. The field of population genomics attempts to address this question by characterizing genome-wide patterns of divergence between taxa, often utilizing next generation sequencing. Here, we focus on a central assumption of such ‘genome scans’: that regions displaying high levels of differentiation contain loci contributing to reproductive isolation. Three major issues are discussed concerning the relationship between gene flow, genomic divergence, and speciation: (1) patterns expected in the presence versus absence of gene flow; (2) processes such as direct selection and genetic hitchhiking allowing for divergence with gene flow; and (3) the consequences of the timing of when gene flow occurs during speciation (e.g., continuous gene flow versus gene flow following secondary contact after a period of initial allopatric divergence). Theory and existing data are presented for each issue, with avenues for future work highlighted.
    11/2013; 44(1-1). DOI:10.1146/annurev-ecolsys-110512-135825
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    • "Conversely, we note that there are numerous studies showing that linkage between locally adapted genes and between incompatibilities can enhance the effectiveness of selection on these loci (e.g. Barton, 1983; Kirkpatrick and Barton, 2005; Via and West, 2008; Kulathinal et al., 2009; Joron et al., 2011; Yeaman and Whitlock, 2011). Hence if the fitness effects of local adaptation and incompatibility loci become correlated (Barton and de Cara, 2009; Abbott et al., 2013; Trier et al., personal data) -such as if a moving tension zone (Barton and Hewitt, 1985, 1989) becomes aligned with a sharp environmental ecotone evolvability will be increased. "
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    ABSTRACT: Recent genomic studies have highlighted the importance of hybridization and gene exchange in evolution. We ask what factors cause variation in the impact of hybridization, through adaptation in hybrids and the likelihood of hybrid speciation. During speciation, traits that diverge due to both divergent and stabilizing selection can contribute to the buildup of reproductive isolation. Divergent directional selection in parent taxa should lead to intermediate phenotypes in hybrids, whereas stabilizing selection can also produce extreme, transgressive phenotypes when hybridization occurs. By examining existing theory and empirical data, we discuss how these effects, combined with differences between modes of divergence in the chromosomal distribution of incompatibilities, affect adaptation and speciation in hybrid populations. The result is a clear and testable set of predictions that can be used to examine hybrid adaptation and speciation. Stabilizing selection in parents increases transgression in hybrids, increasing the possibility for novel adaptation. Divergent directional selection causes intermediate hybrid phenotypes and increases their ability to evolve along the direction of parental differentiation. Stabilizing selection biases incompatibilities towards autosomes, leading to reduced sexual correlations in trait values and reduced pleiotropy in hybrids, and hence increased freedom in the direction of evolution. Directional selection causes a bias towards sex-linked incompatibilities, with the opposite consequences. Divergence by directional selection leads to greater dominance effects than stabilizing selection, with major but variable impacts on hybrid evolution [Current Zoology 59 (5): 675685, 2013].
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