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: 41.46). 08/2011; 477(7363):203-6. DOI: 10.1038/nature10341
Source: PubMed


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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    • "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.
    Full-text · Article · Sep 2014 · Developmental Biology
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    • "Indeed, new data for certain model organisms have demonstrated a more nuanced role for inversions in adaptive divergence and RI than originally envisioned (Strasburg et al., 2009; Michel et al., 2010). Specifically, genome scans have found numerous differentiated regions mapping outside chromosomal rearrangements (Strasburg et al., 2009; Jones et al., 2012; Reidenbach et al., 2012), although findings from Drosophila, Mimulus, Heliconius, and crows may provide exceptions (Noor et al., 2001, 2007; Lowry and Willis, 2010; Joron et al., 2011; Stevison et al., 2011; McGaugh and Noor, 2012; Poelstra et al., 2014). We are therefore gaining a clearer and more accurate understanding of the adaptive significance of inversions for population divergence and speciation. "
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    ABSTRACT: Many hypotheses have been put forth to explain the origin and spread of inversions, and their significance for speciation. Several recent genic models have proposed that inversions promote speciation with gene flow due to the adaptive significance of the genes contained within them and because of the effects inversions have on suppressing recombination. However, the consequences of inversions for the dynamics of genome wide divergence across the speciation continuum remain unclear, an issue we examine here. We review a framework for the genomics of speciation involving the congealing of the genome into alternate adaptive states representing species ("genome wide congealing"). We then place inversions in this context as examples of how genetic hitchhiking can potentially hasten genome wide congealing. Specifically, we use simulation models to (i) examine the conditions under which inversions may speed genome congealing and (ii) quantify predicted magnitudes of these effects. Effects of inversions on promoting speciation were most common and pronounced when inversions were initially fixed between populations before secondary contact and adaptation involved many genes with small fitness effects. Further work is required on the role of underdominance and epistasis between a few loci of major effect within inversions. The results highlight five important aspects of the roles of inversions in speciation: (i) the geographic context of the origins and spread of inversions, (ii) the conditions under which inversions can facilitate divergence, (iii) the magnitude of that facilitation, (iv) the extent to which the buildup of divergence is likely to be biased within vs. outside of inversions, and (v) the dynamics of the appearance and disappearance of exceptional divergence within inversions. We conclude by discussing the empirical challenges in showing that inversions play a central role in facilitating speciation with gene flow.
    Full-text · Article · Aug 2014 · Frontiers in Genetics
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    • "Papilio dardanus is renowned for the morphological diversity of its mimetic females and has been central to the development of the supergene theory. However, although supergenes have recently been shown to underlie polymorphism in other mimetic butterflies [6], [8], their existence in P. dardanus remains unconfirmed. To promote P. dardanus as a study system, we present a systematic overview of variation displayed within the species accompanied by distribution maps. "
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    ABSTRACT: The history of 20th Century evolutionary biology can be followed through the study of mimetic butterflies. From the initial findings of discontinuous polymorphism through the debates regarding the evolution of mimicry and the step-size of evolutionary change, to the studies on supergene evolution and molecular characterisation of butterfly genomes, mimetic butterflies have been at the heart of evolutionary thought for over 100 years. During this time, few species have received as much attention and in-depth study as Papilio dardanus. To assist all aspects of mimicry research, we present a complete data-derived overview of the extent of polymorphism within this species. Using historical samples permanently held by the NHM London, we document the extent of phenotypic variation and characterise the diversity present in each of the subspecies and how it varies across Africa. We also demonstrate an association between "imperfect" mimetic forms and the transitional race formed in the area where Eastern and Western African populations meet around Lake Victoria. We present a novel portal for access to this collection,, allowing remote access to this unique repository. It is hoped that this online resource can act as a nucleus for the sharing and dissemination of other collections databases and imagery connected with mimetic butterflies.
    Full-text · Article · May 2014 · PLoS ONE
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