Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies

Salazar, Camilo; Baxter, Simon W.; Pardo‐Díaz, Carolina; Wu, Grace C.; Surridge, Alison K.; Linares, Mauricio; Bermingham, Eldredge; Jiggins, Chris D.

doi:10.1371/journal.pgen.1000930

Cited by 92 publications

(140 citation statements)

References 63 publications

(95 reference statements)

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“…For example, in hybrid zones in Peru, kinesin, VanGogh, and GPCR showed strong genotype-by-phenotype association and restricted gene flow (16,17). Even kinesin, which demonstrated expression differences between divergent phenotypes of both H. erato and H. melpomene (16,17,23) and was strongly implicated in the origin of the red forewing band of H. heurippa (24), was only weakly associated with color pattern in our analyses. These patterns likely reflect the physical distances between these loci and the functional differences that are driving phenotypic diversity.…”

Section: Discussionmentioning

confidence: 56%

“…H. melpomene is a member of a larger complex of species that are known to hybridize in nature, including a number of species in the Amazon region with rayed phenotypes (1,27). The acquisition of new color patterns by hybridization is thought to play an important role in the evolution of pattern variation in Heliconius (24,28,29). Additional sequence data around optix across the H. melpomene species-complex should help resolve the origins of red patterns within the melpomene group.…”

Section: Discussionmentioning

confidence: 99%

“…Further population genetic and comparative gene-expression work on this region has identified a gene, optix, that controls red color-pattern variation in both H. erato and H. melpomene (22). Although no other genes show the pattern-specific expression of optix, other genes in this interval have shown significant genotype-by-phenotype associations (16,17,23) and expression differences between divergent color-pattern races (16,17,24).…”

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confidence: 99%

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Wing patterning gene redefines the mimetic history ofHeliconiusbutterflies

Hines

Counterman

Papa

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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The mimetic butterflies Heliconius erato and Heliconius melpomene have undergone parallel radiations to form a near-identical patchwork of over 20 different wing-pattern races across the Neotropics. Previous molecular phylogenetic work on these radiations has suggested that similar but geographically disjunct color patterns arose multiple times independently in each species. The neutral markers used in these studies, however, can move freely across color pattern boundaries, and therefore might not represent the history of the adaptive traits as accurately as markers linked to color pattern genes. To assess the evolutionary histories across different loci, we compared relationships among races within H. erato and within H. melpomene using a series of unlinked genes, genes linked to color pattern loci, and optix, a gene recently shown to control red colorpattern variation. We found that although unlinked genes partition populations by geographic region, optix had a different history, structuring lineages by red color patterns and supporting a single origin of red-rayed patterns within each species. Genes closely linked (80-250 kb) to optix exhibited only weak associations with color pattern. This study empirically demonstrates the necessity of examining phenotype-determining genomic regions to understand the history of adaptive change in rapidly radiating lineages. With these refined relationships, we resolve a long-standing debate about the origins of the races within each species, supporting the hypothesis that the red-rayed Amazonian pattern evolved recently and expanded, causing disjunctions of more ancestral patterns.Müllerian mimicry | population genetics | phylogeography R esearchers typically rely on neutrally evolving loci to generate a phylogenetic and population genetic history of adaptive divergence. The rationale is that these markers provide an unbiased view of the relationships among divergent phenotypes and a better understanding of the evolutionary processes generating variation. However, the genome is a complicated mosaic shaped by an interplay of mutation, drift, selection, and recombination. Recombination allows different regions of the genome to experience alternative restrictions to gene flow, and thus develop different evolutionary trajectories. The closer a genetic marker is to the alleles responsible for adaptive differences, the more likely that it will trace the history of phenotypic change.Understanding how phenotypic variation is generated in nature is greatly enhanced by studying groups that are actively undergoing diversification. By deciphering the history of such diverse phenotypes we gain a clearer understanding of the evolutionary process, including the tempo and mode of phenotypic change. Heliconius butterflies present one of the most striking examples of a recent phenotypic radiation. The 40 species in the genus exhibit hundreds of wing patterns that are involved in Müllerian mimicry complexes, where distasteful species converge on a shared warning signal to avoid predation. Th...

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Section: Discussionmentioning

confidence: 56%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Wing patterning gene redefines the mimetic history ofHeliconiusbutterflies

Hines

Counterman

Papa

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

111

172

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“…In a few identified homoploid hybrid species (for example, Heliconius butterflies), the introgression of relatively few traits that confer an ecological advantage may be sufficient to cause reproductive (mainly ecological) isolation (hybrid trait speciation; Jiggins et al, 2008;Salazar et al, 2010). Such systems present an opportunity to investigate alternative models of hybrid speciation, especially ones in which genic incompatibilities and ecological isolation are of primary importance in reproductive isolation.…”

Section: Introductionmentioning

confidence: 99%

Genomic collinearity and the genetic architecture of floral differences between the homoploid hybrid species Iris nelsonii and one of its progenitors, Iris hexagona

Taylor

Rojas

et al. 2012

Heredity

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Hybrid speciation represents a relatively rapid form of diversification. Early models of homoploid hybrid speciation suggested that reproductive isolation between the hybrid species and progenitors primarily resulted from karyotypic differences between the species. However, genic incompatibilities and ecological divergence may also be responsible for isolation. Iris nelsonii is an example of a homoploid hybrid species that is likely isolated from its progenitors primarily by strong prezygotic isolation, including habitat divergence, floral isolation and post-pollination prezygotic barriers. Here, we used linkage mapping and quantitative trait locus (QTL) mapping approaches to investigate genomic collinearity and the genetic architecture of floral differences between I. nelsonii and one of its progenitor species I. hexagona. The linkage map produced from this cross is highly collinear with another linkage map produced between I. fulva and I. brevicaulis (the two other species shown to have contributed to the genomic makeup of I. nelsonii), suggesting that karyotypic differences do not contribute substantially to isolation in this homoploid hybrid species. Similar to other studies of the genetic architecture of floral characteristics, at least one QTL was found that explained 420% variance in each color trait, while minor QTLs were detected for each morphological trait. These QTLs will serve as hypotheses for regions under selection by pollinators.

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“…These criteria are: (1) a strong RI mechanism between the putative parental and hybrid species; (2) genetic evidence of hybridization; and (3) isolating mechanisms derived from hybridization itself. They concluded that only four examples across the living world fulfil these three requisites and are thus considered as true homoploid hybrid species: the butterfly Heliconius heurippa (Salazar et al, 2010) and the three hybrid sunflower species, Helianthus anomalus, H. deserticola and H. paradoxus (Rieseberg, 1991).…”

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confidence: 99%