What can hybrid zones tell us about speciation? The case of Heliconius erato and H. himera (Lepidoptera: Nymphalidae)

The Galton Laboratory, Department of Biology, University College London, NW1 2HE, London; 23, 12357, Fuchsiensweg, Berlin, Germany
Biological Journal of the Linnean Society (Impact Factor: 2.41). 01/1996; 59(3). DOI: 10.1006/bijl.1996.0063

ABSTRACT To understand speciation we need to study the genetics and ecology of intermediate cases where interspecific hybridization still occurs. Two closely related species of Heliconius butterflies meet this criterion: Heliconius himera is endemic to dry forest and thorn scrub in southern Ecuador and northern Peru, while its sister species, H. erato, is ubiquitous in wet forest throughout south and central America. In three known zones of contact, the two species remain distinct, while hybrids are found at low frequency. Collections in southern Ecuador show that the contact zone is about 5 km wide, half the width of the narrowest clines between colour pattern races of H. erato. The narrowness of this cline argues that very strong selection (s ≈ 1) is maintaining the parapatric distributions of these two species. The zone is closely related with a habitat transition from wet to dry forest, which suggests that the narrow zone of parapatry is maintained primarily by ecological adaptation. Selection on colour pattern loci, assortative mating and hybrid inviability may also be important. The genetics of hybrids between the two species shows that the major gene control of pattern elements is similar to that found in previous studies of H. erato races, and some of the loci are homologous. This suggests that similar genetic processes are involved in the morphological divergence of species and races. Evidence from related Heliconius supports a hypothesis that ecological adaptation is the driving force for speciation in the group.

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    ABSTRACT: Hybrid zones of ecologically divergent populations are ideal systems to study the interaction between natural selection and gene flow during the initial stages of speciation. Here, we perform an amplified fragment length polymorphism (AFLP) genome scan in parallel hybrid zones between divergent ecotypes of the marine snail Littorina saxatilis, which is considered a model case for the study of ecological speciation. Ridged-Banded (RB) and Smooth-Unbanded (SU) ecotypes are adapted to different shore levels and microhabitats, although they present a sympatric distribution at the mid-shore where they meet and mate (partially assortatively). We used shell morphology, outlier and nonoutlier AFLP loci from RB, SU and hybrid specimens captured in sympatry to determine the level of phenotypic and genetic introgression. We found different levels of introgression at parallel hybrid zones and nonoutlier loci showed more gene flow with greater phenotypic introgression. These results were independent from the phylogeography of the studied populations, but not from the local ecological conditions. Genetic variation at outlier loci was highly correlated with phenotypic variation. In addition, we used the relationship between genetic and phenotypic variation to estimate the heritability of morphological traits and to identify potential Quantitative Trait Loci to be confirmed in future crosses. These results suggest that ecology (exogenous selection) plays an important role in this hybrid zone. Thus, ecologically based divergent natural selection is responsible, simultaneously, for both ecotype divergence and hybridization. On the other hand, genetic introgression occurs only at neutral loci (nonoutliers). In the future, genome-wide studies and controlled crosses would give more valuable information about this process of speciation in the face of gene flow.
    Journal of Evolutionary Biology 05/2013; · 3.48 Impact Factor
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    ABSTRACT: Hybrid zones have long intrigued evolutionary biologists and provide a natural laboratory to explore the evolution of reproductive isolation (speciation). Molecular characterization of hybrid zone dynamics can provide insight into the strength of reproductive isolation as well as the underlying evolutionary processes shaping gene flow. Approximately one-third of darter species naturally hybridize making this species-rich North American freshwater teleost fish clade an ideal system to investigate the extent and direction of hybridization. The objective of this study was to use diagnostic microsatellite markers to calculate genetic hybrid index scores of two syntopic, but distantly related darter species, Etheostoma bison and Etheostoma caeruleum. A combination of hybrid index scores, assignment tests, and mitochondrial haplotype profiles uncovered mixed ancestry in approximately 6 % of sampled adult individuals, supporting contemporaneous hybridization that was previously undocumented in E. bison. Moreover, hybrids were not limited to the F(1) generation, but encompassed the entire suite of hybrid categories (F(1), F(2) and backcross hybrids). The low number of hybrids assigned to each hybrid category represents a bimodal hybrid zone, suggesting reproductive isolation is strong (but incomplete) and also advocates for the ability of hybrids to produce second-generation hybrids and backcross into both parental species, mediating introgression across species boundaries. To this end, cytonuclear profiles of the sampled parental species and hybrids were consistent with bidirectional gene flow, although there was an overall trend of asymmetric hybridization between E. caeruleum females and E. bison males. The spatiotemporal variation in hybridization rates and resulting cytonuclear patterns expanded on in this study provide a comparative genetic framework on which future studies can begin to elucidate the underlying processes that not only generate a mosaic hybrid zone, but maintain the distinctness of species in the face of gene flow.
    Genetica 02/2013; · 1.68 Impact Factor
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    ABSTRACT: Theoretical models suggest that traits under divergent ecological selection, which also contribute to assortative mating, will facilitate speciation with gene flow. Evidence for these so-called "magic traits" now exists across a range of taxa. However, their importance during speciation will depend on the extent to which they contribute to reproductive isolation. Addressing this requires experiments to determine the exact cues involved as well as estimates of assortative mating in the wild. Heliconius butterflies are well known for their diversity of bright warning color patterns, and their amenability to experimental manipulation has provided an excellent opportunity to test their role in reproductive isolation. Here, we reveal that divergent color patterns contribute to mate recognition between the incipient species Heliconius himera and H. erato, a taxon pair for which assortative mating by color pattern has been demonstrated among wild individuals: First, we demonstrate that males are more likely to attempt to mate conspecific females; second, we show that males are more likely to approach pinned females that share their own warning pattern. These data are valuable as these taxa likely represent the early stages of speciation, but unusually also allow comparisons with rates of interbreeding between divergent ecologically relevant phenotypes measured in the wild.
    Ecology and Evolution 04/2014; 4(7):911-7. · 1.66 Impact Factor

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