Hybrid Zone Origins, Species Boundaries, and the Evolution of Wing-Pattern Diversity in a Polytypic Species Complex of North American Admiral Butterflies (Nymphalidae: Limenitis)

Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca, New York 14853, USA.
Evolution (Impact Factor: 4.61). 07/2008; 62(6):1400-17. DOI: 10.1111/j.1558-5646.2008.00366.x
Source: PubMed


Hybrid zones present opportunities to study the effects of gene flow, selection, and recombination in natural populations and, thus, provide insights into the genetic and phenotypic changes that occur early in speciation. Here we investigate a hybrid zone between mimetic (Limenitis arthemis astyanax) and nonmimetic (Limenitis arthemis arthemis) populations of admiral butterflies using DNA sequence variation from mtDNA and seven nuclear gene loci. We find three distinct mitochondrial clades within this complex, and observe a strong overall concordance between wing-pattern phenotypes and mitochondrial variation. Nuclear gene genealogies, in contrast, revealed no evidence of exclusivity for either wing-pattern phenotype, suggesting incomplete barriers to gene exchange and/or insufficient time for lineage sorting. Coalescent simulations indicate that gene flow between these two subspecies is highly asymmetric, with the majority of migration occurring from mimetic into nonmimetic populations. Selective sweeps of alleles responsible for mimetic phenotypes may have occurred more than once when mimetic and nonmimetic Limenitis occurred together in the presence of the model (Battus philenor).

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Available from: Richard G Harrison, Oct 04, 2015
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    • "Diversification of both wing coloration and visual pigments has also occurred among North American admiral butterflies in the genus Limenitis (Frentiu, Bernard, Cuevas, et al. 2007). Natural selection for mimetic resemblance between Limenitis arthemis astyanax (the red-spotted purple) and its model Battus philenor (the pipevine swallowtail) has led to a Batesian mimicry polymorphism within the L. a. arthemisastyanax species complex (Mullen et al. 2008). In addition, M€ ullerian mimicry has evolved between unpalatable L. archippus (viceroy) butterflies and the chemically defended monarch Danaus plexippus. "
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    ABSTRACT: Opsins are ancient molecules that enable animal vision by coupling to a vitamin-derived chromophore to form light-sensitive photopigments. The primary drivers of evolutionary diversification in opsins are thought to be visual tasks related to spectral sensitivity and color vision. Typically, only a few opsin amino acid sites affect photopigment spectral sensitivity. We show that opsin genes of the North American butterfly Limenitis arthemis have diversified along a latitudinal cline, consistent with natural selection due to environmental factors. We sequenced single nucleotide (SNP) polymorphisms in the coding regions of the ultraviolet (UVRh), blue (BRh), and long-wavelength (LWRh) opsin genes from ten butterfly populations along the eastern United States and found that a majority of opsin SNPs showed significant clinal variation. Outlier detection and analysis of molecular variance indicated that many SNPs are under balancing selection and show significant population structure. This contrasts with what we found by analysing SNPs in the wingless and EF-1 alpha loci, and from neutral amplified fragment length polymorphisms, which show no evidence of significant locus-specific or genome-wide structure among populations. Using a combination of functional genetic and physiological approaches, including expression in cell culture, transgenic Drosophila, UV-visible spectroscopy, and optophysiology, we show that key BRh opsin SNPs that vary clinally have almost no effect on spectral sensitivity. Our results suggest that opsin diversification in this butterfly is more consistent with natural selection unrelated to spectral tuning. Some of the clinally varying SNPs may instead play a role in regulating opsin gene expression levels or the thermostability of the opsin protein. Lastly, we discuss the possibility that insect opsins might have important, yet-to-be elucidated, adaptive functions in mediating animal responses to abiotic factors, such as temperature or photoperiod.
    Molecular Biology and Evolution 02/2015; 32(2):368-79. DOI:10.1093/molbev/msu304 · 9.11 Impact Factor
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    • "As a result, many examples of hybrid zones appear to be relatively stable (Barton and Hewitt 1985); however, more and more examples of asymmetric introgression are being discovered (Buggs 2007). Evidence for asymmetry can take a number of forms, including direct observation of pairing-related behaviors of hybridizing forms (Bronson et al. 2003; Leichty and Grier 2006; Charpentier et al. 2012), population genetic estimates of migration rates (Geraldes et al. 2008; Mullen et al. 2008; Nevado et al. 2011; Charpentier et al. 2012), patterns of correlation (or lack thereof) among genetic and phenotypic markers (Parsons et al. 1993; Rohwer et al. 2001; Roca et al. 2005; Wang et al. 2011; Hailer et al. 2012), and long-term observation of hybrid zone movement (Dasmahapatra et al. 2002; Carling and Zuckerberg 2011). Another, less commonly-reported pattern that suggests asymmetric hybridization is the disjunct distribution of a phenotype within the range of a phenotypically distinct form or forms with which it is hybridizing (Weisrock et al. 2005; Culumber et al. 2011). "
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    ABSTRACT: Geographic distributions of genetic and phenotypic characters can illuminate historical evolutionary processes. In particular, mosaic distributions of phenotypically similar populations can arise from parallel evolution or from irregular patterns of dispersal and colonization by divergent forms. Two phenotypically divergent forms of the red-winged blackbird (Agelaius phoeniceus) show a mosaic phenotypic distribution, with a “bicolored” form occurring disjunctly in California and Mexico. We analyzed the relationships among these bicolored populations and neighboring typical populations, using ~600 bp of mitochondrial DNA sequence data and 10 nuclear short tandem repeat loci. We find that bicolored populations, although separated by ~3000 km, are genetically more similar to one other than they are to typical populations separated by ~400 km. We also find evidence of ongoing gene flow among populations, including some evidence of asymmetric gene flow. We conclude that the current distribution of bicolored forms represents incomplete speciation, where recent asymmetric hybridization with typical A. phoeniceus is dividing the range of a formerly widespread bicolored form. This hypothesis predicts that bicolored forms may suffer extinction by hybridization. Future work will use fine-scaled geographical sampling and nuclear sequence data to test for hybrid origins of currently typical populations and to more precisely quantify the directionality of gene flow.
    Ecology and Evolution 12/2013; 3(15). DOI:10.1002/ece3.859 · 2.32 Impact Factor
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    • "The prevalence of gene flow between differentiated species has been fully recognized as an evolutionary force contributing to the diversity of plants (Soltis and Soltis 2009), vertebrates (Brumfield et al. 2001; Helbig et al. 2001; Won and Hey 2005; Carling and Brumfield 2008), invertebrates (Cianchi et al. 2003; Mullen et al. 2008), and fungal systems (Gladieux et al. 2008, 2011), but its role in evolution is still matter of debate (Arnold 2004; Barton 2001, 2013; Abbott et al. 2013). The fate of an allele introgressing into a new gene pool is known to be highly dependent on the nature and strength of natural selection acting on its genomic neighbourhood . "
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    ABSTRACT: Inferring a realistic demographic model from genetic data is an important challenge to gain insights into the historical events during the speciation process and to detect molecular signatures of selection along genomes. Recent advances in divergence population genetics have reported that speciation in face of gene flow occurred more frequently than theoretically expected, but the approaches used did not account for genome wide heterogeneity (GWH) in introgression rates. Here we investigate the impact of GWH on the inference of divergence with gene flow between two cryptic species of the marine model Ciona intestinalis by analysing polymorphism and divergence patterns in 852 protein-coding sequence loci.These morphologically similar entities are highly diverged molecular-wise, but evidence of hybridisation has been reported in both laboratory and field studies. We compare various speciation models and test for GWH under the ABC framework. Our results demonstrate the presence of significant extents of gene flow resulting from a recent secondary contact after >3 My of divergence in isolation. The inferred rates of introgression are relatively low, highly variable across loci and mostly unidirectional, which is consistent with the idea that numerous genetic incompatibilities have accumulated over time throughout the genomes of these highly-diverged species. A genomic map of the level of gene flow identified two hotspots of introgression, i.e. large genome regions of unidirectional introgression. This study clarifies the history and degree of isolation of two cryptic and partially sympatric model species, and provides a methodological framework to investigate GWH at various stages of speciation process.
    Molecular Biology and Evolution 04/2013; 30(7). DOI:10.1093/molbev/mst066 · 9.11 Impact Factor
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