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      Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies

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          Abstract

          Homoploid hybrid speciation is the formation of a new hybrid species without change in chromosome number. So far, there has been a lack of direct molecular evidence for hybridization generating novel traits directly involved in animal speciation. Heliconius butterflies exhibit bright aposematic color patterns that also act as cues in assortative mating. Heliconius heurippa has been proposed as a hybrid species, and its color pattern can be recreated by introgression of the H. m. melpomene red band into the genetic background of the yellow banded H. cydno cordula. This hybrid color pattern is also involved in mate choice and leads to reproductive isolation between H. heurippa and its close relatives. Here, we provide molecular evidence for adaptive introgression by sequencing genes across the Heliconius red band locus and comparing them to unlinked wing patterning genes in H. melpomene, H. cydno, and H. heurippa. 670 SNPs distributed among 29 unlinked coding genes (25,847bp) showed H. heurippa was related to H. c. cordula or the three species were intermixed. In contrast, among 344 SNPs distributed among 13 genes in the red band region (18,629bp), most showed H. heurippa related with H. c. cordula, but a block of around 6,5kb located in the 3′ of a putative kinesin gene grouped H. heurippa with H. m. melpomene, supporting the hybrid introgression hypothesis. Genealogical reconstruction showed that this introgression occurred after divergence of the parental species, perhaps around 0.43Mya. Expression of the kinesin gene is spatially restricted to the distal region of the forewing, suggesting a mechanism for pattern regulation. This gene therefore constitutes the first molecular evidence for adaptive introgression during hybrid speciation and is the first clear candidate for a Heliconius wing patterning locus.

          Author Summary

          Hybrid speciation challenges our view of biodiversity as a branching tree and is considered rare or absent in animals. A possible route by which it may occur is establishment of a novel “magic trait,” influencing both ecological adaptation and mating preference, via hybridization. We provide, to our knowledge, the first molecular genetic evidence for this process in the tropical butterfly Heliconius heurippa. We sampled molecular markers both linked to the locus controlling red color pattern and across the genome of Heliconius heurippa and its putative parents, H. cydno and H. melpomene. We found evidence of genetic introgression from H. melpomene into the hybrid H. heurippa only at the genomic region of the forewing red-band locus. This signature of introgression corresponds to the 3′ end of a kinesin gene that also shows a pattern of expression restricted to the distal region of the forewing. As the wing color pattern in these butterflies is crucial in maintaining the isolation of this species through mate choice, this study provides molecular support for the hybrid origin of a new adaptive trait that can lead to speciation.

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          Arlequin (version 3.0): An integrated software package for population genetics data analysis

          Arlequin ver 3.0 is a software package integrating several basic and advanced methods for population genetics data analysis, like the computation of standard genetic diversity indices, the estimation of allele and haplotype frequencies, tests of departure from linkage equilibrium, departure from selective neutrality and demographic equilibrium, estimation or parameters from past population expansions, and thorough analyses of population subdivision under the AMOVA framework. Arlequin 3 introduces a completely new graphical interface written in C++, a more robust semantic analysis of input files, and two new methods: a Bayesian estimation of gametic phase from multi-locus genotypes, and an estimation of the parameters of an instantaneous spatial expansion from DNA sequence polymorphism. Arlequin can handle several data types like DNA sequences, microsatellite data, or standard multi-locus genotypes. A Windows version of the software is freely available on http://cmpg.unibe.ch/software/arlequin3.
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            DnaSP, DNA polymorphism analyses by the coalescent and other methods.

            DnaSP is a software package for the analysis of DNA polymorphism data. Present version introduces several new modules and features which, among other options allow: (1) handling big data sets (approximately 5 Mb per sequence); (2) conducting a large number of coalescent-based tests by Monte Carlo computer simulations; (3) extensive analyses of the genetic differentiation and gene flow among populations; (4) analysing the evolutionary pattern of preferred and unpreferred codons; (5) generating graphical outputs for an easy visualization of results. The software package, including complete documentation and examples, is freely available to academic users from: http://www.ub.es/dnasp
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              Divergent selection and heterogeneous genomic divergence.

              Levels of genetic differentiation between populations can be highly variable across the genome, with divergent selection contributing to such heterogeneous genomic divergence. For example, loci under divergent selection and those tightly physically linked to them may exhibit stronger differentiation than neutral regions with weak or no linkage to such loci. Divergent selection can also increase genome-wide neutral differentiation by reducing gene flow (e.g. by causing ecological speciation), thus promoting divergence via the stochastic effects of genetic drift. These consequences of divergent selection are being reported in recently accumulating studies that identify: (i) 'outlier loci' with higher levels of divergence than expected under neutrality, and (ii) a positive association between the degree of adaptive phenotypic divergence and levels of molecular genetic differentiation across population pairs ['isolation by adaptation' (IBA)]. The latter pattern arises because as adaptive divergence increases, gene flow is reduced (thereby promoting drift) and genetic hitchhiking increased. Here, we review and integrate these previously disconnected concepts and literatures. We find that studies generally report 5-10% of loci to be outliers. These selected regions were often dispersed across the genome, commonly exhibited replicated divergence across different population pairs, and could sometimes be associated with specific ecological variables. IBA was not infrequently observed, even at neutral loci putatively unlinked to those under divergent selection. Overall, we conclude that divergent selection makes diverse contributions to heterogeneous genomic divergence. Nonetheless, the number, size, and distribution of genomic regions affected by selection varied substantially among studies, leading us to discuss the potential role of divergent selection in the growth of regions of differentiation (i.e. genomic islands of divergence), a topic in need of future investigation.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, USA )
                1553-7390
                1553-7404
                April 2010
                April 2010
                29 April 2010
                : 6
                : 4
                : e1000930
                Affiliations
                [1 ]Department of Zoology, University of Cambridge, Cambridge, United Kingdom
                [2 ]Smithsonian Tropical Research Institute, Balboa, Panamá
                [3 ]Instituto de Genética, Universidad de los Andes, Bogotá, Colombia
                University of Arizona, United States of America
                Author notes

                Conceived and designed the experiments: CS ML EB CDJ. Performed the experiments: CS CPD GW. Analyzed the data: CS CPD CDJ. Contributed reagents/materials/analysis tools: CS SWB AS CDJ. Wrote the paper: CS SWB CPD CDJ. Mapped and annotated the HmB color pattern region: SWB. Specimen collection: ML.

                Article
                10-PLGE-RA-2406R2
                10.1371/journal.pgen.1000930
                2861694
                20442862
                38611936-6392-46e1-9e86-548a250c48e8
                Salazar et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 19 January 2010
                : 30 March 2010
                Page count
                Pages: 12
                Categories
                Research Article
                Evolutionary Biology
                Evolutionary Biology/Animal Genetics

                Genetics
                Genetics

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