DOCSLIB.ORG

Butterfly Genome Reveals Promiscuous Exchange of Mimicry Adaptations Among Species

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Butterfly Genome Reveals Promiscuous Exchange of Mimicry Adaptations Among Species LETTER doi:10.1038/nature11041 Butterfly genome reveals promiscuous exchange of mimicry adaptations among species The Heliconius Genome Consortium* The evolutionary importance of hybridization and introgression has The butterfly genus Heliconius (Nymphalidae: Heliconiinae) is long been debated1. Hybrids are usually rare and unfit, but even associated with a suite of derived life-history and ecological traits, infrequent hybridization can aid adaptation by transferring bene- including pollen feeding, extended lifespan, augmented ultraviolet ficial traits between species. Here we use genomic tools to investigate colour vision, ‘trap-lining’ foraging behaviour, gregarious roosting and introgression in Heliconius, a rapidly radiating genus of neotropical complex mating behaviours, and provides outstanding opportunities for butterflies widely used in studies of ecology, behaviour, mimicry and genomic studies of adaptive radiation and speciation4,6. The genus is best speciation2–5. We sequenced the genome of Heliconius melpomene known for the hundreds of races with different colour patterns seen and compared it with other taxa to investigate chromosomal evolu- among its 43 species, with repeated examples of both convergent evolu- tion in Lepidoptera and gene flow among multiple Heliconius tion among distantly related species and divergent evolution between species and races. Among 12,669 predicted genes, biologically closely related taxa3. Geographic mosaics of multiple colour-pattern important expansions of families of chemosensory and Hox races, such as in Heliconius melpomene (Fig. 1), converge to similar genes are particularly noteworthy. Chromosomal organization mosaics in other species, and this led to the hypothesis of mimicry2. has remained broadly conserved since the Cretaceous period, when Heliconius are unpalatable to vertebrate predators and Mu¨llerian butterflies split from the Bombyx (silkmoth) lineage. Using mimicry of warning colour patterns enables species to share the cost genomic resequencing, we show hybrid exchange of genes between of educating predators3. As a result of its dual role in mimicry and mate three co-mimics, Heliconius melpomene, Heliconius timareta and selection, divergence in wing pattern is also associated with speciation Heliconius elevatus, especially at two genomic regions that control and adaptive radiation3,5. A particularly recent radiation is the mimicry pattern. We infer that closely related Heliconius species melpomene–silvaniform clade, in which mimetic patterns often seem exchange protective colour-pattern genes promiscuously, implying to be polyphyletic (Fig. 1a). Most species in this clade occasionally that hybridization has an important role in adaptive radiation. hybridize in the wild with other clade members7. Gene genealogies at a b H. melpomene H. numata rosina H. ethilla Silvaniform clade H. melpomene melpomene H. hecale 1,000 km H. pardalinus sergestus H. elevatus (rayed) H. pardalinus butleri H. melpomene H. timareta florencia aglaope/malleti (rayed) H. timareta ssp. nov. (postman) H. heurippa H. melpomene H. cydno amaryllis H. melpomene rosina (postman) H. melpomene H. melpomene melpomene (postman) p H. melpomene amaryllis (postman) H. melpomene aglaope/malleti (rayed) H. erato Figure 1 | Distribution, mimicry and phylogenetic relationships of H. melpomene races studied here (blue, yellow and purple), and the entire sequenced taxa. a, Phylogenetic relationship of sequenced species and distribution of H. melpomene (grey). The H. timareta races investigated have subspecies in the melpomene–silvaniform clade of Heliconius. Heliconius limited distributions (red) indicated by arrows and mimic sympatric races of elevatus falls in the silvaniform clade, but it mimics colour patterns of H. melpomene. Heliconius elevatus and the other silvaniform species are melpomene–timareta clade taxa. Most other silvaniforms mimic unrelated distributed widely across the Amazon basin (Supplementary Information, ithomiine butterflies24. b, Geographic distribution of postman and rayed section 22). *Lists of participants and their affiliations appear at the end of the paper. 00 MONTH 2012 | VOL 000 | NATURE | 1 ©2012 Macmillan Publishers Limited. All rights reserved RESEARCH LETTER a small number of loci indicate introgression between species8, and The origin of butterflies was associated with a switch from nocturnal one non-mimetic species, Heliconius heurippa, has a hybrid origin9. to diurnal behaviour, and a corresponding increase in visual commun- Adaptive introgression of mimicry loci is therefore a plausible ication16. Heliconius have increased visual complexity through explanation for parallel evolution of multiple mimetic patterns in the expression of a duplicate ultraviolet opsin6, in addition to the long- melpomene–silvaniform clade. wavelength-, blue- and ultraviolet-sensitive opsins in Bombyx.We A Heliconius melpomene melpomene stock from Darie´n, Panama might therefore predict reduced complexity of olfactory genes, but (Fig. 1), was inbred through five generations of sib mating. We in fact Heliconius and Danaus17 genomes have more chemosensory sequenced a single male to 338 coverage (after quality filtering) using genes than any other insect genome: 33 and 34, respectively combined 454 and Illumina technologies (Supplementary Informa- (Supplementary Information, section 9). For comparison, there are tion, sections 1–8). The complete draft genome assembly, which is 24 in Bombyx and 3–4 in Drosophila18. Lineage-specific expansions 269 megabases (Mb) in size, consists of 3,807 scaffolds with an N50 of chemosensory genes were evident in both Danaus and Heliconius of 277 kb and contains 12,669 predicted protein-coding genes. (Fig. 2b). By contrast, all three lepidopteran genomes have similar Restriction-site-associated DNA (RAD) linkage mapping was used numbers of odorant binding proteins and olfactory receptors to assign and order 83% of the sequenced genome onto the 21 chro- (Supplementary Information, section 9). Hox genes are involved in mosomes (Supplementary Information, section 4). These data permit body plan development and show strong conservation across animals. a considerably improved genome-wide chromosomal synteny com- We identified four additional Hox genes located between the canonical parison with the silkmoth Bombyx mori10,11. Hox genes pb and zen, orthologous to shx genes in B. mori19 (Sup- Using 6,010 orthologues identified between H. melpomene and plementary Information, section 10). These Hox gene duplications B. mori, we found that 11 of 21 H. melpomene linkage groups show in the butterflies and Bombyx have a common origin and are inde- homology to single B. mori chromosomes and that ten linkage groups pendent of the two tandem duplications known in dipterans (zen2 have major contributions from two B. mori chromosomes (Fig. 2a and and bcd). Immunity-related gene families are similar across all three Supplementary Information, section 8), revealing several previously lepidopterans (Supplementary Information, section 11), whereas there unidentified chromosomal fusions. These fusions on the Heliconius are extensive duplications and losses within dipterans20. lineage most probably occurred after divergence from the sister genus The Heliconius reference genome allowed us to perform rigorous Eueides4, which has the lepidopteran modal karyotype of n 5 31 (ref. 12). tests for introgression among melpomene–silvaniform clade species. Three chromosomal fusions are evident in Bombyx (B. mori chromo- We used RAD resequencing to reconstruct a robust phylogenetic tree somes 11, 23 and 24; Fig. 2a), as required for evolution of the Bombyx based on 84 individuals of H. melpomene and its relatives, sampling on n 5 28 karyotype from the ancestral n 5 31 karyotype. Heliconius and average 12 Mb, or 4%, of the genome (Fig. 1a and Supplementary Bombyx lineages diverged in the Cretaceous, more than 100 million Information, sections 12–18). We then tested for introgression between years ago11, so the gross chromosomal structures of Lepidoptera the sympatric co-mimetic postman butterfly races of Heliconius genomes have remained highly conserved compared with those of flies melpomene amaryllis and H. timareta ssp. nov. (Fig. 1) in Peru, using or vertebrates13,14. By contrast, small-scale rearrangements were ‘ABBA/BABA’ single nucleotide sites and Patterson’s D-statistics frequent. In the comparison with Bombyx, we estimate there to be (Fig. 3a), originally developed to test for admixture between 0.05–0.13 breaks per megabase per million years, and in that with Neanderthals and modern humans21,22 (Supplementary Information, Danaus plexippus (Monarch butterfly), we estimate there to be section 12). Genome-wide, we found an excess of ABBA sites, giving a 0.04–0.29 breaks per megabase per million years. Although lower than significantly positive Patterson’s D of 0.037 6 0.003 (two-tailed Z-test previously suggested for Lepidoptera15, these rates are comparable to for D 5 0, P 5 1 3 10240), indicating greater genome-wide introgres- those in Drosophila (Supplementary Information, section 8). sion between the sympatric mimetic taxa H. melpomene amaryllis and 9 10 8 7 a 11 b Chemosensory proteins Heliconius 6 12 5 1 DpCSP5 10 Mb 4 HmCSP3 2 BmCSP3 Bm 13 3 Bootstrap support >80% H 24 DpCSP2mCSP5 CSP5 pCSP16 5 2 H CSP21 D HmCSP16 BmCSP16 mCSP2 BmCSP 14 BmCSP2 HmCSP21 Dp mCSP DpCSP20 B HmCSP20 BmCSP23 15 1 BmCSP25 B HmCSP2 mCSP16 DpCSP25 BmCSP7 16 DpCSP23 HmCSP7 2 HmCSP23 DpCSP7 DpCSP29 B 3 HmCSP22 u
Load more

Recommended publications
  • The Speciation History of Heliconius: Inferences from Multilocus DNA Sequence Data
    The speciation history of Heliconius: inferences from multilocus DNA sequence data by Margarita Sofia Beltrán A thesis submitted for the degree of Doctor of Philosophy of the University of London September 2004 Department of Biology University College London 1 Abstract Heliconius butterflies, which contain many intermediate stages between local varieties, geographic races, and sympatric species, provide an excellent biological model to study evolution at the species boundary. Heliconius butterflies are warningly coloured and mimetic, and it has been shown that these traits can act as a form of reproductive isolation. I present a species-level phylogeny for this group based on 3834bp of mtDNA (COI, COII, 16S) and nuclear loci (Ef1α, dpp, ap, wg). Using these data I test the geographic mode of speciation in Heliconius and whether mimicry could drive speciation. I found little evidence for allopatric speciation. There are frequent shifts in colour pattern within and between sister species which have a positive and significant correlation with species diversity; this suggests that speciation is facilitated by the evolution of novel mimetic patterns. My data is also consistent with the idea that two major innovations in Heliconius, adult pollen feeding and pupal-mating, each evolved only once. By comparing gene genealogies from mtDNA and introns from nuclear Tpi and Mpi genes, I investigate recent speciation in two sister species pairs, H. erato/H. himera and H. melpomene/H. cydno. There is highly significant discordance between genealogies of the three loci, which suggests recent speciation with ongoing gene flow. Finally, I explore the phylogenetic relationships between races of H. melpomene using an AFLP band tightly linked to the Yb colour pattern locus (which determines the yellow bar in the hindwing).
    [Show full text]
  • Characterising Reproductive Barriers Between Three Closely Related Heliconius Butterfly Taxa
    Characterising reproductive barriers between three closely related Heliconius butterfly taxa. Lucie M. Queste MSc by Research University of York, Biology November 2015 1 Abstract Debates about the possibility of divergence in the face of gene flow have been an ongoing feature in the field of speciation. However, recent theoretical studies and examples in nature have demonstrated evidence for such a process. Much research now focuses on finding more evidence of reinforcement such as stronger isolation in sympatric populations. Genomic studies have also been investigating the role of gene flow in sympatric speciation and the formation of islands of divergence. Heliconius butterflies offer extensive opportunities to answer such questions. Here, I test whether male colour pattern preference and female host plant preference act as reproductive barriers in three Heliconius taxa with varying degrees of geographic overlap. Further experiments on the F2 hybrids of two of these taxa aimed to identify the underlying genomic architecture of these traits. My results suggest that male colour pattern preference and host preference are acting as reproductive barriers. Stronger differences between the sympatric species were found demonstrating evidence for reinforcement and divergence with gene flow. Initial analyses of the F2 hybrid phenotypes suggest that several loci control these traits and pave the way for future genetic analyses to further understand the role of gene flow in speciation. 2 Table of Contents Abstract 2 Table of Contents 3 List of Figures 4 List of Tables 5 Acknowledgements 6 Author’s Declaration 7 Chapter 1 – Introduction 8 1. Speciation 8 2. Heliconius 15 3. Aims and Objectives 20 Chapter 2 – Identifying traits acting as reproductive barriers between three taxa of 21 Heliconius with varying levels of gene flow.
    [Show full text]
  • Divergence of Chemosensing During the Early Stages of Speciation
    Divergence of chemosensing during the early stages of speciation Bas van Schootena,b,1,2, Jesyka Meléndez-Rosaa,1,2, Steven M. Van Belleghema, Chris D. Jigginsc, John D. Tand, W. Owen McMillanb, and Riccardo Papaa,b,e,2 aDepartment of Biology, University of Puerto Rico, Rio Piedras, San Juan, Puerto Rico 00925; bSmithsonian Tropical Research Institution, Balboa Ancón, 0843-03092 Panama, Republic of Panama; cDepartment of Zoology, University of Cambridge, CB2 8PQ Cambridge, United Kingdom; dRoche NimbleGen Inc., Madison, WI 53719; and eMolecular Sciences and Research Center, University of Puerto Rico, San Juan, Puerto Rico 00907 Edited by Joan E. Strassmann, Washington University in St. Louis, St. Louis, MO, and approved June 1, 2020 (received for review December 5, 2019) Chemosensory communication is essential to insect biology, play- few studies have identified chemosensory genes involved in re- ing indispensable roles during mate-finding, foraging, and ovipo- productive isolation (9, 15, 16). sition behaviors. These traits are particularly important during To date, most of the work on the genetic basis of chemo- speciation, where chemical perception may serve to establish spe- sensory signaling has been conducted on insects, with an em- cies barriers. However, identifying genes associated with such phasis on Drosophila and moths (e.g., Heliothis and Bombyx). complex behavioral traits remains a significant challenge. Through However, in the past few years, the growing accessibility of a combination of transcriptomic and genomic approaches, we whole-genome and transcriptome sequencing has allowed us to characterize the genetic architecture of chemoperception and the describe chemosensory genes for a number of new butterfly role of chemosensing during speciation for a young species pair of species.
    [Show full text]
  • Do Pollen Feeding, Pupal-Mating and Larval Gregariousness Have a Single Origin in Heliconius Butterflies? Inferences from Multilocus DNA Sequence Data
    Biological Journal of the Linnean Society, 2007, 92, 221-239. With 4 figures Do pollen feeding, pupal-mating and larval gregariousness have a single origin in Heliconius butterflies? Inferences from multilocus DNA sequence data MARGAEITA BELTRAN1'2'3*, CHRIS D. JIGGINS3, ANDREW V. Z. BROWER4, ELDREDGE BERMINGHAM1 and JAMES MALLET2 Smithsonian Tropical Research Institute, AA 2072, Balboa, Panama 2The Galton Laboratory, Department of Biology, University College London, London NW1 2HE, UK ^Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK department of Biology, Middle Tennessee State University, Murfreesboro, TN 37132, USA Received 22 November 2005; accepted for publication 4 November 2006 Phylogenetic information is useful in understanding the evolutionary history of adaptive traits. Here, we present a well-resolved phylogenetic hypothesis for Heliconius butterflies and related genera. We use this tree to investigate the evolution of three traits, pollen feeding, pupal-mating behaviour and larval gregariousness. Phylogenetic relationships among 60 Heliconiina species (86% of the subtribe) were inferred from partial DNA sequences of the mitochondrial genes cytochrome oxidase I, cytochrome oxidase II and 16S rRNA, and fragments of the nuclear genes elongation factor-la, apterous, decapentaplegic and wingless (3834 bp in total). The results corroborate previous hypotheses based on sequence data in showing that Heliconius is paraphyletic, with Laparus doris and Neruda falling within the genus, demonstrating a single origin for pollen feeding but with a loss of the trait in Neruda. However, different genes are not congruent in their placement of Neruda; therefore, monophyly of the pollen feeding species cannot be ruled out. There is also a highly supported monophyletic 'pupal-mating clade' suggesting that pupal mating behaviour evolved only once in the Heliconiina.
    [Show full text]
  • Cryptic Speciation Associated with Geographic and Ecological
    Zoological Journal of the Linnean Society, 2019, 186, 233–249. With 7 figures. Cryptic speciation associated with geographic and ecological divergence in two Amazonian Heliconius Downloaded from https://academic.oup.com/zoolinnean/article-abstract/186/1/233/5066664 by University of York user on 13 June 2019 butterflies NEIL ROSSER1,2*, , ANDRÉ V. L. FREITAS3, BLANCA HUERTAS4, MATHIEU JORON5, GERARDO LAMAS6, CLAIRE MÉROT7, FRASER SIMPSON8, KEITH R. WILLMOTT9, JAMES MALLET2 and KANCHON K. DASMAHAPATRA1 1Department of Biology, University of York, Wentworth Way, Heslington YO10 5DD, UK 2Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA 3Departamento de Biologia Animal and Museu de Zoologia, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, São Paulo, Brazil 4Life Sciences Department, Natural History Museum, Cromwell Road, London, SW7 5BD, UK 5Centre d’Ecologie Fonctionnelle et Evolutive, UMR 5175 CNRS - Université de Montpellier - Université Paul Valéry Montpellier - EPHE, 1919 route de Mende, 34293 Montpellier, France 6Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Apartado 14–0434, Lima-14, Peru 7IBIS, Université Laval, 1030 Avenue de la Médecine, Québec, Canada 8Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK 9McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL, USA Received 23 February 2018; revised 14 May 2018; accepted for publication 27 May 2018 The evolution of reproductive isolation via a switch in mimetic wing coloration has become the paradigm for speci- ation in aposematic Heliconius butterflies. Here, we provide a counterexample to this, by documenting two cryptic species within the taxon formerly considered Heliconius demeter Staudinger, 1897.
    [Show full text]
  • Abstract Book
    Species boundaries among Heliconius butterflies reflect the genetic architecture of speciation Simon Martin University of Cambridge We still lack a detailed understanding of the genetic mechanisms that allow species to coexist and hybridize without collapsing. Theory predicts that genetic incompatibilities that reduce fitness of hybrids and recombinants may form barriers to gene flow, particularly in genomic regions of reduced recombination. This has proved difficult to test empirically. Conventional methods for studying the landscape of gene flow across the genome are prone to biases, making them difficult to interpret. We addressed this issue by using novel, and less biased, approaches to study relatedness across the genome between hybridizing species of Heliconius butterflies. We compared two pairs of species using multiple resequenced genomes from multiple replicated regions of sympatry. We found that relatedness between species fluctuates on a large scale across the genome, and that patterns of introgression differ between the two species pairs. In one pair, gene flow is correlated with recombination rate, reduced at chromosome centres and in gene-rich regions. In the other pair, rates of gene flow are more even across the genome. Using simulations, we show that these patterns are consistent with biological differences between the two species pairs. One pair has distinct wing patterns that are under strong ecological selection and may provide a genome-wide barrier to gene flow. The other pair lacks this dramatic ecological difference, so the species boundary depends more on the distribution of genetic incompatibilities and recombination. Our findings therefore supplement theoretical work, showing how the shape of the species boundary reflects the genetic architecture of species differences.
    [Show full text]
  • Conservation and Flexibility in the Gene Regulatory Landscape of Heliconiine Butterfly Wings 1
    bioRxiv preprint doi: https://doi.org/10.1101/541599; this version posted February 5, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Hanly et al, Conservation and flexibility in the gene regulatory landscape of Heliconiine butterfly wings 1 1 Conservation and flexibility in the gene regulatory 2 landscape of Heliconiine butterfly wings 3 Joseph J Hanly1,2,3*, Richard WR Wallbank1,2, W Owen 4 McMillan2, Chris D Jiggins1,2 5 1. Department of Zoology, University of Cambridge, Downing St., Cambridge 6 CB2 3EJ, UK 7 2. Smithsonian Tropical Research Institute, Gamboa, Panama 8 3. The George Washington University, Washington DC, 20052, USA 9 * = corresponding author. [email protected] 10 Abstract 11 Background 12 Many traits evolve by cis-regulatory modification, by which changes to non-coding 13 sequences affect the binding affinity for available transcription factors and thus 14 modify the expression profile of genes. Multiple examples of cis-regulatory evolution 15 have been described at pattern switch genes responsible for butterfly wing pattern 16 polymorphism, including in the diverse neotropical genus Heliconius, but the 17 identities of the factors that can regulate these switch genes have not been identified. 18 Results 19 We investigated the spatial transcriptomic landscape across the wings of three closely 20 related butterfly species, two of which have a convergently-evolved, co-mimetic 21 pattern, the other having a divergent pattern.
    [Show full text]
  • Dasmahapatra Et Al. 2007
    Biol. Lett. morphology both between species and among geo- doi:10.1098/rsbl.2007.0401 graphical races within species. The bright wing Published online colours act as a warning of their unpalatability to Evolutionary biology potential predators. Many species share similar pat- terns with unrelated Heliconiinae and Ithomiinae, leading to impressive Mu¨llerian mimicry rings (Bates Genetic analysis of a 1862; Turner 1981; Beccaloni 1997; Joron & Mallet 1998). Although hybrids are rare within most wild-caught hybrid between Heliconius populations, the existence of naturally occurring hybrids is intriguing because it suggests non-sister Heliconius that gene flow will be possible between species. Hence, this could lead to the transfer of adaptive butterfly species genes between species (Gilbert 2003). Kanchon K. Dasmahapatra*, Hybridization in Heliconius has hitherto been Armando Silva-Va´squez, Jae-Woo Chung examined genetically only in a few cases that involve and James Mallet closely related species: Heliconius erato and Heliconius himera,orHeliconius melpomene and Heliconius cydno Galton Laboratory, Department of Biology, University College London, London NW1 2HE, UK (Jiggins et al. 1997; Bull et al. 2006; Kronforst et al. *Author for correspondence ([email protected]). 2006). In all other cases, inferences of hybridization have been made on the basis of phenotypes of wild- Interspecific hybridization occurs regularly in caught specimens. In contrast, the extremely rare wild Heliconius butterflies, although hybrid individuals are usually very rare. However, hybrids between H. melpomene and the more distant hybridization generally occurs only between the species in the ‘silvaniform’ Heliconius (Mallet et al. most closely related species. We report a rare 2007) have never been examined genetically.
    [Show full text]
  • Do Pollen Feeding, Pupal-Mating and Larval Gregariousness Have a Single Origin in Heliconius Butterflies? Inferences from Multilocus DNA Sequence Data
    Biological Journal of the Linnean Society, 2007, 92, 221–239. With 4 figures Do pollen feeding, pupal-mating and larval gregariousness have a single origin in Heliconius butterflies? Inferences from multilocus DNA sequence data MARGARITA BELTRÁN1,2,3*, CHRIS D. JIGGINS3, ANDREW V. Z. BROWER4, ELDREDGE BERMINGHAM1 and JAMES MALLET2 1Smithsonian Tropical Research Institute, AA 2072, Balboa, Panama 2The Galton Laboratory, Department of Biology, University College London, London NW1 2HE, UK 3Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK 4Department of Biology, Middle Tennessee State University, Murfreesboro, TN 37132, USA Received 22 November 2005; accepted for publication 4 November 2006 Phylogenetic information is useful in understanding the evolutionary history of adaptive traits. Here, we present a well-resolved phylogenetic hypothesis for Heliconius butterflies and related genera. We use this tree to investigate the evolution of three traits, pollen feeding, pupal-mating behaviour and larval gregariousness. Phylogenetic relationships among 60 Heliconiina species (86% of the subtribe) were inferred from partial DNA sequences of the mitochondrial genes cytochrome oxidase I, cytochrome oxidase II and 16S rRNA, and fragments of the nuclear genes elongation factor-1a, apterous, decapentaplegic and wingless (3834 bp in total). The results corroborate previous hypotheses based on sequence data in showing that Heliconius is paraphyletic, with Laparus doris and Neruda falling within the genus, demonstrating a single origin for pollen feeding but with a loss of the trait in Neruda. However, different genes are not congruent in their placement of Neruda; therefore, monophyly of the pollen feeding species cannot be ruled out. There is also a highly supported monophyletic ‘pupal-mating clade’ suggesting that pupal mating behaviour evolved only once in the Heliconiina.
    [Show full text]
  • Published By: American Entomological Society Stable URL: Your Use of the JSTOR Archive In
    An Illustrated Key to the Silvaniform Heliconius (Lepidoptera: Nymphalidae) with Descriptions of New Subspecies Author(s): Keith S. Brown, .Tr. Source: Transactions of the American Entomological Society (1890-), Vol. 102, No. 3 (Sep., 1976), pp. 373-484 Published by: American Entomological Society Stable URL: http://www.jstor.org/stable/25078195 Accessed: 24/09/2011 20:04 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. American Entomological Society is collaborating with JSTOR to digitize, preserve and extend access to Transactions of the American Entomological Society (18904 AN ILLUSTRATED KEY TO THE SILVANIFORM HELICONIUS (LEPIDOPTERA: NYMPHALIDAE) 1 WITH DESCRIPTIONS OF NEW SUBSPECIES BY KEITH S. BROWN, JR. Departamento de Zoologia, Institute de Biologia, Universidade Estadual de Campinas, C.P. 1170 Campinas, Sao Paulo 13.100 Brazil INTRODUCTION The group of Nymphaline butterflies classified under the general name "silvaniform heliconians" represents one of the most difficult taxonomic groups in the Lepidoptera. The fact that their wing colors and patterns are extremely plastic, responding rapidly to local selective pressures usually linked to Miillerian mimicry rings, make traditional classification based on these color-patterns labor- ious and often contradictory. The importance of developing a reasonable, orderly, and accurate systematic arrangement for the group derives from the fundamental significance of the mimicry in the ecology of these organisms, and of many related insects in the mimicry rings.
    [Show full text]
  • Reply to Andrew Brower's Critique of the Evidence for Hybridization
    Zootaxa 4679 (3): 577–595 ISSN 1175-5326 (print edition) https://www.mapress.com/j/zt/ Article ZOOTAXA Copyright © 2019 Magnolia Press ISSN 1175-5334 (online edition) https://doi.org/10.11646/zootaxa.4679.3.11 http://zoobank.org/urn:lsid:zoobank.org:pub:6457E92D-5531-4039-9B44-21F1E2CD4D29 Reply to Andrew Brower’s critique of the evidence for hybridization among Heliconius butterfly species in the wild JAMES MALLET Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Avenue, Cambridge MA 02138, USA. Abstract Andrew Brower recently published a long article in this journal that seeks to dismantle evidence for hybridization between species of Heliconius butterflies. The main evidence that Brower criticizes here is given in two papers published by my colleagues and myself in 2007. In this reply, I briefly defend our evidence, and at greater length provide additional background information to help establish the credibility of the evidence even more firmly than previously. Key words: Introduction Andrew van Zandt Brower recently published a paper (Brower 2018a) arguing that many interspecific hybrid speci- mens we reported in our review of hybrids among species of Heliconius (Mallet et al. 2007) were unreliably identi- fied. He further argues that a wild hybrid between H. ethilla and H. melpomene, captured by our team in Peru and verified as a hybrid using DNA sequencing (Dasmahapatra et al. 2007), is also open to doubt. The combined studies of many colleagues and myself, both then and since, has shown that hybridization among many Heliconius species occurs at a low rate in nature, and also that introgression of genetic material is a somewhat frequent result of these occasional misalliances.
    [Show full text]
  • For Review Only
    Page 1 of 41 Molecular Ecology A CRYPTIC SPECIES OF HELICONIUS BUTTERFLY PROVIDES EVIDENCE OF VICARIANT SPECIATION IN THE AMAZON VIA A HOST PLANT SHIFT Neil Rosser1,2*, André V. L. Freitas3, Blanca Huertas4, Mathieu Joron5, Gerardo Lamas6, Claire Mérot7, Fraser Simpson8, Keith Willmott9, James Mallet2, Kanchon K. Dasmahapatra1. 1. Department of Biology, University of York, Wentworth Way, York YO10 5DD, UK 2. Department of OrganismicFor and EvolutionaryReview Biology, Only Harvard University, Cambridge, Massachusetts 02138, USA 3. Departamento de Biologia Animal and Museu de Zoologia, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, São Paulo, Brazil. 4. Department of Entomology, Natural History Museum, Cromwell Road, London SW7 5BD, UK. 5. Centre d'Ecologie Fonctionnelle et Evolutive, UMR 5175 CNRS - Université de Montpellier - Université Paul Valéry Montpellier - EPHE, 1919 route de Mende, 34293 Montpellier, France 6. Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Apartado 14-0434, Lima-14, Peru. 7. IBIS, Université Laval, 1030 Avenue de la Médecine, Québec, Canada. 8. Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, United Kingdom; 9. McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL, USA *Author for correspondence; [email protected] 1 Molecular Ecology Page 2 of 41 ABSTRACT The evolution of reproductive isolation via a switch in mimetic wing coloration has become the paradigm for speciation in aposematic Heliconius butterflies. Here, we provide an interesting counterexample to this, by demonstrating the presence of a cryptic species within Heliconius demeter Staudinger, 1897. Amplified fragment length polymorphisms identify two sympatric genotypic clusters in northern Peru, corresponding to subspecies Heliconius demeter ucayalensis H.
    [Show full text]