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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). -
Genomic Architecture of Adaptive Color Pattern Divergence and Convergence in Heliconius Butterflies
Downloaded from genome.cshlp.org on September 29, 2021 - Published by Cold Spring Harbor Laboratory Press Research Genomic architecture of adaptive color pattern divergence and convergence in Heliconius butterflies Megan A. Supple,1,2 Heather M. Hines,3,4 Kanchon K. Dasmahapatra,5,6 James J. Lewis,7 Dahlia M. Nielsen,3 Christine Lavoie,8 David A. Ray,8 Camilo Salazar,1,9 W. Owen McMillan,1,10 and Brian A. Counterman8,10,11 1Smithsonian Tropical Research Institute, Panama City, Republic of Panama; 2Biomathematics Program, North Carolina State University, Raleigh, North Carolina 27695, USA; 3Department of Genetics, North Carolina State University, Raleigh, North Carolina 27695, USA; 4Department of Biology, Pennsylvania State University, University Park, Pennsylvania 16802, USA; 5Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, United Kingdom; 6Department of Biology, University of York, York YO10 5DD, United Kingdom; 7Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York 14853, USA; 8Department of Biological Sciences, Mississippi State University, Mississippi State, Mississippi 39762, USA; 9Facultad de Ciencias Naturales y Matema´ticas, Universidad del Rosario, Bogota´ DC, Colombia Identifying the genetic changes driving adaptive variation in natural populations is key to understanding the origins of biodiversity. The mosaic of mimetic wing patterns in Heliconius butterflies makes an excellent system for exploring adaptive variation using next-generation sequencing. In this study, we use a combination of techniques to annotate the genomic interval modulating red color pattern variation, identify a narrow region responsible for adaptive divergence and con- vergence in Heliconius wing color patterns, and explore the evolutionary history of these adaptive alleles. -
Ecological Divergence and Speciation in Heliconius Cydno and H
Ecological divergence and speciation in Heliconius cydno and H. melpomene by Russell Edward Naisbit A thesis submitted for the degree of Doctor of Philosophy of the University of London September 2001 Department of Biology University College London To my family, for their support and encouragement throughout this crazy endeavour 2 “It is hardly an exaggeration to say, that whilst reading and reflecting on the various facts given in this Memoir, we feel to be as near witnesses, as we can ever hope to be, of the creation of a new species on this earth.” Charles Darwin, Natural History Review: Quarterly Journal of Biological Science, 1863. From a review of “Contributions to an Insect Fauna of the Amazon Valley,” in which Henry Walter Bates gave an adaptive explanation for mimicry in Amazonian butterflies and argued that variation in mimicry might cause speciation 3 Abstract We are in the midst of a renaissance in speciation research. There is a return to Darwin’s belief in the role of natural selection in driving speciation, after a lengthy focus on geographic isolation and hybrid sterility. Here I describe the ecological, behavioural, and genetic bases of speciation in Heliconius cydno and Heliconius melpomene (Lepidoptera: Nymphalidae). The two species are sympatric in tropical rainforest across most of Central America and the foothills of the Andes. Ecological differentiation allows coexistence of these sister species despite rare hybridisation. Divergence in microhabitat and larval host plant use has reduced both the potential for gene flow and for competition. In Panama H. cydno uses most Passiflora species in closed canopy forest, whilst H. -
High Evolutionary Potential in the Chemical Defenses of an Aposematic Heliconius Butterfly
bioRxiv preprint doi: https://doi.org/10.1101/2020.01.14.905950; this version posted January 15, 2020. 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 4.0 International license. 1. GENERAL INFORMATION Article Type: Research Paper Title: High evolutionary potential in the chemical defenses of an aposematic Heliconius butterfly Authors: Mattila, Anniina L. K.1; Jiggins, Chris D.2; Opedal, Øystein H.1,3; Montejo-Kovacevich, Gabriela2; de Castro, Érika2; McMillan, William O.4; Bacquet, Caroline5; Saastamoinen, Marjo1,6 Author affiliations: 1. Research Centre for Ecological Change, Organismal and Evolutionary Biology Research Programme, University of Helsinki, Finland 2. Department of Zoology, University of Cambridge, UK 3. Department of Biology, Lund University, Sweden 4. Smithsonian Tropical Research Institute, Panama 5. Universidad Regional Amazónica de Ikiam, Tena, Ecuador 6. Helsinki Life Science Institute, University of Helsinki, Finland Orcid ID: Anniina L. K. Mattila: 0000-0002-6546-6528 Chris D. Jiggins: 0000-0002-7809-062X Øystein H. Opedal: 0000-0002-7841-6933 Gabriela Montejo-Kovacevich: 0000-0003-3716-9929 Érika de Castro: 0000-0002-4731-3835 William O. McMillan: 0000-0003-2805-2745 Caroline Bacquet: 0000-0002-1954-1806 Marjo Saastamoinen: 0000-0001-7009-2527 Keywords: chemical defense – aposematism – mimicry – Heliconius – cyanogenic glucosides – evolvability 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.01.14.905950; this version posted January 15, 2020. 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. -
Genetic Evidence for a Sibling Species of Heliconius Charithonia (Lepidoptera; Nymphalidae)
Biological Journal of the Linnean Society (1998), 64: 57±67. With 1 ®gure Article ID: bj970211 Genetic evidence for a sibling species of Heliconius charithonia (Lepidoptera; Nymphalidae) CHRIS D. JIGGINS* The Galton Laboratory, Department of Biology, University College London, 4 Stephenson Way, London NW1 2HE NEIL DAVIES University of Hawaii at Manoa, Center for Conservation Research and Training, Honolulu, HI 96822, U.S.A. Received 29 May 1997; accepted for publication 22 December 1997 Heliconius charithonia is a widespread species which, unlike many Heliconius, is non-mimetic and shows little racial diVerentiation. Only one form, `peruvianus', which occurs in the dry forest habitats of western Ecuador and Peru, has a distinct and clearly mimetic colour pattern. Here it was shown that H. peruvianus was distinct from H. charithonia bassleri at allozyme loci (D=0.25 over 22 loci). This diVerentiation was ten times greater than that between H. charithonia sampled from Ecuador and the Caribbean (D=0.027) and was consistent with analysis of mitochondrial sequence data (3.4±4% sequence divergence between H. peruvianus and H. charithonia). One individual with a H. peruvianus colour pattern and allozyme genotype was collected in an area where H. charithonia was known to be common, demonstrating that contact between the taxa occurs in western Ecuador. Furthermore, the allozyme genotype of another individual was heterozygous for four of ®ve diagnostic loci and was most likely an F1 hybrid between H. charithonia and H. peruvianus. These data imply that H. charithonia and H. peruvianus are distinct species which hybridize occasionally. This species pair show many similarities with H. -
Gilbert 1975 Coevolution and Heliconius.Pdf
ECOLOGICAL CONSEQUENCES OF A COEVOLVED MUTUALISM BUTTERFLIES AND PLANTS 2 11 BETWEEN BUTTERFLIES AND PLANTS* PASSIFLORA : CATERPILLAR FOOD Lawrence E. Gilbert Passiflora and several small genera of the Passifloraceae are the only larval host plants for Heliconius butterflies. Most of Department of Zoology the 350+ species recorded for the New World are tropical vines University of Texas which display some of the most striking intra- and inter-specific Austin, Texas 78712 leaf-shape and stipular variation known for plants (Killip, 1938). Locally, Passiflora species generally exist as low density popula tions in which individuals are difficult to find without the aid of INTRODUCTION egg-laying butterflies. Moreover, because of herbivore damage , plants are rarely in flower or fruiting condition. More interesting Apimal-plant mutualisms have been extensively described and however, is the pattern of Passiflora diversity among many l ocal yet, to date, we have no clear understanding of the general ecologi habitats . In spite of the vast number of Passiflora species cal and evolutionary importance of such interactions. Ecologist s available in the neo-tropics, local habitats always have less than have practically ignored mutualism when considering the kinds of 5% and more typically less than 2-3% of the 350 total.3 I will pro population interactions which explain community structure and pose causal explanation for both leaf shape variation and apparent dynamics.I Williamson (1972) accurately reflects the tone of limits to species packing in Passiflora in a later section of the recent temperate zone ecology in relegating mutualisms to the level paper. of interesting curiosity. As is true of perhaps most plants, Passiflora species possess In this paper, I present a qualitative and empirically derived a range of defensive chemicals which remove all but closely co model of the various order effects of mutualism between pollen and evolved herbivores from their list of predators and parasites. -
Dissecting Comimetic Radiations in Heliconius Reveals Divergent Histories of Convergent Butterflies
Dissecting comimetic radiations in Heliconius reveals divergent histories of convergent butterflies Swee-Peck Queka, Brian A. Countermanb, Priscila Albuquerque de Mourac, Marcio Z. Cardosoc, Charles R. Marshalld, W. Owen McMillanb, and Marcus R. Kronforsta,1 aFaculty of Arts and Sciences Center for Systems Biology, Harvard University, Cambridge, MA 02138; bDepartment of Genetics, North Carolina State University, Raleigh, NC 27695; cDepartment of Botany, Ecology and Zoology, Universidade Federal do Rio Grande do Norte, Natal RN 59072-970, Brazil; and dDepartments of Organismic and Evolutionary Biology and Earth and Planetary Sciences, Harvard University, Cambridge, MA 02138 Edited by May R. Berenbaum, University of Illinois at Urbana–Champaign, Urbana, IL, and approved March 16, 2010 (received for review October 6, 2009) Mimicry among Heliconius butterflies provides a classic example of tandem, from location to location (4, 9, 10). The racial variation coevolution but unresolved relationships among mimetic subspe- in H. erato and H. melpomene involves both major phenotypic cies have prevented examination of codiversification between shifts, such as the difference between rayed and postman pat- species. We present amplified fragment length polymorphism terns, as well as relatively minor variations, such as the subtle and mtDNA datasets for the major comimetic races of Heliconius differences among rayed populations or among postman pop- erato and H. melpomene. The AFLP data reveal unprecedented ulations. Two primary hypotheses have been proposed -
Mallet 1986C
RNATIONAL ❑ GEOGRAPHIC A SCIENTIFIC JOURNAL SPRING 1986 GREGARIOUS BUTTERFLIES ❑ YORUBA RITUAL I=1 DINOSAUR EVOLUTION ❑ TROPICAL ISLAND WATER BALANCE 0. , James Mallet Gregarious Roosting and Home Range in Heliconius Butterflies Individual Heliconius butterfliesfly within a restricted area by day and roost gregariously at night. In premosting gatherings, individuals `fan" already roosted conspecifics. Fanning does not have an aggressive function, as has been previously suggested; it is a courtshiplike behav- ior, although it never leads to mating. The behavior occurs with high frequencyjust before roosting and torpidity, rather Mart during the day when mating takes place. Individuals also fan detul ir rdividuals of Their own and other species, and even crude cardboard models. Fan n ing is probably a means of testingfor species-specific stimuli that enable indi- viduals to aggregate. Roosts of H. erato do not consist of discrete farn P groups; both ten- eral and older butterflies disperse among roosting groups. The home ranges of individual erato are independent of those of their roostmates, and frequently overlap with home ranges of individuals from other roosts. The loose population structure found in erato contrasts with that required for kin selection models of the evolution of warning color and unpalatability. There is little predation of Heliconius near the roost, but foraging birds often disturb erato during the early morning, before the roosts disperse. The selective value ofgregarious roosting is discussed. Heliconius butterflies inhabit tropical forests and woods from the south- ern United States to Argentina. Their long wings, which allow a lazy, hovering flight, are usually black with gaudy patches of red, orange, yellow, white, or iridescent blue. -
Rapid Speciation, Hybridization and Adaptive Radiation in the Heliconius Melpomene Group James Mallet
//FS2/CUP/3-PAGINATION/SPDY/2-PROOFS/3B2/9780521883184C10.3D 177 [177–194] 19.9.2008 3:02PM CHAPTER TEN Rapid speciation, hybridization and adaptive radiation in the Heliconius melpomene group james mallet In 1998 it seemed clear that a pair of ‘sister species’ of tropical butterflies, Heliconius melpomene and Heliconius cydno persisted in sympatry in spite of occasional although regular hybridization. They speciated and today can coexist as a result of ecological divergence. An important mechanism in their speciation was the switch in colour pattern between different Mu¨ llerian mimicry rings, together with microhabitat and host-plant shifts, and assortative mating pro- duced as a side effect of the colour pattern differences. An international con- sortium of Heliconius geneticists has recently been investigating members of the cydno superspecies, which are in a sense the ‘sisters’ of one of the original ‘sister species’, cydno. Several of these locally endemic forms are now recognized as separate species in the eastern slopes of the Andes. These forms are probably most closely related to cydno, but in several cases bear virtually identical colour patterns to the local race of melpomene, very likely resulting from gene transfer from that species; they therefore can and sometimes do join the local mimicry ring with melpomene and its more distantly related co-mimic Heliconius erato. I detail how recent genetic studies, together with ecological and behavioural observations, suggest that the shared colour patterns are indeed due to hybrid- ization and transfer of mimicry adaptations between Heliconius species. These findings may have general applicability: rapidly diversifying lineages of both plants and animals may frequently share and exchange adaptive genetic variation. -
Passiflora (Passifloraceae) Defenses Against Heliconius Cydno (Nymphalidae: Heliconiinae) Oviposition
Passiflora (Passifloraceae) defenses against Heliconius cydno (Nymphalidae: Heliconiinae) oviposition Kim Khuc Department of Integrative Biology, University of California, Berkeley ABSTRACT The purpose of this study was to determine the relative effectiveness of Passiflora defenses: elevated levels of cyanide, egg mimics, and variable leaf shapes, against oviposition from Heliconius cydno. The effectiveness of these defenses would reveal H. cydno’s preferences for oviposition sites and the primary criteria it uses when evaluating oviposition sites. Forty-two Passiflora oerstedii vines from the Monteverde Butterfly Garden, in Costa Rica, were divided into three treatments that added either cyanide, false eggs, or changed the shape of young leaves. Another twelve Passiflora coccinea vines were used in a second experiment that added false eggs to the young leaves, tendrils, and meristems. The results show trends that the various treatments deterred oviposition. Out of the 11 total eggs laid on leaves in the cyanide treatment, 82% of the total number of eggs was on the control leaves, then 9% on the methanol leaves and 9% on the methanol-cyanide leaves, indicating that the chemical cues from methanol discourage oviposition by H. cydno (χ2 = 11.64, df = 2, p = 0.003). For the vines with false eggs, out of a total of 19 eggs, 68% of the eggs were on the control leaves (χ 2 = 2.58, df = 1, p = 0.11). Lastly, the control leaves of the modified leaf shape experiment had 73% of the total number of eggs, 15, while the modified leaves had 27% (χ 2 = 3.23, df = 1, p = 0.07). These trends show that H. -
A Remarkable New Subspecies of Heliconius Kluk from Northeastern Venezuela (Lepidoptera: Nymphalidae)
Rev. perú. Entomol. 45: 71 - 74. Diciembre 2006 71 A remarkable new subspecies of Heliconius Kluk from northeastern Venezuela (Lepidoptera: Nymphalidae) Andrés M. Orellana1 SUMMARY ORELLANA AM. 2006. A remarkable new subspecies of Heliconius Kluk from northeastern Venezuela (Lepidoptera: Nymphalidae). Rev. perú. Entomol. 45.- A remarkable new subspecies of the Amazonian and Guianan Heliconius burneyi (Hübner) is described from the state of Sucre in northeastern Venezuela. Its wing pattern resembles that of the peculiar heliconiine Neruda metharme (Erichson), which is absent in Sucre. Considering that races of H. burneyi are variations on basically the same theme, a new wing pattern element for this species is recognized. Natural selection, shifting balance and relictual mimicry may explain its occurrence. Key Words: Aposematísm, evolución, Paria, taxonomy. RESUMEN ORELLANA AM. 2006. Una notable subespecie nueva de Heliconius Kluk del nororiente de Venezuela (Lepidoptera: Nymphalidae). Rev. perú. Entomol. 45- Se describe una notable subespecie de la mariposa amazónica y guayanesa Heliconius burneyi (Hübner), del estado Sucre en el nororiente de Venezuela. El patrón de coloración de las alas la acerca a la peculiar especie de heliconiino Neruda metharme (Erichson), que no ocurre en Sucre. Dado que el patrón de coloración alar de las diferentes subespecies de H. burneyi no representa básicamente más que variaciones de un mismo tema, se reconoce un nuevo elemento en el patrón de coloración de la especie. Se presenta hipótesis sobre selección natural, balance cambiante y mimetismo relictual que se esgrimen para explicar su ocurrencia. Palabras clave: Aposematismo, evolución, Paria, taxonomía. Introduction hitherto unknown and striking subspecies of the Amazonian and Guianan Heliconius burneyi The Heliconiini, a tribe of the nymphalid (Hübner, 1831), which I describe herein. -
Curran Thesis Full.Pdf
An exploration of the parallel evolution of iridescent structural colour in Heliconius butterflies Emma V. Curran A thesis submitted in partial fulfilment of the requirements for the degree of Doctor of Philosophy The University of Sheffield Faculty of Science Department of Animal and Plant Sciences Submission Date September 2018 2 Abstract Understanding how selection interacts with genetic variation to produce biodiversity is a central theme in evolutionary biology. Many studies have taken advantage of the rich diversity of colouration in animals to tackle this, as colour is both ecologically relevant and a clearly visible phenotype. This has carried over into the ‘omics’ era, with plenty of studies addressing evolutionary questions by examining the genomics of colouration in natural populations. These studies tend to focus on discrete colour variation and pigmentation. However, most phenotypic variation is continuous, and little is known about the genetics of structural colour. Heliconius butterflies display warning colouration that boasts both striking diversity, alongside near-perfect convergence between mimetic species. Repeated evolution of pigment colour patterns is driven by the repeated use of a small set of genes. On the western slopes of the Andes, convergent iridescence has also evolved between the co-mimics Heliconius erato and Heliconius melpomene, which appears to vary continuously. In this thesis I (1) describe clinal variation in iridescence across hybrid zones between iridescent and non-iridescent subspecies of H. erato and H. melpomene and highlight a common selective agent (mimetic warning colouration), yet different migration-selection balance between the species. 2) I demonstrate a striking difference in levels of population structure between the co-mimics across their hybrid zones.