Phylogenetic systematics of Colotis and associated genera (Lepidoptera: Pieridae): evolutionary and taxonomic implications
2011; Wiley; Volume: 49; Issue: 3 Linguagem: Inglês
10.1111/j.1439-0469.2011.00620.x
ISSN1439-0469
AutoresVazrick Nazari, Torben Bjerregaard Larsen, David C. Lees, Oskar Brattström, Thierry Bouyer, Guy Van de Poel, Paul D. N. Hebert,
Tópico(s)Genetic diversity and population structure
ResumoJournal of Zoological Systematics and Evolutionary ResearchVolume 49, Issue 3 p. 204-215 Phylogenetic systematics of Colotis and associated genera (Lepidoptera: Pieridae): evolutionary and taxonomic implications Systématique et Phylogenie de Colotis et des genres apparentés (Lépidoptères: Pieridae): implications évolutives et taxonomiques Vazrick Nazari, Vazrick Nazari Department of Integrative Biology, University of Guelph, Guelph, ON, Canada Present address: Agriculture and Agri-Food Canada, 3058-C KW Neatby Bldg, 960 Carling Avenue, Ottawa, ON, K1A 0C6 Canada.Search for more papers by this author Torben B. Larsen, Torben B. Larsen Jacobys alle 2, 1806 Frederiksberg C, DenmarkSearch for more papers by this author David C. Lees, David C. Lees Department of Entomology, Natural History Museum, London, UK Centre de Recherche d' Orléans, INRA, UR 633 Zoologie Forestière, Orléans, FranceSearch for more papers by this authorOskar Brattström, Oskar Brattström University Museum of Zoology, Cambridge, UKSearch for more papers by this authorThierry Bouyer, Thierry Bouyer 57 rue Genot, B-4032 Chênée, BelgiumSearch for more papers by this authorGuy Van de Poel, Guy Van de Poel Kerkhoflei 54, Hofstade (Zemst), BelgiumSearch for more papers by this author Paul D. N. Hebert, Paul D. N. Hebert Department of Integrative Biology, University of Guelph, Guelph, ON, CanadaSearch for more papers by this author Vazrick Nazari, Vazrick Nazari Department of Integrative Biology, University of Guelph, Guelph, ON, Canada Present address: Agriculture and Agri-Food Canada, 3058-C KW Neatby Bldg, 960 Carling Avenue, Ottawa, ON, K1A 0C6 Canada.Search for more papers by this author Torben B. Larsen, Torben B. Larsen Jacobys alle 2, 1806 Frederiksberg C, DenmarkSearch for more papers by this author David C. Lees, David C. Lees Department of Entomology, Natural History Museum, London, UK Centre de Recherche d' Orléans, INRA, UR 633 Zoologie Forestière, Orléans, FranceSearch for more papers by this authorOskar Brattström, Oskar Brattström University Museum of Zoology, Cambridge, UKSearch for more papers by this authorThierry Bouyer, Thierry Bouyer 57 rue Genot, B-4032 Chênée, BelgiumSearch for more papers by this authorGuy Van de Poel, Guy Van de Poel Kerkhoflei 54, Hofstade (Zemst), BelgiumSearch for more papers by this author Paul D. N. Hebert, Paul D. N. Hebert Department of Integrative Biology, University of Guelph, Guelph, ON, CanadaSearch for more papers by this author First published: 19 April 2011 https://doi.org/10.1111/j.1439-0469.2011.00620.xCitations: 14 Corresponding author: Vazrick Nazari ([email protected])Contributing authors: Torben B. Larsen ([email protected]), David C. Lees ([email protected]), Oskar Brattström ([email protected]), Thierry Bouyer ([email protected]), Guy Van de Poel ([email protected]), Paul D. N. Hebert ([email protected]) Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Abstracten We investigated the genetic diversity and phylogenetic placement of the butterflies in the genus Colotis and eight related pierid genera using sequence information from two mitochondrial and two nuclear genes. To establish the status of species, we initially barcoded 632 specimens representative of all genera and most species and subspecies in those genera. A subset was then selected for phylogenetic analysis where additional gene regions were sequenced: 16S rRNA (523 bp), EF-1α (1126 bp) and wg (404 bp). DNA barcode results were largely congruent with the traditional classification of species in the Colotis group, but deep splits or lack of genetic divergence in some cases supported either species-level differentiation or synonymy. Despite using information from four genes, the deeper nodes in our phylogeny were not strongly supported, and monophyly of the 'Colotis group' and the genera Colotis and Eronia could not be established. To preserve the monophyly of Colotis, we revive the genus Teracolus for three outlying species previously in Colotis (i.e. Colotis eris, Colotis subfasciatus and Colotis agoye), as well as the genus Afrodryas for Eronia leda. The position of Calopieris is unresolved although it appears to be well outside the molecular variation in Colotis (s.l.). A dispersal/vicariance analysis suggested that major diversification in Colotis (s.str.) occurred in Africa with subsequent dispersal to India and Madagascar. Résuméfr Nous avons étudié la diversité génétique et la position phylogénétique des papillons du genre Colotis et de huit autres genres de Piéridés apparentés, à l'aide de quatre gènes, deux mitochondriaux et deux nucléaires. Afin d'établir le statut taxonomique des espèces, nous avons dans un premier temps établi les codes-barres génétiques de 523 spécimens représentant tous les genres et la plupart des espèces et sous-espèces constituantes. Nous avons ensuite choisi un sous-ensemble de ces taxons que nous avons soumis à une analyse phylogénétique après avoir établi les séquences de portions des gènes suivants : 16S ARNr (523 bp), EF-1α (1126 bp) et wg (404 bp). Les résultats des codes-barres génétiques concordent bien dans l'ensemble avec la classification traditionnelle des espèces du groupe Colotis, mais quelques cas de divergence génétique prononcée, ou à l'inverse des cas de similitudes génétiques, indiquent soit des différenciations spécifiques insoupçonnées, soit des cas de synonymie. Malgré l'analyse de données provenant de quatre gènes, les branchements de base de notre arbre phylogénétique sont peu fiables et nous n'avons pas réussi àétablir la monophylie du 'groupe Colotis', ni des genres Colotis et Eronia. Afin de maintenir la monophylie de Colotis, nous avons rétabli le genre Teracolus pour y transférer trois espèces de Colotis (Colotis eris, Colotis subasciatus et Colotis agoye), et le genre Afrodryas pour inclure E. leda. La position de Calopieris n'est pas résolue mais ce genre présente un profil bien au-dehors de la variation observée dans Colotis (s.l.). Une analyse de vicariance/dispersion indique qu'une diversification importante des Colotis (s. str.) aurait eu lieu en Afrique, suivie d'une dispersion vers l'Inde et Madagascar. References Ackery PR, Smith CR, Vane-Wright RI (1995) Carcasson's African Butterflies: An Annotated Catalogue of the Papilionoidea and Hesperioidea of the Afrotropical Region. British Museum (Natural History), London, UK. Aduse-Poku K, Vingerhoedt E, Wahlberg N (2009) Out-of-Africa again: a phylogenetic hypothesis of the genus Charaxes (Lepidoptera: Nymphalidae) based on five gene regions. Mol Phylogenet Evol 53: 463– 478. Aubert J, Legal L, Descimon H, Michel F (1999) Molecular phylogeny of swallowtail butterflies of the tribe Papilionini (Papilionidae, Lepidoptera). Mol Phylogenet Evol 12: 156– 167. Aurivillius C (1925) Pieridae. In: Seitz A (ed.), Die Gross-Schmetterlinge der Erde. 13. Band: Die Afrikanischen Tagfalter. Alfred Kernen, Stuttgart, pp 29– 69. Bernardi G (1954) Notes sur la taxonomie de deux Colotis malgaches. Le Naturaliste malgache 6: 57– 60. Boisduval JBA (1847) Catalogue des Lépidoptères recuellis par M. Delegorgue pendant les années 1838–1844 à Port-Natal, au pays de Amazoulous et dans la contrée de Massilicatzi. In: Delegorgue A (ed.), Voyage dans l'Afrique australe, 2: 585– 602. Bouyer T (2010) Colotis praeclarus (Butler, 1886) (Lepidoptera, Pieridae). Entomologia Africana 15: 22– 24. Braby MF (2005) Afrotropical mistletoe butterflies: larval food plant relationships of Mylothris Hübner (Lepidoptera: Pieridae). J Nat Hist 39: 499– 513. Braby MF, Pierce NE (2007) Systematics, biogeography and diversification of the Indo-Australian genus Delias Hübner (Lepidoptera: Pieridae): phylogenetic evidence supports an 'out-of-Australia' origin. Syst Entomol 32: 2– 25. Braby MF, Trueman JWH (2006) Evolution of larval host plant associations and adaptive radiation in pierid butterflies. J Evol Biol 19: 1677– 1690. Braby MF, Vila R, Pierce NE (2006) Molecular phylogeny and systematics of the Pieridae (Lepidoptera: Papilionoidea): higher classification and biogeography. Zool J Linn Soc 147: 239– 275. Braby MF, Pierce NE, Vila R (2007) Phylogeny and historical biogeography of the subtribe Aporiina (Lepidoptera: Pieridae): implications for the origin of Australian butterflies. Biol J Linn Soc 90: 413– 440. Brower AVZ, De Salle R (1994) Practical and theoretical considerations for choice of a DNA sequence region in insect molecular systematics, with a short review of published studies using nuclear gene regions. Ann Entomol Soc Am 87: 702– 716. Butler AG (1869) Descriptions of new Rhopalocera from the collection of Herbert Druce Esq. Cistula Entomol 1: 1– 16. Butler AG (1876) Revision of the lepidopterous genus Teracolus with descriptions of the new species. Proc Zool Soc Lond 1876: 126– 165. Carcasson RH (1964) A preliminary survey of the zoogeography of African butterflies. East Afr Wildl J 2: 122– 157. [reprinted in Ackery et al. 1995]. Caterino MS, Sperling FAH (1999) Papilio phylogeny based on mitochondrial cytochrome oxidase I and II genes. Mol Phylogenet Evol 11: 122– 137. Caterino MS, Reed RD, Kuo MM, Sperling FAH (2001) A partitioned likelihood analysis of swallowtail butterfly phylogeny (Lepidoptera: Papilionidae). Syst Biol 50: 106– 127. Chew FS, Watt WB (2006) The Green-veined White (Pieris napi L.), its pierine relatives, and the systematics dilemmas of divergent character sets (Lepidoptera, Pieridae). Biol J Linn Soc 88: 413– 435. Cogan BH, Hutson AM (1971) Preliminary observations on the affinities and composition of the insect fauna of Aldabra. Phil Trans R Soc Lond B Biol Sci 260: 315– 325. Cramer P (1780) De Uitlandsche Kapellen voorkomende in de drie waereld-deelen Asia, Africa en America. Amsteldam and Utrecht. 4 [part]: 1– 28. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214. Drury D (1773) Illustrations of Natural History. White, London. Fabricius JC (1775) Systema Entomologiae. Flensburgi and Lipsiae. Gardner D, Howarth B (2007) A butterfly migration: blue-spotted Arab at Jabal Barakah, western Abu Dhabi. Tribulus 17: 98. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696– 704. Hajibabaei M, Janzen DH, Burns JM, Hallwachs W, Hebert PDN (2006) DNA barcodes distinguish species of tropical Lepidoptera. Proc Natl Acad Sci USA 103: 968– 971. Hausmann A, Hebert PDN, Mitchell A, Rougerie R, Sommerer M, Edwards T, Young CJ (2009) Revision of the Australian Oenochroma vinaria Guenée, 1858 species-complex (Lepidoptera: Geometridae, Oenochrominae): DNA barcoding reveals cryptic diversity and assesses status of type specimen without dissection. Zootaxa 2239: 1– 21. Hebert PDN, Cywinska A, Ball SL, Dewaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B Biol Sci 270: 313– 321. Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA 101: 14812– 14817. Hecq J (1975) Le complexe Colotis eucharis F. (Lepidopt. Pieridae). Lambillionea 75: 4– 10. Henning GA, Henning SF, Joannou JG, Woodhall SE (1997) Living Butterflies of the Southern Africa. Umdaus Press, Hatfield, South Africa. Hesselbarth G, Van Oorschot H, Wagener S (1995) Die Tagfalter der Türkei, I. Selbstverlag Sigbert Wagener, Bocholt. Howe K, Bateman A, Durbin R (2002) QuickTree: building huge neighbour-joining trees of protein sequences. Bioinformatics 18: 1546– 1547. Hübner J (1823) Sammlung exotischer Schmetterlinge, 2. In: Hübner J (1819–1827). Jacob Hübner Verlag, Augsburg. Ivanova NV, Dewaard JR, Hebert PDN (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Mol Ecol Notes 6: 998– 1002. Keane TM, Naughton TJ, McInerney JO (2007) MultiPhyl: a high-throughput phylogenomics webserver using distributed computing. Nucleic Acids Res 35: W33– W37. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16: 111– 120. Klots AB (1933) A generic revision of the Pieridae (Lepidoptera) together with a study of the male genitalia. Entomol Am (NS) 12: 139– 242. Klug JCF (1829). Symbolae physicae seu icones et descriptiones insectorum quae ex itinere per Africam borealem et Asiam occidentalem Fridrichi Guilelmi Hemprich et Christiani Godofredi Ehrenberg Medicinae et Chirurgiae Doctorum studio novae aut illustratae redierunt. Decas Prima (1929), Berolini: ex Officina Academia, Impensis G. Reimer. Kodandaramaiah U, Wahlberg N (2007) Out-of-Africa origin and dispersal mediated diversification of the butterfly genus Junonia (Nymphalidae: Nymphalinae). J Evol Biol 20: 2181– 2191. Kodandaramaiah U, Wahlberg N (2009) Phylogeny and biogeography of Coenonympha butterflies (Nymphalidae: Satyrinae) – patterns of colonization in the Holarctic. Syst Entomol 34: 315– 323. Kodandaramaiah U, Peña C, Braby MF, Grund R, Müller CJ, Nylin S, Wahlberg N (2010) Phylogenetics of Coenonymphina (Nymphalidae: Satyrinae) and the problem of rooting rapid radiations. Mol Phylogenet Evol 54: 386– 394. Larsen TB (1984) Butterflies of Saudi Arabia and its Neighbours. Stacey International, London. Larsen TB (1991) The Butterflies of Kenya and their Natural History. Oxford University Press, Oxford. Larsen TB (1992) On the status of Colotis agoye (Wallengren, 1857) and its subspecies. Metamorphosis 3: 5– 10. Larsen TB (2005) Butterflies of West Africa. Apollo Books, Stenstrup, Denmark. Lohman DJ, Peggie D, Pierce NE, Meier R (2008) Phylogeography and genetic diversity of a widespread Old World butterfly, Lampides boeticus (Lepidoptera: Lycaenidae). BMC Evol Biol 8: 301. Maddison WP, Maddison DR (2009) Mesquite: a modular system for evolutionary analysis. Version 2.72. Available from: http://mesquiteproject.org (accessed December 2009). Monaghan MT, Gattolliat JL, Sartori M, Elouard JM, James H, Derleth P, Glaizot O, de Moor F, Vogler AP (2005) Trans-oceanic and endemic origins of the small minnow mayflies (Ephemeroptera, Baetidae) of Madagascar. Proc R Soc Lond B Biol Sci 272: 1829– 1836. Morinaka S, Miyata T, Tanaka K (2002) Molecular phylogeny of the Eichhorni group of Delias Hübner, 1819 (Lepidoptera: Pieridae). Mol Phylogenet Evol 23: 276– 287. Narita S, Nomura M, Kato Y, Fukatsu T (2006) Genetic structure of sibling butterfly species affected by Wolbachia infection sweep: evolutionary and biogeographical implications. Mol Ecol 15: 1095– 1108. Nazari V (2003) Butterflies of Iran. Dayereye Sabz publications, Tehran. Nazari V, Zakharov EV, Sperling FAH (2007) Phylogeny, historical biogeography, and taxonomic ranking of Parnassiinae (Lepidoptera, Papilionidae) based on morphology. Mol Phylogenet Evol 42: 131– 156. Peters W (1952) A Provisional Checklist of the Butterflies of the Ethiopian Region. E.W. Classey, Feltham, Middlesex. Rambaut A (2002) Sequence alignment editor, version 2.0. Available from: http://evolve.zoo.ox.ac.uk/software/Se-Al/Main.html (accessed December 2009). Ronquist F (1997) DIVA (dispersal-vicariance analysis) ver. 1.2. Computer program and manual. Available from http://www.ebc.uu.se/systzoo/research/diva/diva.html (accessed January 2010). Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572– 1574. Sharpe EM (18981902) Monographiae Entomologicae. 1. A Monograph of the Genus Teracolus. Lovell Reeve, London. Sorenson MD, Franzosa EA (2007) TREEROT, Version 3. Boston University, Boston, MA. Available from http://people.bu.edu/msoren/TreeRot.html (accessed December 2009). Staudinger O (1884) Exotische Tagfalter in systematischer Reinfolge mit Berücksichtigung neuer Arten. In: Staudinger O, Schatz E (eds), Exotische Schmetterlinge. 4, Theil I, VII, pp 43– 44. Stavenga DG, Arikawa K (2006) Evolution of color and vision of butterflies. Arthropod Struct Dev 35: 307– 318. Stavenga DG, Leertouwer HL (2007) Colourful butterfly wings: scale stacks, iridescence and sexual dichromatism of Pieridae. Entomol Ber (Amsterdam) 67: 158– 164. Stavenga DG, Giraldo MA, Hoenders BJ (2006) Reflectance and transmittance of light scattering scales stacked on the wings of pierid butterflies. Optics Express 14: 4880– 4890. Stoneham HF (1957) Two new generic names, and new subspecies and forms of Pieridae. Bull. Stoneham Mus. 70: 1– 3. Suárez NM, Betancor E, Pestano J (2009) Intraspecific evolution of Canarian Euchloe (Lepidoptera: Pieridae) butterflies, based on mtDNA sequences. Mol Phylogenet Evol 51: 601– 605. Swainson W (1833) (ed.) Zoological illustrations, or original figures and descriptions of new, rare or interesting animals selected chiefly from the classes of ornithology, entomology and conchology, (2) 3, [ix]. James Moyes, London. Swinhoe C (1909) New species of Indo-Malayan and African Lepidoptera. Ann Mag Nat Hist 3: 89– 98. Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, MA. Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56: 564– 577. Talbot G (1939) Revisional notes on the genus Colotis Hubn. (Lepid. Pieridae) with a systematic list. Trans R Entomol Soc Lond 88: 173– 233. Templeton AR, Routman E, Phillips CA (1995) Separating population structure from population history: a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the tiger salamander, Ambystoma tigrinum. Genetics 140: 767– 782. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTALX Windows inference: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Res 25: 4876– 4882. Wahlberg N, Braby MF, Brower AVZ, de Jong R, Lee MM, Nylin S, Pierce N, Sperling FAH, Vila R, Warren AD, Zakharov E (2005) Synergistic effects of combining morphological and molecular data in resolving the phylogeny of butterflies and skippers. Proc R Soc Lond B Biol Sci 272: 1577– 1586. Wallengren HDJ (1857) Kafferlandets Dag-fjärilar, insamlade åren 1838–1845 af J. A. Wahlberg/Lepidoptera Rhopalocera in Terra Caffrorum annis 1838–1845 collecta a J. A. Wahlberg. K Svenska Vetensk Akad Handl 2: 1– 55. Wheat CW, Watt WB (2008) A mitochondrial-DNA-based phylogeny for some evolutionary-genetic model species of Colias butterflies (Lepidoptera, Pieridae). Mol Phylogenet Evol 47: 893– 902. Wheat CW, Vogel H, Wittstock U, Braby MF, Underwood D, Mitchell-Olds T (2007) The genetic basis of a plant–insect coevolutionary key innovation. Proc Natl Acad Sci USA 104: 20427– 20431. Wiemers M, Keller A, Wolf M (2009) ITS2 secondary structure improves phylogeny estimation in a radiation of blue butterflies of the subgenus Agrodiaetus (Lepidoptera: Lycaenidae: Polyommatus). BMC Evol Biol 9: 300. Wijnen B, Leertouwer HL, Stavenga DG (2007) Colors and pterin pigmentation of pierid butterfly wings. J Insect Physiol 53: 1206– 1217. Xu L, Hao JS, Zhu GP, Yin XB, Pan HC, Huang DY, Zhang XP (2007) Molecular phylogenetic relationships of some species and genera in Pierinae and Coliadnae [Coliadinae] (Pieridae) based on partial sequence of mitochondrial CO I and Cyt b genes. Acta Zootaxon Sinica 32: 842– 850. Zakharov EV, Smith CR, Lees DC, Cameron A, Vane-Wright RI, Sperling FAH (2004) Independent gene phylogenies and morphology demonstrate a Malagasy origin for a wide-ranging group of swallowtail butterflies. Evolution 58: 2763– 2782. Citing Literature Supporting Information Figure S1. TCS haplotype networks for cytochrome oxidase I barcodes in the Colotis vesta (a) and Colotis phisadia (b) groups of species. Table S1. Material examined and GenBank Accession numbers. Table S2. Taxa and sequences used in phylogenetic reconstructions. Table S3. Summary of character partitions. Table S4. Support values for clades supported through both maximum likelihood and Bayesian analyses. Filename Description JZS_620_sm_fS1.TIF4.2 MB Supporting info item JZS_620_sm_tS1.xls334.5 KB Supporting info item JZS_620_sm_tS2.xls35 KB Supporting info item JZS_620_sm_tS3.xls14 KB Supporting info item JZS_620_sm_tS4.xls28.5 KB Supporting info item Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article. Volume49, Issue3August 2011Pages 204-215 ReferencesRelatedInformation
Referência(s)