Wolbachia infections mimic cryptic speciation in two parasitic butterfly species, Phengaris teleius and P. nausithous (Lepidoptera: Lycaenidae)

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Ritter, Sylvia ^a   Michalski, Stefan G ^a   Settele, Josef ^a,b   Wiemers, Martin ^a   Fric, Zdenek F ^c   Sielezniew, Marcin ^d   Šašić, Martina ^e   Rozier, Yves ^f   Durka, Walter ^a,b  

^a HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^b GERMAN CENTRE FOR INTEGRATIVE BIODIVERSITY RESEARCH IDIV HALLE JENA LEIPZIG   (Germany)

^c INSTITUTE OF MATHEMATICS   (Czech Republic)

^d UNIVERSITY OF BIALYSTOK   (Poland)

^e CROATIAN NATURAL HISTORY MUSEUM   (Croatia)

^f CEDS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

ARTICLE; BACTERIAL GENOME; BACTERIUM IDENTIFICATION; CLADISTICS; CONTROLLED STUDY; CRYPTIC (ERA); DNA SEQUENCE; GENOME ANALYSIS; HAPLOTYPE; HOST RANGE; LEPIDOPTERA; MICROSATELLITE MARKER; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENGARIS NAUSITHOUS; PHENGARIS TELEIUS; PHYLOGEOGRAPHY; RICKETTSIACEAE INFECTION; SEQUENCE ANALYSIS; SPECIES DIFFERENTIATION; SPECIES DIVERSITY; WOLBACHIA;

ANIMALS; ANTS; ASIA; BUTTERFLIES; CELL NUCLEUS; ELECTRON TRANSPORT COMPLEX IV; EUROPE; FEMALE; GENETIC MARKERS; GENETIC SPECIATION; GENETIC VARIATION; GENOME, MITOCHONDRIAL; INSECT PROTEINS; MICROSATELLITE REPEATS; PHYLOGENY; PHYLOGEOGRAPHY; SEQUENCE ANALYSIS, DNA; SYMBIOSIS; WOLBACHIA;

EID: 84892405310     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078107     Document Type: Article

References (109)

1. Bickford D, Lohman DJ, Sodhi NS, Ng PK, Meier R, et al. (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22: 148-155.
2. Pfenninger M, Schwenk K (2007) Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evol Biol 7: 121.
3. Huyse T, Poulin R, Theron A (2005) Speciation in parasites: a population genetics approach. Trends Parasitol 21: 469-475.
4. Hebert PD, 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 U S A 101: 14812-14817.
5. Hebert PD, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc Biol Sci 270: 313-321.
6. McBride CS, Van Velzen R, Larsen TB (2009) Allopatric origin of cryptic butterfly species that were discovered feeding on distinct host plants in sympatry. Mol Ecol 18: 3639-3651.
7. Galtier N, Nabholz B, Glemin S, Hurst GDD (2009) Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol Ecol 18: 4541-4550.
8. Duplouy A, Hurst GDD, O'Neill SL, Charlat S (2010) Rapid spread of male-killing Wolbachia in the butterfly Hypolimnas bolina. J Evol Biol 23: 231-235.
9. Munoz AG, Baxter SW, Linares M, Jiggins CD (2011) Deep mitochondrial divergence within a Heliconius butterfly species is not explained by cryptic speciation or endosymbiotic bacteria. BMC Evol Biol 11: 358.
10. Wiemers M, Fiedler K (2007) Does the DNA barcoding gap exist? - a case study in blue butterflies (Lepidoptera: Lycaenidae). Front Zool 4: 8.
11. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6: 741-751.
12. Russell JA, Funaro CF, Giraldo YM, Goldman-Huertas B, Suh D, et al. (2012) A veritable menagerie of heritable bacteria from ants, butterflies, and beyond: broad molecular surveys and a systematic review. Plos One 7: e51027.
13. Hurst GD, Jiggins FM (2005) Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc R Soc Biol Sci Ser B 272: 1525-1534.
14. Werren JH, Zhang W, Guo LR (1995) Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc R Soc Biol Sci Ser B 261: 55-63.
15. Caspari E, Watson GS (1959) On the evolutionary importance of cytoplasmic sterility in mosquitos. Evolution 13: 568-570.
16. Hoffmann AA, Turelli M (1988) Unidirectional incompatibility in Drosophila simulans - Inheritance, geographic variation and fitness effects. Genetics 119: 435-444.
17. Hatcher MJ (2000) Persistence of selfish genetic elements: population structure and conflict. Trends Ecol Evol 15: 271-277.
18. 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.
19. Hurst GDD, Jiggins FM, von der Schulenburg JHG, Bertrand D, West SA, et al. (1999) Male-killing Wolbachia in two species of insect. P R Soc B 266: 735-740.
20. Bordenstein SR, Marshall ML, Fry AJ, Kim U, Wernegreen JJ (2006) The tripartite associations between bacteriophage, Wolbachia, and arthropods. Plos Pathog 2: 384-393.
21. Egas M, Vala F, Breeuwer JAJ (2002) On the evolution of cytoplasmic incompatibility in haplodiploid species. Evolution 56: 1101-1109.
22. Jansen VAA, Turelli M, Godfray HCJ (2008) Stochastic spread of Wolbachia. P R Soc B 275: 2769-2776.
23. Mouton L, Henri H, Bouletreau M, Vavre F (2006) Effect of temperature on Wolbachia density and impact on cytoplasmic incompatibility. Parasitology 132: 49-56.
24. Reynolds KT, Thomson LJ, Hoffmann AA (2003) The effects of host age, host nuclear background and temperature on phenotypic effects of the virulent Wolbachia strain popcorn in Drosophila melanogaster. Genetics 164: 1027-1034.
25. Whitworth TL, Dawson RD, Magalon H, Baudry E (2007) DNA barcoding cannot reliably identify species of the blowfly genus Protocalliphora (Diptera: Calliphoridae). P R Soc B 274: 1731-1739.
26. Bordenstein SR, O'Hara FP, Werren JH (2001) Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature 409: 707-710.
27. Hurst GDD, Werren JH (2001) The role of selfish genetic elements in eukaryotic evolution. Nat Rev Genet 2: 597-606.
28. Dasmahapatra KK, Elias M, Hill RI, Hoffman JI, Mallet J (2010) Mitochondrial DNA barcoding detects some species that are real, and some that are not. Mol Ecol Resources 10: 264-273.
29. Smith MA, Bertrand C, Crosby K, Eveleigh ES, Fernandez-Triana J, et al. (2012) Wolbachia and DNA barcoding insects: patterns, potential, and problems. Plos One 7: e36514.
30. Heath BD, Butcher RDJ, Whitfield WGF, Hubbard SF (1999) Horizontal transfer of Wolbachia between phylogenetically distant insect species by a naturally occurring mechanism. Curr Biol 9: 313-316.
31. Pierce NE, Braby MF, Heath A, Lohman DJ, Mathew J, et al. (2002) The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annu Rev Entomol 47: 733-771.
32. Thomas JA, Settele J (2004) Evolutionary biology - Butterfly mimics of ants. Nature 432: 283-284.
33. van Swaay C, Collins S, Dušej G, Maes D, Munguira ML, et al. (2012) Dos and Don'ts for butterflies of the Habitats Directive of the European Union. Nature Conservation 1: 73-153.
34. Munguira ML, Martín J, editors (1999) Action plan for Maculinea butterflies in Europe. Nature and environment. Strasbourg: Council of Europe.
35. Sielezniew M, Rutkowski R, Ponikwicka-Tyszko D, Ratkiewicz M, Dziekanska I, et al. (2012) Differences in genetic variability between two ecotypes of the endangered myrmecophilous butterfly Phengaris (= Maculinea) alcon- the setting of conservation priorities. Insect Conserv Divers 5: 223-236.
36. Patricelli D, Sielezniew M, Ponikwicka-Tyszko D, Ratkiewicz M, Bonelli S, et al. (2013) Contrasting genetic structure of rear edge and continuous range populations of a parasitic butterfly infected by Wolbachia. BMC Evol Biol 13: 14.
37. Salunke BK, Salunkhe RC, Dhotre DP, Walujkar SA, Khandagale AB, et al. (2012) Determination of Wolbachia diversity in butterflies from Western Ghats, India, by a multigene approach. Appl Environ Microbiol 78: 4458-4467.
38. Fric Z, Wahlberg N, Pech P, Zrzavy J (2007) Phylogeny and classification of the Phengaris-Maculinea clade (Lepidoptera: Lycaenidae): total evidence and phylogenetic species concepts. Syst Entomol 32: 558-567.
39. Wang M, Settele J (2010) Notes on and key to the genus Phengaris (s. str.) (Lepidoptera, Lycaenidae) from mainland China with description of a new species. Zookeys 48: 21-28.
40. Sibatani A, Saigusa T, Hirowatari T (1994) The genus Maculinea van Eecke, 1915 (Lepidoptera: Lycaenidae) from the East Palaearctic Region. Tyô to Ga 44: 157-220.
41. Rákosy L, Tartally A, Goia M, Mihali C, Varga Z (2010) The Dusky Large Blue Maculinea nausithous kijevensis (Sheljuzhko, 1928) in the Transylvanian basin: New data on taxonomy and ecology. Nota lepid 33: 31-37.
42. Wynhoff I (1998) The recent distribution of the European Maculinea species. J Insect Conserv 2: 15-27.
43. Pech P, Fric Z, Konvicka M, Zrzavy J (2004) Phylogeny of Maculinea blues (Lepidoptera: Lycaenidae) based on morphological and ecological characters: evolution of parasitic myrmecophily. Cladistics-the International Journal of the Willi Hennig Society 20: 362-375.
44. Als TD, Vila R, Kandul NP, Nash DR, Yen SH, et al. (2004) The evolution of alternative parasitic life histories in large blue butterflies. Nature 432: 386-390.
45. Ugelvig LV, Vila R, Pierce NE, Nash DR (2011) A phylogenetic revision of the Glaucopsyche section (Lepidoptera: Lycaenidae), with special focus on the Phengaris-Maculinea clade. Mol Phylogenet Evol 61: 237-243.
46. Murayama S (1992) Some new Lycaenid species of Chinese Rhopalocera. Nature Insects 27: 37-41.
47. Staudinger O (1892) Lepidopteren des Kentei-Gebirges. Deutsche Entomologische Zeitschrift Iris 5: 300-393.
48. Staudinger O (1887) Neue Arten und Varietäten von Lepidopteren aus dem Amurgebiet. In: Romanoff NM, editor. Mémoires sur les lépidoptères. St. Pétersbourg: Imprimerie de M.M. Stassuléwitch. 126-232.
49. Takahashi A (1973) Maculinea teleius Bergsträsser at high elevation in the Central HonshÛ, Japan, with description of a new subspecies. Tyô to Ga 23: 75-85.
50. Druce HH (1875) Descriptions of new species of diurnal lepidoptera. Cistula Entomologica 1: 357-363.
51. Matsumura S (1910) Lycaeniden Japans. Entomol Z 23: 221-222.
52. Matsumura S (1926) Some new and unrecorded Lycaenids-species from Japan, Corea and Formosa. Insecta Matsumurana 1: 23-31.
53. Zhou W, Rousset F, O'Neil S (1998) Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc R Soc Biol Sci Ser B 265: 509-515.
54. Jolley KA, Chan MS, Maiden MC (2004) mlstdbNet - distributed multi-locus sequence typing (MLST) databases. BMC Bioinformatics 5: 86.
55. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41: 95-98.
56. Williams ST, Knowlton N (2001) Mitochondrial pseudogenes are pervasive and often insidious in the snapping shrimp genus Alpheus. Mol Biol Evol 18: 1484-1493.
57. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
58. Lunt DH, Zhang DX, Szymura JM, Hewitt GM (1996) The insect cytochrome oxidase I gene: evolutionary patterns and conserved primers for phylogenetic studies. Insect Mol Biol 5: 153-165.
59. Kim I, Lee EM, Seol KY, Yun EY, Lee YB, et al. (2006) The mitochondrial genome of the Korean hairstreak, Coreana raphaelis (Lepidoptera: Lycaenidae). Insect Mol Biol 15: 217-225.
60. Ratnasingham S, Hebert PD (2007) BOLD: The Barcode of Life Data System (http://www.barcodinglife.org). Mol Ecol Notes 7: 355-364.
61. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9: 1657-1660.
62. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10: 512-526.
63. Posada D (2008) jModelTest: Phylogenetic Model Averaging. Mol Biol Evol 25: 1253-1256.
64. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, et al. (2010) New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0. Syst Biol 59: 307-321.
65. Quek S-P, Davies SJ, Itino T, Pierce NE (2004) Codiversification in ant-plant mutualism: stem texture and the evolution of host use in Crematogaster (Formicidae: Myrmicinae) inhabitants of Macaranga (Euphorbiaceae). Evolution 58: 554-570.
66. Brower AVZ (1994) Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc Natl Acad Sci U S A 91: 6491-6495.
67. Papadopoulou A, Anastasiou I, Vogler AP (2010) Revisiting the insect mitochondrial molecular clock: The mid-Aegean trench calibration. Mol Biol Evol 27: 1659-1672.
68. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
69. Fu YX (1996) New statistical tests of neutrality for DNA samples from a population. Genetics 143: 557-570.
70. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resources 10: 564-567.
71. Zeisset I, Als TD, Settele J, Boomsma JJ (2005) Microsatellite markers for the large blue butterflies Maculinea nausithous and Maculinea alcon (Lepidoptera: Lycaenidae) and their amplification in other Maculinea species. Mol Ecol Notes 5: 165-168.
72. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
73. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 2611-2620.
74. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23: 1801-1806.
75. Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24: 2498-2504.
76. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
77. Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59: 1633-1638.
78. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www.unil.ch/izea/ softwares/fstat.html. Updated from Goudet (1995).
79. R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/.
80. Dieringer D, Schlötterer C (2003) Microsatellite Analyser (MSA): A platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3: 167-169.
81. Kikuchi Y, Fukatsu T (2003) Diversity of Wolbachia endosymbionts in heteropteran bugs. Appl Environ Microbiol 69: 6082-6090.
82. Tagami Y, Miura K (2004) Distribution and prevalence of Wolbachia in Japanese populations of Lepidoptera. Insect Mol Biol 13: 359-364.
83. Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, et al. (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18: 489-522.
84. 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.
85. Charlat S, Duplouy A, Hornett EA, Dyson EA, Davies N, et al. (2009) The joint evolutionary histories of Wolbachia and mitochondria in Hypolimnas bolina. BMC Evol Biol 9: 64.
86. Gompert Z, Nice CC, Fordyce JA, Forister ML, Shapiro AM (2006) Identifying units for conservation using molecular systematics: the cautionary tale of the Karner blue butterfly. Mol Ecol 15: 1759-1768.
87. Nice CC, Gompert Z, Forister ML, Fordyce JA (2009) An unseen foe in arthropod conservation efforts: The case of Wolbachia infections in the Karner blue butterfly. Biol Conserv 142: 3137-3146.
88. Hurst GDD, Jiggins FM, Robinson SJW (2001) What causes inefficient transmission of male-killing Wolbachia in Drosophila? Heredity 87: 220-226.
89. Novikova O, Sliwinska E, Fet V, Settele J, Blinov A, et al. (2007) CRI clade of non-LTR retrotransposons from Maculinea butterflies (Lepidoptera: Lycaenidae): evidence for recent horizontal transmission. BMC Evol Biol 7: 93.
90. Bordenstein SR, Werren JH (2000) Do Wolbachia influence fecundity in Nasonia vitripennis? Heredity 84: 54-62.
91. Sarakatsanou A, Diamantidis AD, Papanastasiou SA, Bourtzis K, Papadopoulos NT (2011) Effects of Wolbachia on fitness of the Mediterranean fruit fly (Diptera: Tephritidae). J Appl Entomol 135: 554-563.
92. Schneider DI, Garschall KI, Parker AG, Abd-Alla AMM, Miller WJ (2013) Global Wolbachia prevalence, titer fluctuations and their potential of causing cytoplasmic incompatibilities in tsetse flies and hybrids of Glossina morsitans subgroup species. J Invertebr Pathol 112: S104-S115.
93. Fiedler K (1998) Lycaenid-ant interactions of the Maculinea type: tracing their historical roots in a comparative framework. J Insect Conserv 2: 3-14.
94. Schmitt T (2007) Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Front Zool 4: 1-13.
95. Tsukada M (1982) Cryptomeria japonica - Glacial refugia and late-glacial and postglacial migration. Ecology 63: 1091-1105.
96. Wahlberg N, Saccheri I (2007) The effects of Pleistocene glaciations on the phylogeography of Melitaea cinxia (Lepidoptera: Nymphalidae). Eur J Entomol 104: 675-684.
97. Cassel A, Tammaru T (2003) Allozyme variability in central, peripheral and isolated populations of the scarce heath (Coenonympha hero: Lepidoptera, Nymphalidae): Implications for conservation. Conserv Genet 4: 83-93.
98. Vandewoestijne S, Baguette M, Brakefield PM, Saccheri IJ (2004) Phylogeography of Aglais urticae (Lepidoptera) based on DNA sequences of the mitochondrial COI gene and control region. Mol Phylogenet Evol 31: 630-646.
99. Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405: 907-913.
100. Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7: 453-464.
101. Gerth M, Geissler A, Bleidorn C (2011) Wolbachia infections in bees (Anthophila) and possible implications for DNA barcoding. Syst Biodiv 9: 319-327.
102. Roine A (2000) LepiBase 2.0. Butterflies of Europe - Species and Habitat. Vanha-Ulvila: Antti Roine.
103. Jolley KA, Maiden MC (2010) BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11: 595.
104. Wolbachia MLST databases. Available: http://pubmlst.org/wolbachia/. Last accessed: 19 Sep 2013.
105. Kudrna O, Harpke A, Lux K, Pennerstorfer J, Schweiger O, et al. (2011) Distribution Atlas of Butterflies in Europe. Halle (Saale): Gesellschaft für Schmetterlingsschutz. 576 p.
106. Lukhtanov V, Lukhtanov A (1994) Die Tagfalter Nordwestasiens. Herbipoliana 3.
107. Tshikolovets VV, Bidzilya A, Golovushkin M (2002) The butterflies of Transbaikal Siberia. Kyiv-Brno: Author's edition. 320 p.
108. Tshikolovets VV, Yakovlev RV, Bálint Z (2009) The butterflies of Mongolia. Kiev: Tshikolovets Publ.
109. Tshikolovets VV, Yakovlev RV, Kosterin OE (2009) The butterflies of Altai, Sayan and Tuva. Kiev: Tshikolovets Publ.