Eur. J. Entomol. 106 (2): 315-321, 2009 | 10.14411/eje.2009.037

No genetic differentiation in the rose-infesting fruit flies Rhagoletis alternata and Carpomya schineri (Diptera: Tephritidae) across central Europe

Annette KOHNEN1, Volker WISSEMANN2, Roland BRANDL1
1 Department of Animal Ecology, Marburg University, Karl-von-Frisch-Stra▀e 8, D-35032 Marburg, Germany; e-mail: Kohnen@students.uni-marburg.de
2 Department of Systematic Botany, Giessen University, Heinrich-Buff-Ring 38, D-35392 Giessen, Germany

After the last glacial retreat in Europe, multiple recolonizations led to intraspecific differentiation in many of the recolonizing taxa. Here we investigate the genetic diversification across central Europe in two recolonizing taxa, the tephritid fruit flies Rhagoletis alternata (FallÚn, 1814) and Carpomya schineri (Loew, 1856), which attack rose hips. Analysis of amplified and sequenced fragments of the mitochondrial genes encoding cytochrome oxidase I (800 bp), cytochrome oxidase II (470 bp) and cytochrome b (450 bp), indicate that all the individuals of R. alternata (n = 21) collected from across Europe share the same haplotype. Two individuals of C. schineri form Berlin, which is further north of the range than previously reported in the literature, differ from the other individuals (n = 13) in one nucleotide position on the cytochrome oxidase II gene fragment. This level of genetic variation in sequences with a summed length of 1720 bp is unexpectedly lower than in other insect taxa (n = 63). This might have been caused by a selective sweep by a cytoplasmic symbiont such as Wolbachia, or a recent range expansion associated with a host shift or a single recolonization event.

Keywords: Genetic variation, genetic structure, mitochondrial DNA, Tephritidae, dog roses, range expansion, host shift, Rhagoletis alternata, Carpomya schineri

Received: December 22, 2008; Accepted: January 30, 2009; Published: May 20, 2009

Download citation

References

  1. ALTHOFF D.M. & THOMPSON J.N. 2001: Geographic structure in the searching behaviour of a specialist parasitoid: combining molecular and behavioural approaches. J. Evolution. Biol. 14: 406-417 Go to original source...
  2. ARIAS L., BEJARANO E.E., MARQUEZ E., MONCADA J., VELEZ I. & URIBE S. 2005: Mitochondrial DNA divergence between wild and laboratory populations of Anopheles albimanus Wiedemann (Diptera: Culicidae). Neotrop. Entomol. 34: 499-506 Go to original source...
  3. BAUER G. 1986: Life-history strategy of Rhagoletis alternata (Diptera: Trypetidae), a fruit fly operating in a "noninteractive" system. J. Anim. Ecol. 55: 785-794 Go to original source...
  4. BAUER G. 1998: Structure and function of a non-interactive, reactive insect-plant system. Oecologia 115: 154-160 Go to original source...
  5. CARISIO L., CERVELLA P., PALESTRINI C., DELPERO M. & ROLANDO A. 2004: Biogeographical patterns of genetic differentiation in dung beetles of the genus Trypocopris (Coleoptera, Geotrupidae) inferred from mtDNA and AFLP analyses. J. Biogeogr. 31: 1149-1162 Go to original source...
  6. CLARKE G.M. & WHYTE L.S. 2003: Phylogeography and population history of the endangered golden sun moth (Synemon plana) revealed by allozymes and mitochondrial DNA analysis. Conserv. Genet. 4: 719-734 Go to original source...
  7. CLARY D.O. & WOLSTENHOLME D.R. 1985: The mitochondrial DNA molecule of Drosophila yakuba: Nucleotide sequence, gene organization, and genetic code. J. Mol. Evol. 22: 252-271 Go to original source...
  8. COATES B.S., SUMERFORD D.V. & HELLMICH R.L. 2004: Geographic and voltinism differentiation among North American Ostrinia nubilalis (European corn borer) mitochondrial cytochrome c oxidase haplotypes. J. Insect Sci. 4: Art no. 35
  9. DA COSTA-DA-SILVA A.L., CAPURRO M.L. & BRACCO J.E. 2005: Genetic lineages in the yellow fever mosquito Aedes (Stegomyia) aegypti (Diptera: Culicidae) from Peru. Mem. Inst. Oswaldo Cruz 100: 639-644 Go to original source...
  10. DALLAS J.F., CRUICKSHANK R.H., LINTON Y.-M., NOLAN D.V., PATAKAKIS M., BRAVERMAN Y., CAPELA R., CAPELA M., PENA I., MEISWINKEL R., ORTEGA M.D., BAYLIS M., MELLOR P.S. & MORDUE A.J. 2003: Phylogenetic status and matrilineal structure of the biting midge, Culicoides imicola, in Portugal, Rhodes and Israel. Med. Vet. Entomol. 17: 379-387 Go to original source...
  11. DIEGISSER T., JOHANNESEN J., LEHR C. & SEITZ A. 2004: Genetic and morphological differentiation in Tephritis bardanae (Diptera: Tephritidae): evidence for host-race formation. J. Evol. Biol. 17: 83-93 Go to original source...
  12. DINGLER H. 1907: Versuch einer Erklaerung gewisser Erscheinungen in der Ausbildung und Verbreitung der wilden Rosen. Mitt. Naturw. Ver. Aschaffen. 6: 1-38
  13. EMERSON B.C., ORAMI P. & HEWITT G.M. 2000: Tracking colonization and diversification of insect lineages on islands: mitochondrial DNA phylogeography of Tarphius canariensis (Coleoptera: Colydiidae) on the Canary Islands. Proc. R. Soc. Lond. (B) 267: 2199-2205 Go to original source...
  14. ESSEGHIR S., READY P.D., KILLICK-KENDRICK R. & BENLSMAIL R. 1997: Mitochondrial haplotypes and phylogeography of Phlebotomus vectors of Leishmania major. Insect Mol. Biol. 6: 211-225 Go to original source...
  15. FOLEY D.H. & TORRES E.P. 2006: Population structure of an island malaria vector. Med. Vet. Entomol. 20: 393-401 Go to original source...
  16. HARRISON R.G. 1991: Molecular changes at speciation. Annu. Rev. Ecol. Syst. 22: 281-308 Go to original source...
  17. HE L., WATABE H., XIANGYU J., GAO J., LIANG X., AOTSUKA T. & ZHANG Y. 2007: Genetic differentiation and cryptic speciation in natural populations of Drosophila lacertosa. Mol. Phylogen. Evol. 43: 24-31 Go to original source...
  18. HEGI G. 1975: Illustrierte Flora Mitteleuropa IV/2C. Parey, Muenchen, p. 50
  19. HENDEL F. 1927: Trypetidae. In Lindner E. (eds): Die Fliegen der palaearktischen Region Bd. V. Schweizerbart, Stuttgart, pp. 91-93
  20. HEWITT G.M. 1996: Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linn. Soc. 58: 247-276 Go to original source...
  21. HUFBAUER R.A., BOGDANOWICZ S.M. & HARRISON R.G. 2004: The population genetics of a biological control introduction: mitochondrial DNA and microsatellite variation in native and introduced populations of Aphidus ervi, a parasitoid wasp. Mol. Ecol. 13: 337-348 Go to original source...
  22. HUNDSDOERFER A.K. & WINK M. 2006: Incongruence of morphology and genetic markers in Hyles tithymali (Lepidoptera: Sphingidae) from the Canary Islands. J. Zool. Syst. Evol. Res. 44: 316-322 Go to original source...
  23. HURST G.D.D. & JIGGINS F.M. 2005: Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc. R. Soc. Lond. (B) (Biol. Sci.) 272: 1525-1534 Go to original source...
  24. KANDYBINA M.N. 1977: Larvae of fruit-infesting fruit flies (Diptera: Tephritidae). Opred. Faune SSSR 114: 153-156 [in Russian]
  25. KITTAYAPONG P., MILNE J.R., TIGVATTANANONT S. & BAIMAI V. 2000: Distribution of the reproduction-modifying bacteria, Wolbachia, in natural populations of tephritid fruit flies in Thailand. Sci. Asia 26: 93-103 Go to original source...
  26. LAFFIN R.D., LANGOR D.W. & SPERLING F.A.H. 2004: Population structure and gene flow in the white pine weevil, Pissodes strobi (Coleoptera: Curculionidae). Ann. Entomol. Soc. Am. 97: 949-956 Go to original source...
  27. LECLAIRE M. & BRANDL R. 1994: Phenotypic plasticity and nutrition in a phytophagous insect - Consequences of colonizing a new host. Oecologia 100: 379-385 Go to original source...
  28. LEEBENS-MACK J. & PELLMYR O. 2004: Patterns of genetic structure among populations of an oligophagous pollinating yucca moth (Tegeticula yuccasella). J. Hered. 95: 127-135 Go to original source...
  29. LEWTER J.A., SZALANSKI A.L., NAGOSHI R.N., MEAGHER R.L., OWENS C.B. & LUTTRELL R.G. 2006: Genetic variation within and between strains of the fall armyworm Spodoptera frugiperda. Fla Entomol. 89: 63-68 Go to original source...
  30. LI J., ZHAO F., CHOI Y.S., KIM I., SOHN H.D. & JIN B.R. 2006: Genetic variation in the diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae) in China inferred from mitochondrial COI gene sequence. Eur. J. Entomol. 103: 605-611 Go to original source...
  31. LONG Y., WAN H., YAN F., XU C., LEI G., LI S. & WANG R. 2006: Glacial effects on sequences divergence of mitochondrial COII of Polyura eudamippus (Lepidoptera: Nymphalidae) in China. Biochem. Genet. 44: 361-377 Go to original source...
  32. LOZIER J.D., RODERICK G.K. & MILLS N.J. 2007: Genetic evidence from mitochondrial, nuclear, and endosymbiont markers for the evolution of host plant associated species in the aphid genus Hyalopterus (Hemiptera: Aphididae). Evolution 61: 1353-1367 Go to original source...
  33. LUNT D.H., IBRAHIM K.M. & HEWITT G.M. 1998: mtDNA phylogeography and postglacial patterns of subdivision in the meadow grasshopper Chorthippus parallelus. Heredity 80: 633-641 Go to original source...
  34. MARDULYN P. & MILINKOVITCH M.C. 2005: Inferring contemporary levels of gene flow and demographic history in a local population of the leaf beetle Gonioctena olivacea from mitochondrial DNA sequence variation. Mol. Ecol. 14: 1641-1653 Go to original source...
  35. MAROJA L.S., BOGDANOWICZ S.M., WALLIN K.F., RAFFA K.F. & HARRISON R.G. 2007: Phylogeography of spruce beetles (Dendroctonus rufipennis Kirby) (Curculionidae: Scolytinae) in North America. Mol. Ecol. 16: 2560-2573 Go to original source...
  36. MIROL P.M., SCHAFER M.A., ORSINI L., ROUTTU J., SCHLOTTERER C., HOIKKALA A. & BUTLIN R.K. 2007: Phylogeographic patterns in Drosophila montana. Mol. Ecol. 16: 1085-1097 Go to original source...
  37. MUN J., BOHONAK A.J. & RODERICK G.K. 2003: Population structure of the pumpkin fruit fly Bactrocera depressa (Tephritidae) in Korea and Japan: Pliocene allopatry or recent invasion? Mol. Ecol. 12: 2941-2951 Go to original source...
  38. NARDI F., CARAPELLI A., DALLAI R. & RODERICK G.K. 2005: Population structure and colonization history of the olive fly, Bactrocera oleae (Diptera, Tephritidae). Mol. Ecol. 14: 2729-2738 Go to original source...
  39. OSHAGHI M.A., YAAGHOOBI F. & ABAIE M.R. 2006: Pattern of mitochondrial DNA variation between and within Anopheles stephensi (Diptera: Culicidae) biological forms suggests extensive gene flow. Acta Trop. 99: 226-233 Go to original source...
  40. OSHAGHI M.A., SHEMSHAD K., YAGHOBI-ERSHADI M.R., PEDRAM M., VATANDOOST H., ABAIE M.R., AKBARZADEH K. & MOHTARAMI F. 2007: Genetic structure of the malaria vector Anopheles superpictus in Iran using mitochondrial cytochrome oxidase (COI and COII) and morphologic markers: A new species complex? Acta Trop. 101: 241-248 Go to original source...
  41. PORRETTA D., CANESTRELLI D., BELLINI R., CELLI G. & URBANELLI S. 2007: Improving insect pest management through population genetic data: a case study of the mosquito Ochlerotatus caspius (Pallas). J. Appl. Ecol. 44: 682-691 Go to original source...
  42. PRAMUAL P., KUVANGKADILOK C., BAIMAI V. & WALTON C. 2005: Phylogeography of the black fly Simulium tani (Diptera: Simuliidae) from Thailand as inferred from mtDNA sequences. Mol. Ecol. 14: 3989-4001 Go to original source...
  43. REED L.K., NYBOER M. & MARKOW T.A. 2007: Evolutionary relationships of Drosophila mojavensis geographic host races and their sister species Drosophila arizonae. Mol. Ecol. 16: 1007-1022 Go to original source...
  44. RIEGLER M. & STAUFFER C. 2002: Wolbachia infections and superinfections in cytoplasmically incompatible populations of the European cherry fruit fly Rhagoletis cerasi (Diptera, Tephritidae). Mol. Ecol. 11: 2425-2434 Go to original source...
  45. RITZ C.M., SCHMUTHS H. & WISSEMANN V. 2005: Evolution by reticulation: European dogroses originated by multiple hybridization across the genus Rosa. J. Hered. 96: 4-14 Go to original source...
  46. ROKAS A., NYLANDER J.A.A., RONQUIST F. & STONE G.N. 2002: A maximum-likelihood analysis of eight phylogenetic markers in gallwasps (Hymenoptera: Cynipidae): Implications for insect phylogenetic studies. Mol. Phylogen. Evol. 22: 206-219 Go to original source...
  47. ROKAS A., ATKINSON R.J., WEBSTER L., CSOKA G. & STONE G.N. 2003: Out of Anatolia: longitudinal gradients in genetic diversity support an eastern origin for a circum-Mediterranean oak gallwasp Andricus quercustozae. Mol. Ecol. 12: 2153-2174 Go to original source...
  48. SCHREY N.M., REEVE J.D. & ANDERSON F.E. 2005: Mitochondrial DNA analysis of the bark beetle predator Thanasimus dubius F. (Coleoptera: Cleridae) reveals regional genetic differentiation. Mol. Ecol. 14: 3317-3324 Go to original source...
  49. SEZONLIN M., DUPAS S., LE RU B., LE GALL P., MOYAL P., CALATAYUD P.A., GIFFARD I., FAURE N. & SILVAIN J.F. 2006: Phylogeography and population genetics of the maize stalk borer Busseola fusca (Lepidoptera, Noctuidae) in sub-Saharan Africa. Mol. Ecol. 15: 407-420 Go to original source...
  50. SHA Z.-L., ZHU C.-D., MURPHY R.W., SALLE J.L. & HUANG D.-W. 2006: Mitochondrial phylogeography of a leafminer parasitoid Diglyphus isaea (Hymenoptera: Eulophidae) in China. Biol. Contr. 38: 380-389 Go to original source...
  51. SHI W., KERDELHUE C. & YE H. 2005: Population genetics of the oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae), in Yunnan (China) based on mitochondrial DNA sequences. Envir. Entomol. 34: 977-983 Go to original source...
  52. SIMON C., FRATI F., BECKENBACH A., CRESPI B., LIU H. & FLOOK P. 1994: Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann. Entomol. Soc. Am. 87: 651-701 Go to original source...
  53. SIMONATO M., MENDEL Z., KERDELHUE C., ROUSSELET J., MAGNOUX E., SALVATO P., ROQUES A., BATTISTI A. & ZANE L. 2007: Phylogeography of the pine processionary moth Thaumetopoea wilkinsoni in the Near East. Mol. Ecol. 16: 2273-2283 Go to original source...
  54. SMITH P. 2005: Mitochondrial DNA variation among populations of the glassy-winged sharpshooter, Homalodisca coagulata. J. Insect Sci. 5: Art no. 41
  55. SMITH J.J. & BUSH G.L. 1997: Phylogeny of the genus Rhagoletis (Diptera: Tephritidae) inferred from DNA sequences of mitochondrial cytochrome oxidase II. Mol. Phylogen. Evol. 7: 33-43 Go to original source...
  56. SMITH J.J. & BUSH G.L. 2000: Phylogeny of the subtribe Carpomyina (Trypetinae), emphasizing relationships of the genus Rhagoletis. In Aluja M. & Norrbom A.L. (eds): Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. CRC Press, Boca Raton, FL, pp. 187-217.
  57. SMITH C.I. & FARRELL B.D. 2005: Phylogeography of the longhorn cactus beetle Moneilema appressum LeConte (Coleoptera: Cerambycidae): was the differentiation of the Madrean sky islands driven by Pleistocene climate changes? Mol. Ecol. 14: 3049-3065 Go to original source...
  58. SNALL N., HUOPONEN K., SALONIEM I., SAVONTAUS M.-L. & RUOHOMAKI K. 2004: Dispersal of females and differentiation between populations of Epirrita autumnata (Lepidoptera: Geometridae) inferred from variation in mitochondrial DNA. Eur. J. Entomol. 101: 495-502 Go to original source...
  59. STAUFFER C., LAKATOS F. & HEWITT G.M. 1999: Phylogeography and postglacial colonization routes of Ips typographus L. (Coleoptera, Scolytidae). Mol. Ecol. 8: 763-773 Go to original source...
  60. SZALANSKI A.L., OWENS C.B., LEWTER J.A. & BORCE A.B 2006: Genetic structure of Aedes vexans (Diptera: Culicidae) populations from Central United States based on mitochondrial ND5 sequences. Ann. Entomol. Soc. Am. 99: 157-163 Go to original source...
  61. TABERLET P., FUMAGALLI L., WUST-SAUCY A.G. & COSSON J.F. 1998: Comparative phylogeography and postglacial colonization routes in Europe. Mol. Ecol. 7: 453-464 Go to original source...
  62. THEMU E.A. & YAN G. 2005: Microsatellite and mitochondrial genetic differentiation of Anopheles arabiensis (Diptera: Culicidae) from western Kenya, the great rift valley and coastal Kenya. Am. J. Trop. Med. Hyg. 73: 726-733
  63. TIMMERMANS M.J.T.N., ELLERS J., MARIEN J., VERHOEF S.C., FERWERDA E.B. & VAN STRAALEN N.M. 2005: Genetic structure in Orchesella cincta (Collembola): strong subdivision of European populations inferred from mtDNA and AFLP markers. Mol. Ecol. 14: 2017-2024 Go to original source...
  64. VANDEWOESTIJNE S., BAGUETTE M., BRAKEFIELD P.M. & SACCHERI I.J. 2004: Phylogeography of Aglais urticae (Lepidoptera) based on DNA sequences of the mitochondrial COI gene and control region. Mol. Phylogen. Evol. 31: 630-646 Go to original source...
  65. VASCONCELOS T., HORN A., LIEUTIER F., BRANCO M. & KERDELHUE C. 2006: Distribution and population genetic structure of the Mediterranean pine shoot beetle Tomicus destruens in the Iberian Peninsula and Southern France. Agr. Forest Entomol. 8: 103-111 Go to original source...
  66. VAUPEL A., KLINGE K., BRAENDLE M., WISSEMANN V., TSCHARNTKE T. & BRANDL R. 2007: Genetic differentiation between populations of the European rose hip fly Rhagoletis alternata. Biol. J. Linn. Soc. 90: 619-625 Go to original source...
  67. VILA M. & BJORKLUND M. 2004: The utility of the neglected mitochondrial control region for evolutionary studies in Lepidoptera (Insecta). J. Mol. Evol. 58: 280-290 Go to original source...
  68. VILA M. & BJORKLUND M. 2004: Testing biennialism in the butterfly Erebia palarica (Nymphalidae: Satyrinae) by mtDNA sequencing. Insect Mol. Biol. 13: 213-217 Go to original source...
  69. VILA M., VIDAL-ROMANI J.R. & BJORKLUND M. 2005: The importance of time scale and multiple refugia: Incipient speciation and admixture of lineages in the butterfly Erebia triaria (Nymphalidae). Mol. Phylogen. Evol. 36: 249-260 Go to original source...
  70. WHITE I.M. & ELSON-HARRIS M.M. 1992: Fruit Flies of Economic Significance: Their Identification and Bionomics. CABI Wallingford, Oxon, 601 pp
  71. WILLIAMS H.C., ORMEROD S.J. & BRUFORD M.W. 2006: Molecular systematics and phylogeography of the cryptic species complex Baetis rhodani (Ephemeroptera, Baetidae). Mol. Phylogen. Evol. 40: 370-382 Go to original source...
  72. WISSEMANN V. 2002: Molecular evidence for allopolyploid origin of the Rosa canina-complex (Rosaceae, Rosoideae). J. Appl. Bot. 76: 176-178