Eur. J. Entomol. 106 (4): 457-469, 2009 | DOI: 10.14411/eje.2009.058

Contrasting levels of polymorphism in cross-amplified microsatellites in two endangered xerothermophilous, obligatorily myrmecophilous, butterflies of the genus Phengaris (Maculinea) (Lepidoptera: Lycaenidae)

Robert RUTKOWSKI1, Marcin SIELEZNIEW2, Agnieszka SZOSTAK3
1 Department of Molecular and Biometrical Techniques, Museum and Institute of Zoology, Polish Academy of Sciences, Wilcza 64, PL-00-679 Warszawa, Poland; e-mail: robertrut@miiz.waw.pl
2 Department of Invertebrate Zoology, Institute of Biology, University of Bialystok, Swierkowa 20B, PL-15-950 Białystok, Poland; e-mail: marcins@uwb.edu.pl
3 Ks. St. Konarskiego 15, PL-08-400 Garwolin, Poland

We analysed the polymorphism of cross-amplified microsatellite loci in two endangered butterflies of the genus Phengaris, which inhabit warm grasslands. Specimens of P. arion and P. 'rebeli' collected in Poland showed contrasting levels of variability in the investigated loci. All six tested microsatellites were highly variable in P. arion, whereas in P. 'rebeli' one locus was monomorphic and the other four loci showed a rather low level of polymorphism. Genetic differentiation was small or moderate among P. arion populations and high among P. 'rebeli' populations. We hypothesise that these differences reflect: (1) the relatively high genetic variability of P. arion compared with other members of the genus, indicated by previous studies on allozymes; (2) the small, in the majority of cases, genetic differentiation among populations of P. arion, which suggests recent gene flow; (3) a decrease in the genetic variability and increased isolation of peripheral populations of P. 'rebeli'. In both species, the occurrence of "null" alleles was suggested for some loci, which should be taken into consideration in future studies of the population structure. Additional analysis performed on the corrected frequency of alleles indicated that "null" alleles constitute only a minor problem when estimating genetic differentiation, using FST and AMOVA, however they strongly influence estimates of heterozygosity and FIS, and inferences about the number of genetic groups and assignment of individuals, especially in the case of 'P. rebeli'.

Keywords: Lycaenidae, Phengaris arion, P. rebeli, genetic polymorphism, cross-amplification, Poland

Received: March 9, 2009; Revised: June 17, 2009; Accepted: June 17, 2009; Published: November 20, 2009  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
RUTKOWSKI, R., SIELEZNIEW, M., & SZOSTAK, A. (2009). Contrasting levels of polymorphism in cross-amplified microsatellites in two endangered xerothermophilous, obligatorily myrmecophilous, butterflies of the genus Phengaris (Maculinea) (Lepidoptera: Lycaenidae). EJE, 106(4), 457-469. doi: 10.14411/eje.2009.058
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. ALS T.D., VILA R., KANDUL N.P., NASH D.R., YEN S.H., HSU Y.F., MIGNAULT A.A., BOOMSMA J.J. & PIERCE N.E. 2004: The evolution of alternative parasitic life histories in large blue butterflies. Nature 432: 386-390 Go to original source...
    2. ANTON C., ZEISSET I., MUSCHE M., DURKA W., BOOMSMA J.J. & SETTELE J. 2007: Population structure of a large blue butterfly and its specialist parasitoid in a fragmented landscape. Mol. Ecol. 16: 3828-3838 Go to original source...
    3. ARNAUD-HAOND S., TEIXEIRA S., MASSA S.I., BILLOT C., SAENGER P., COUPLAND G., DUARTE C.M. & SERRAO E.A. 2006: Genetic structure at range edge: low diversity and high inbreeding in Southeast Asian mangrove (Avicennia marina) populations. Mol. Ecol. 13: 3515-3525 Go to original source...
    4. ARNYAS E., BERECZKI J., TOTH A., VARGA K., PECSENYE K., TARTALLY A., KOVICS GY., KARSA D. & VARGA Z. 2009: Oviposition preferences of Maculinea alcon as influenced by aphid (Aphis gentianae) and fungal (Puccinia gentianae) infestation of larval host plants. Ecol. Entomol. 34: 90-97 Go to original source...
    5. BARBERO F., THOMAS J.A., BONELLI S., BALLETTO E. & SCHONROGGE K. 2009: Queen ants make distinctive sounds that are mimicked by a Butterfly Social Parasite. Science 323: 782-785 Go to original source...
    6. BERECZKI J., PECSENYE K., PEREGOVITS L. & VARGA Z. 2005: Pattern of genetic differentiation in the Maculinea alcon species group (Lepidoptera, Lycaenidae) in Central Europe. J. Zool. Syst. Evol. Res. 43: 157-165 Go to original source...
    7. BOUZA C., ARIAS J., CASTRO J., SANCHEZ L. & MARTINEZ P. 1999: Genetic structure of brown trout, Salmo trutta L., at the southern limit of the distribution range of the anadromous form. Mol. Ecol. 8: 1991-2001 Go to original source...
    8. BOUZAT J.L. & JOHNSON K. 2004: Genetic structure among closely spaced leks in a peripheral population of lesser prairie-chickens. Mol. Ecol. 13: 499-505 Go to original source...
    9. BROOKFIELD J.F. 1996: A simple new method for estimating null allele frequency from heterozygote deficiency Mol. Ecol. 5: 453-455 Go to original source...
    10. CHISTIAKOV D.A., HELLEMANS B. & VOLCKAERT F.A.M. 2006: Microsatellites and their genomic distribution, evolution, function and applications: a review with special reference to fish genetics. Aquaculture 255: 1-29 Go to original source...
    11. EXCOFFIER L., SMOUSE P.E. & QUATTRO J.M. 1992: Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479-491 Go to original source...
    12. FAUGERON S., MARTINEZ E.A., CORREA J.A., CARDENAS L., DESTOMBE C. & VALERO M. 2004: Reduced genetic diversity and increased population differentiation in peripheral and overharvested populations of Gigartina skottsbergii (Rhodophyta, Gigartinales) in southern Chile. J. Phycol. 40: 454-462 Go to original source...
    13. FAUVELOT C. 2005: Isolation and characterization of microsatellites in two tropical butterflies, Drupadia theda and Arhopala epimuta (Lepidoptera: Lycaenidae). Mol. Ecol. Notes 5: 724-726 Go to original source...
    14. FIGURNY-PUCHALSKA E., GADEBERG R.M.E. & BOOMSMA J.J. 2000: Comparison of genetic population structure of the large blue butterflies Maculinea nausithous and M. teleius. Biodiv. Conserv. 9: 419-432 Go to original source...
    15. FRANCK P., GUERIN F., LOISEAU A. & SAUPHANOR B. 2005: Isolation and characterization of microsatellite loci in the codling moth Cydia pomonella L. (Lepidoptera, Tortricidae). Mol. Ecol. Notes 5: 99-102 Go to original source...
    16. FRANKHAM R., BALLOU J.D. & BRISCOE D.A. 2003: Introduction to Conservation Genetics. Cambridge University Press, Cambridge, 617 pp Go to original source...
    17. 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 Go to original source...
    18. GADEBERG R.M.E. & BOOMSMA J.J. 1997: Genetic population structure of the large blue butterfly Maculinea alcon in Denmark. J. Insect Cons. 1: 99-111 Go to original source...
    19. GALBUSERA P., VAN DONGEN S. & MATTHYSEN E. 2000: Crossspecies amplification of microsatellite primers in passerine birds. Conserv. Genet. 1: 163-168 Go to original source...
    20. GOUDET J. 2001: FSTAT V2.9.3, a Program to Estimate and Test Gene Diversities and Fixation Indices. http://www.unil.ch/ izea/softwares/fstat.htlm
    21. HARR B., ZANGERL B., BREM G. & SCHLOTTERER C. 1998: Conservation of locus-specific microsatellite variability across species: a comparison of two Drosophila sibling species, D. melanogaster and D. simulans. Mol. Biol. Evol. 15: 176-184 Go to original source...
    22. HUTTER C.M., SCHUG M.D. & AQUADRO C.F. 1998: Microsatellite variation in Drosophila melanogaster and Drosophila simulans: a reciprocal test of the ascertainment bias hypothesis. Mol. Biol. Evol. 15: 1620-1636 Go to original source...
    23. JARNE P. & LAGODA P.J.L. 1996: Microsatellites, from molecules to populations and back. Trends Ecol. Evol. 11: 424-429 Go to original source...
    24. KEYGHOBADI N., ROLAND J. & STROBECK C. 2005: Genetic differentiation and gene flow among populations of the alpine butterfly, Parnassius smintheus, vary with landscape connectivity. Mol. Ecol. 14: 1897-1909 Go to original source...
    25. KOSKINEN M.T., HIRVONEN H., LANDRY P-A. & PRIMMER C.R. 2004: The benefits of increasing the number of microsatellites utilized in genetic population studies: an empirical perspective from analyses of grayling (Thymallus thymallus) evolutionary relationships. Hereditas 141: 61-67 Go to original source...
    26. LUNA C., BONIZZONI M., CHENG Q., ROBINSON A.S., AKSOY S. & ZHENG L. 2001: Microsatellite polymorphism in tsetse flies (Diptera: Glossinidae). J. Med. Entomol. 38: 376-381 Go to original source...
    27. MAVAREZ J. & GONZALEZ M. 2006: A set of microsatellite markers for Heliconius melpomene and closely related species. Mol. Ecol. Notes 6: 20-23 Go to original source...
    28. MEGLECZ E., PETENIAN F., DANCHIN E., D'ACIER A.C., RASPLUS J.Y. & FAURE E. 2004: High similarity between flanking regions of different microsatellites detected within each of two species of Lepidoptera: Parnassius apollo and Euphydryas aurinia. Mol. Ecol. 13: 1693-1700 Go to original source...
    29. MEGLECZ E., ANDERSON S.J., BOURGUET D., BUTCHER R., CALDAS A., CASSEL-LUNDHAGEN A., D'ACIER A.C., DAWSON D.A., FAURE N., FAUVELOT C., FRANCK P., HARPER G., KEYGHOBADI N., KLUETSCH C., MUTHULAKSHMI M., NAGARAJU J., PATT A., PETENIAN F., SILVAIN J.F. & WILCOCK H.R. 2007: Microsatellite flanking region similarities among different loci within insect species. Insect. Mol. Biol. 16: 175-185. Go to original source...
    30. MORIN P.A., MAHBOUBI P., WEDEL S. & ROGERS J. 1998: Rapid screening and comparison of human microsatellite markers in baboons: allele size is conserved, but allele number is not. Genomics 53: 12-20 Go to original source...
    31. NASH D.R., ALS T.D., MAILE R., JONES G.R. & BOOMSMA J.J. 2008: A mosaic of chemical coevolution in a large blue butterfly. Science 319: 88-90 Go to original source...
    32. NEI M. & ROYCHOUDHURY A.K. 1974: Sampling variances of heterozygosity and genetic distance. Genetics 76: 379-390 Go to original source...
    33. NEVE G. & MEGLECZ E. 2000: Microsatellite frequencies in different taxa. Trends Ecol. Evol. 15: 376-377 Go to original source...
    34. NOWICKI P., WITEK M., SKORKA P., SETTELE J. & WOYCIECHOWSKI M. 2005: Population ecology of the endangered butterflies Maculinea teleius and M. nausithous, and its implications for conservation. Popul. Ecol. 47: 193-202 Go to original source...
    35. PAEKAL R. & SMOUSE P.E. 2001: GenAlEx V5: Genetic Analysis in Excel. Population genetic software for teaching and research. http://www.anu.ed.au/BoZo/GenAlEx/
    36. PECSENYE K., BERECZKI J., TIHANYI B., TOTH A., PEREGOVITS L. & VARGA Z. 2007: Genetic differentiation among the Maculinea species (Lepidoptera: Lycaenidae) in eastern Central Europe. Biol. J. Linn. Soc. 91: 11-21 Go to original source...
    37. 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 20: 362-375 Go to original source...
    38. PEDERSEN A.A. & LOESCHCKE V. 2001: Conservation genetics of peripheral populations of the mygalomorph spider Atypus affinis (Atypidae) in northern Europe. Mol. Ecol. 10: 1133-1142 Go to original source...
    39. PRIMMER C.R., MOLLER A.P. & ELLEGREN H. 1996: A wide-range survey of cross-species microsatellite amplification in birds. Mol. Ecol. 5: 365-378 Go to original source...
    40. PRIMMER C.R., PAINTER J.N., KOSKINEN M.T., PALO J.U. & MERILA J. 2005: Factors affecting avian cross-microsatellite amplification. J. Avian Biol. 36: 348-360 Go to original source...
    41. PRITCHARD J.K., STEPHENS M., DONNELLY P. 2000: Inference of population structure using multilocus genotype data. Genetics 155: 945-959 Go to original source...
    42. ROSSITER S.J., JONES G., RANSOME R.D. & BARRATT E.M. 2000: Genetic variation and population structure in the endangered greater horseshoe bat Rhinolophus ferrumequinum. Mol. Ecol. 9: 1131-1135 Go to original source...
    43. RUBINSZTEIN D.C., AMOS W., LEGGO J., GOODBURN S., JAIN S., LI S.H., MARGOLIS R.L., ROSS C.A. & FERGUSON-SMITH M.A. 1995: Microsatellite evolution - evidence for directionality and variation in rate between species. Nat. Genet. 10: 337-343 Go to original source...
    44. RUTKOWSKI R., MAZGAJSKI T.D. & REJT L. 2006: Cross-species amplification of microsatellite loci in European woodpeckers (Picidae). Ann. Zool. 56: 819-826
    45. RUTKOWSKI R., OLEJNICZAK I., BONIECKI P., TEREBA A., CYBULSKA M. & PARYS A. 2007: Cross-species amplification of microsatellite loci in Orchesella flavescens (Apterygota: Collembola). Genus (Suppl.) 14: 59-62
    46. SCHNEIDER S.D., ROESSLI D. & EXCOFFIER L. 2000: Arlequin ver. 2000: A Software for Population Genetics Data Analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland
    47. SCRIBNER K.T. & PEARCE J.M. 2000: Microsatellites: evolutionary and methodological background and empirical applications at individual, population and phylogenetic level. In Baker A. (ed.): Molecular Methods in Ecology, Blackwell Science, London, pp. 235-271
    48. SELKOE K.A. & TOONEN R.J. 2006: Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol. Lett. 9: 615-629 Go to original source...
    49. SETTELE J., KUHN E. & THOMAS J.A. 2005: Studies on the Ecology and Conservation of Butterflies in Europe. Vol. 2: Species Ecology along a European Gradient: Maculinea Butterflies as a Model. Pensoft Publishers, Sofia-Moscow, 289 pp
    50. SIELEZNIEW M. & DZIEKANSKA I. 2009: Butterfly-ant relationships: Host ant specificity of Phengaris 'rebeli' Hirschke (Lepidoptera: Lycaenidae) in Pieniny Mts (southern Poland). Pol. J. Ecol. 57: 403-409
    51. SIELEZNIEW M. & STANKIEWICZ A.M. 2007: Differences in the development of the closely related myrmecophilous butterflies Maculinea alcon and M. rebeli (Lepidoptera: Lycaenidae). Eur. J. Entomol. 104: 433-444 Go to original source...
    52. SIELEZNIEW M. & STANKIEWICZ A.M. 2008: Myrmica sabuleti (Hymenoptera: Formicidae) not necessary for the survival of the population of Phengaris (Maculinea) arion (Lepidoptera: Lycaenidae) in eastern Poland: lower host-ant specificity or evidence for geographical variation of an endangered social parasite? Eur. J. Entomol. 105: 637-641 Go to original source...
    53. SIELEZNIEW M., BUSZKO J. & STANKIEWICZ A.M. 2005: Maculinea arion in Poland: distribution, ecology and prospects of conservation. In Settele J., Kuehn E. & Thomas J.A. (eds): Studies on the Ecology and Conservation of Butterflies in Europe. Vol. 2: Species Ecology along a European Gradient: Maculinea Butterflies as a Model. Pensoft Publishers, Sofia-Moscow, pp. 231-233
    54. SIGAARD P., PERTOLDI C., MADSEN A.B, SOGAARD B. & LOESCHCKE V. 2008: Patterns of genetic variation in isolated Danish populations of the endangered butterfly Euphydryas aurinia. Biol. J. Linn. Soc. 95: 677-687 Go to original source...
    55. STEINER F., SIELEZNIEW M., SCHLICK-STEINER B.C., HOTTINGER H., STANKIEWICZ A. & GORNICKI A. 2003: Host specificity revisited: New data on Myrmica host ants of the lycaenid butterfly Maculinea rebeli. J. Insect Cons. 7: 1-6 Go to original source...
    56. TARTALLY A., NASH D.R., LENGYEL S. & VARGA Z. 2008: Patterns of host ant use by sympatric populations of Maculinea alcon and M. 'rebeli' in the Carpathian Basin. Insect Soc. 55: 370-381 Go to original source...
    57. THOMAS J.A. 1995: The ecology and conservation of Maculinea arion and other European species of large blue butterfly. In Pullin A.S. (ed.): Ecology and Conservation of Butterflies. Chapman & Hall, London, pp. 180-197 Go to original source...
    58. THOMAS J.A. & ELMES G.W. 1998: Higher productivity at the cost of increased host-specificity when Maculinea butterfly larvae exploit ant colonies through trophallaxis rather than by predation. Ecol. Entomol. 23: 457-464 Go to original source...
    59. THOMAS J.A. & SETTELE J. 2004: Butterfly mimics of ants. Nature 432: 283-284 Go to original source...
    60. THOMAS J.A., ELMES G.W., WARDLAW J.C. & WOYCIECHOWSKI M. 1989: Host specificity among Maculinea butterflies in Myrmica ant nests. Oecologia 79: 425-457 Go to original source...
    61. VAN OOSTERHOUT C., HUTCHINSON W.F., WILLS D.P. & SHIPLEY P. 2004: Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4: 535-538 Go to original source...
    62. VAN SWAAY C. & WARREN M. 1999: Red Data Book of European Butterflies (Rhopalocera). Council of Europe Publishing, Strasbourg, 260 pp
    63. VAN'T HOF A.E., BRAKEFIELD P.M., SACCHERI I.J. & ZWAAN B.J. 2007: Evolutionary dynamics of multilocus microsatellite arrangements in the genome of the butterfly Bicyclus anynana, with implications for other Lepidoptera. Heredity 98: 320-328. Go to original source...
    64. WEIR B.S. & COCKERHAM C.C. 1984: Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370 Go to original source...
    65. ZAKHAROV E.V. & HELLMANN J.J. 2008: Genetic differentiation across a latitudinal gradient in two co-occurring butterfly species: revealing population differences in a context of climate change. Mol. Ecol. 17: 189-208 Go to original source...
    66. ZAKHAROV E.V., HELLMANN J.J. & ROMERO-SEVERSON J. 2007: Microsatellite loci in the Propertius duskywing, Erynnis propertius (Lepidoptera: Hesperiidae), and related species. Mol. Ecol. Notes 7: 266-268 Go to original source...
    67. ZEISSET I., ALS T.D., SETTELE J. & BOOMSMA J.J. 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 Go to original source...
    68. ZHANG D.-X. 2004: Lepidopteran microsatellite DNA: redundant but promising. Trends Ecol. Evol. 19: 507-509 Go to original source...

    This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content