Eur. J. Entomol. 108 (2): 261-266, 2011 | DOI: 10.14411/eje.2011.035

Challenges of microsatellite development in Lepidoptera: Euphydryas aurinia (Nymphalidae) as a case study

Melthide SINAMA*,1, Vincent DUBUT*,1, Caroline COSTEDOAT1, André GILLES1, Marius JUNKER2, Thibaut MALAUSA3, Jean-François MARTIN4, Gabriel NÈVE1, Nicolas PECH1, Thomas SCHMITT2, Marie ZIMMERMANN5, Emese MEGLÉCZ1
1 Aix-Marseille Université, CNRS, IRD, UMR 6116 - IMEP, Equipe Evolution Génome Environnement, Case 36, 3 place Victor Hugo, 13331 Marseille Cedex 3, France; e-mails: melthide.sinama@gmail.com, vincent.dubut@univ-provence.fr, caroline.costedoat@univ-provence.fr, andre.gilles@univ-provence.fr, gabriel.neve@univ-provence.fr, nicolas.pech@univ-provence.fr, emese.meglecz@univ-provence.fr
2 Trier University, Department of Biogeography, 54286 Trier, Germany; e-mails: marius.junker@gmx.de, thsh@uni-trier.de
3 INRA, UMR 1301 - IBSV (INRA / UNSA / CNRS), Equipe Biologie des Populations en Interaction, 400 route des Chappes, BP 167, 06903 Sophia-Antipolis Cedex, France; e-mail: thibaut.malausa@sophia.inra.fr
4 Montpellier SupAgro, UMR CBGP (INRA / IRD / CIRAD / Montpellier SupAgro), Campus International de Baillarguet, CS 30016, 34988 Montferrier-sur-Lez Cedex, France; e-mail: martinjf@supagro.inra.fr
5 Université de Tours, CNRS, UMR 6035 - IRBI, Avenue Monge, Parc Grandmont, 37200 Tours, France; e-mail: marie.zimmermann@univ-tours.fr

Currently it remains difficult to obtain robust microsatellite markers for Lepidoptera. In an attempt to overcome the problems associated with developing microsatellite markers for this insect order we combined (i) biotin-enrichment protocol, (ii) next generation pyrosequencing (through 454 GS-FLX Titanium technology) and (iii) the use of individuals collected from eight geographically distant European populations representing three subspecies of Euphydryas aurinia. Out of 96 stringently designed primer pairs, 12 polymorphic microsatellite loci amplified without obvious evidence of null alleles in eight individuals from different subspecies. Between five and seven of these loci showed full within population applicability and three revealed to be robust and transferable between populations and sub-species, providing a first step towards the development of a valuable and robust tool for studying conservation issues and evolution in E. aurinia populations. Nevertheless, as in most studies dealing with Lepidoptera microsatellites, null alleles were detected in most of the developed markers. Our results emphasize the need for further research in order to better understand the complex evolution and organization of Lepidopteran genomes.

Keywords: Lepidoptera, microsatellite, null allele, 454 sequencing, QDD, Euphydryas aurinia

Received: August 9, 2010; Revised: September 20, 2010; Accepted: September 20, 2010; Published: April 5, 2011  Show citation

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SINAMA, M., DUBUT, V., COSTEDOAT, C., GILLES, A., JUNKER, M., MALAUSA, T., ... MEGLÉCZ, E. (2011). Challenges of microsatellite development in Lepidoptera: Euphydryas aurinia (Nymphalidae) as a case study. EJE108(2), 261-266. doi: 10.14411/eje.2011.035
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References

  1. ABBOTT C.L., EBERT D., TABATA A. & THERRIAULT T.W. 2010: Twelve microsatellite markers in the invasive tunicate, Didemnum vexillum, isolated from low genome coverage 454 pyrosequencing reads. Conserv. Genet. Resour. 3: 79-81 Go to original source...
  2. ABDELKRIM J., ROBERTSON B.C., STANTON J.A.L. & GEMMELL N.J. 2009: Fast, cost-effective development of species-specific microsatellite markers by genomic sequencing. BioTechniques 46: 185-191 Go to original source...
  3. ALTSCHUL S.F., MADDEN T.L., SCHAFFER A.A., ZHANG J., ZHANG Z., MILLER W. & LIPMAN D.J. 1997: Gapped BLAST and PSIBLAST: A new generation of protein database search programs. Nucl. Acids Res. 25: 3389-3402 Go to original source...
  4. ANTHONY N., GELEMBIUK G., RATERMAN D., NICE C. & FFRENCHCONSTANT R.H. 2001: Isolation and characterization of microsatellite markers from the endangered Karner blue butterfly Lycaeides melissa samuelis (Lepidoptera). Hereditas 134: 271-273 Go to original source...
  5. BELDADE P., VAN'T HOF A.E., JERONIMO M.A. & LONG A.D. 2009: Microsatellite markers associated with genes expressed in developing wings of Bicyclus anynana butterflies. Mol. Ecol. Resour. 9: 1487-1492 Go to original source...
  6. BENJAMINI Y. & HOCHBERG Y. 1995: Controlling the false discovery rate - a practical and powerful approach to multiple testing. J. R. Stat. Soc. (B) 57: 289-300 Go to original source...
  7. CASTOE T.A., POOLE A.W., GU W., DE KONING A.P.J., DANZA J.M., SMITH E.M. & POLLOCK D.D. 2010: Rapid identification of thousands of copperhead snake (Agkistrodon contortrix) microsatellite loci from modest amounts of 454 shotgun genome sequence. Mol. Ecol. Resour. 10: 341-347 Go to original source...
  8. COATES B.S., HELLMICH R.L. & LEWIS L.C. 2005: Polymorphic CA/GT and GA/CT microsatellite loci for Ostrinia nubilalis (Lepidoptera: Crambidae). Mol. Ecol. Notes 5: 10-12 Go to original source...
  9. COATES B.S., SUMERFORD D.V., HELLMICH R.L. & LEWIS L.C. 2009: Repetitive genome elements in a European corn borer, Ostrinia nubilalis, bacterial artificial chromosome library were indicated by bacterial artificial chromosome end sequencing and development of sequence tag site markers: Implications for lepidopteran genomic research. Genome 52: 57-67 Go to original source...
  10. CSENCSICS D., BRODBECK S. & HOLDEREGGER R. 2010: Costeffective, species-specific microsatellite development for the endangered dwarf bulrush (Typha minima) using nextgeneration sequencing technology. J. Hered. 101: 789-793 Go to original source...
  11. DALECKY A., BOGDANOWICZ S.M., DOPMAN E.B., BOURGUET D. & HARRISON R.G. 2006: Two multiplex sets of eight and five microsatellite markers for the European corn borer, Ostrinia nubilalis Hubner (Lepidoptera: Crambidae). Mol. Ecol. Notes 6: 945-947 Go to original source...
  12. DALY D., WALTHAM K., MULLEY J., WATTS P.C., ROSIN A., KEMP S.J. & SACCHERI I.J. 2004: Trinucleotide microsatellite loci for the peppered moth (Biston betularia). Mol. Ecol. Notes 4: 179-181 Go to original source...
  13. DOPMAN E.B., BOGDANOWICZ S.M. & HARRISON R.G. 2004: Genetic mapping of sexual isolation between E and Z pheromone strains of the European corn Borer (Ostrinia nubilalis). Genetics 167: 301-309 Go to original source...
  14. DUBUT V., MARTIN J.F., COSTEDOAT C., CHAPPAZ R. & GILLES A. 2009: Isolation and characterization of polymorphic microsatellite loci in the freshwater fishes Telestes souffia and Telestes muticellus (Teleostei: Cyprinidae). Mol. Ecol. Resour. 9: 1001-1005 Go to original source...
  15. DUBUT V., GRENIER R., MEGLECZ E., CHAPPAZ R., COSTEDOAT C., DANANCHER D., DESCLOUX S., MALAUSA T., MARTIN J.F., PECH N. & GILLES A. 2010: Development of 55 novel polymorphic microsatellite loci for the critically endangered Zingel asper L. (Actinopterygii: Perciformes: Percidae) and cross-species amplification in five other percids. Eur. J. Wildl. Res. 56: 931-938 Go to original source...
  16. ENDERSBY N.M., MCKECHNIE S.W., VOGEL H., GAHAN L.J., BAXTER S.W., RIDLAND P.M. & WEEKS A.R. 2005: Microsatellites isolated from diamondback moth, Plutella xylostella (L.), for studies of dispersal in Australian populations. Mol. Ecol. Notes 5: 51-53 Go to original source...
  17. FAUVELOT C., CLEARY D.F.R. & MENKEN S.B.J. 2006: Short-term impact of 1997/1998 ENSO-induced disturbance on abundance and genetic variation in a tropical butterfly. J. Hered. 97: 367-380 Go to original source...
  18. FLANAGAN N.S., BLUM M.J., DAVISON A., ALAMO M., ALBARRAN R., FAULHABER K., PETERSON E. & MCMILLAN W.O. 2002: Characterization of microsatellite loci in neotropical Heliconius butterflies. Mol. Ecol. Notes 2: 398-401 Go to original source...
  19. FRANCK P., GUERIN B., 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...
  20. HABEL J.C., FINGER A., MEYER M., SCHMITT T. & ASSMANN T. 2008: Polymorphic microsatellite loci in the endangered butterfly Lycaena helle (Lepidoptera: Lycaenidae). Eur. J. Entomol. 105: 361-362 Go to original source...
  21. HARPER G.L., MACLEAN N. & GOULSON D. 2003: Microsatellite markers to assess the influence of population size, isolation and demographic change on the genetic structure of the UK butterfly Polyommatus bellargus. Mol. Ecol. 12: 3349-3357 Go to original source...
  22. HIGGINS L.G. 1950: A descriptive catalogue of the Palaearctic Euphydryas (Lepidoptera: Rhopalocera). Trans. R. Entomol. Soc. Lond. 101: 435-487 Go to original source...
  23. HIGGINS L.G. 1955: A descriptive catalogue of the genus Mellicta Billberg (Lepidoptera: Nymphalidae) and its species, with supplementary notes on the genera Melitaea and Euphydryas. Trans. R. Entomol. Soc. Lond. 106: 1-127 Go to original source...
  24. JIGGINS C.D. 2005: A genetic linkage map of the mimetic butterfly Heliconius melpomene. Genetics 171: 557-570 Go to original source...
  25. KEYGHOBADI N., ROLAND J. & STROBECK C. 1999: Influence of landscape on the population genetic structure of the alpine butterfly Parnassius smintheus (Papilionidae). Mol. Ecol. 8: 1481-1495 Go to original source...
  26. KIJAS J.M.H., FOWLER J.C.S., GARBETT C.A. & THOMAS M.R. 1994: Enrichment of microsatellites from the Citrus genome using biotinylated oligonucleotide sequences bound to streptavidin-coated magnetic particles. Biotechniques 16: 656-662
  27. KIM K.S., COATES B.S., HELLMICH R.L., SUMERFORD D.V. & SAPPINGTON T.W. 2008: Isolation and characterization of microsatellite loci from the European corn borer, Ostrinia nubilalis (Hubner) (Insecta: Lepidoptera: Crambidae). Mol. Ecol. Resour. 8: 409-411 Go to original source...
  28. MARTIN J.F., PECH N., MEGLECZ E., FERREIRA S., COSTEDOAT C., DUBUT V., MALAUSA T. & GILLES A. 2010: Representativeness of microsatellite distributions in genomes, as revealed by 454 GS-FLX Titanium pyrosequencing. BMC Genomics 11: 560 Go to original source...
  29. MAZEL R. 1986: Structure et evolution du peuplement d'Euphydryas aurinia Rottemburg (Lepidoptera) dans le sud-ouest europeen. Vie Milieu 36: 205-225
  30. MEGLECZ E., PETENIAN F., DANCHIN E., COEUR D'ACIER A., 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...
  31. MEGLECZ E., ANDERSON S.J., BOURGUET D., BUTCHER R., CALDAS A., CASSEL-LUNDHAGEN A., COEUR D'ACIER A., 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...
  32. MEGLECZ E., COSTEDOAT C., DUBUT V., GILLES A., MALAUSA T., PECH N. & MARTIN J.F. 2010: QDD: A user-friendly program to select microsatellite markers and design primers from large sequencing projects. Bioinformatics 26: 403-404 Go to original source...
  33. MIKHEYEV A.S., VO T., WEE B., SINGER M.C. & PARMESAN C. 2010: Rapid microsatellite isolation from a butterfly by de novo transcriptome sequencing: Performance and a comparison with AFLP-derived distances. PLoS ONE 5: e11212 Go to original source...
  34. MOLECULAR ECOLOGY RESOURCES PRIMER DEVELOPMENT CONSORTIUM, ABDOULLAYE D., ACEVEDO I., ADEBAYO A.A., BEHRMANNGODEL J., BENJAMIN R.C., BOCK D.G., BORN C., BROUAT C., CACCONE A., CAO L.Z., CASADO-AMEZUA P., CATANEO J., CORREA-RAMIREZ M.M., CRISTESCU M.E., DOBIGNY G., EGBOSIMBA E.E., ETCHBERGER L.K., FAN B., FIELDS P.D., FORCIOLI D., FURLA P., GARCIA DE LEON F.J., GARCIA-JIMENEZ R., GAUTHIER P., GERGS R., GONZALEZ C., GRANJON L., GUTIERREZRODRIGUEZ C., HAVILL N.P., HELSEN P., HETHER T.D., HOFFMAN E.A., HU X., INGVARSSON P.K., ISHIZAKI S., JI H., JI X.S., JIMENEZ M.L., KAPIL R., KARBAN R., KELLER S.R., KUBOTA S., LI S., LI W., LIM D.D., LIN H., LIU X., LUO Y., MACHORDOM A., MARTIN A.P., MATTHYSEN E., MAZZELLA M.N., MCGEOCH M.A., MENG Z., NISHIZAWA M., O'BRIEN P., OHARA M., ORNELAS J.F., ORTU M.F., PEDERSEN A.B., PRESTON L., REN Q., ROTHHAUPT K.O., SACKETT L.C., SANG Q., SAWYER G.M., SHIOJIRI K., TAYLOR D.R., VAN DONGEN S., VAN VUUREN B.J., VANDEWOESTIJNE S., WANG H., WANG J.T., WANG L, XU X.L., YANG G., YANG Y., ZENG Y.Q., ZHANG Q.W., ZHANG Y., ZHAO Y. & ZHOU Y. 2010: Permanent genetic resources added to Molecular Ecology Resources database 1 August 2009 - 30 September 2009. Mol. Ecol. Resour. 10: 232-236 Go to original source...
  35. NAGARAJA G.M., MAHESH G., SATISH V., MADHU M., MUTHULAKSHMI M. & NAGARAJU J. 2005: Genetic mapping of Z chromosome and identification of W chromosome-specific markers in the silkworm, Bombyx mori. Heredity 95: 148-157 Go to original source...
  36. NOWAK C., BROWN C.M. & HELLMANN J.J. 2009: Microsatellite markers for the hybridizing tiger swallowtails, Papilio glaucus and P. canadensis, and their applicability to historic specimens and congeneric species. Mol. Ecol. Resour. 9: 800-803 Go to original source...
  37. PETENIAN F., MEGLECZ E., GENSON G., RASPLUS J.Y. & FAURE E. 2005: Isolation and characterization of polymorphic microsatellites in Parnassius apollo and Euphydryas aurinia (Lepidoptera). Mol. Ecol. Notes 5: 243-245 Go to original source...
  38. PRASAD M.D., MUTHULAKSHMI M., MADHU M., ARCHAK S., MITA K. & NAGARAJU J. 2005: Survey and analysis of microsatellites in the silkworm, Bombyx mori: Frequency, distribution, mutations, marker potential and their conservation in heterologous species. Genetics 169: 197-214 Go to original source...
  39. ROUSSET F. 2008: Genepop'007: A complete re-implementation of the Genepop software for Windows and Linux. Mol. Ecol. Resour. 8: 103-106 Go to original source...
  40. 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...
  41. TAY W.T., BEHERE G.T., BATTERHAM P. & HECKEL D.G. 2010: Generation of microsatellite repeat families by RTE retrotransposons in Lepidopteran genomes. BMC Evol. Biol. 10: 144 Go to original source...
  42. TORRES-LEGUIZAMON M., SOLIGNAC M., VAUTRIN D., CAPDEVIELLEDULAC C., DUPAS S. & SILVAIN J.F. 2009: Isolation and characterization of polymorphic microsatellites in the Potato Tuber Moth Tecia solanivora (Povolny, 1973) (Lepidoptera: Gelechiidae). Mol. Ecol. Resour. 9: 1167-1169 Go to original source...
  43. VAN OOSTERHOUT C., HUTCHINSON W.F., WILLS D.P.M. & 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...
  44. VAN SWAAY C.A.M. & WARREN M.S. 1999: Red Data Book of European Butterflies (Rhopalocera). Council of Europe Publishing, Strasbourg, 259 pp
  45. VAN'T HOF A.E., ZWAAN B.J., SACCHERI I.J., DALY D., BOT A.N.M. & BRAKEFIELD P.M. 2005: Characterization of 28 microsatellite loci for the butterfly Bicyclus anynana. Mol. Ecol. Notes 5: 169-172 Go to original source...
  46. 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...
  47. WEIR B.S. & HILL W.G. 2002: Estimating F-statistics. Annu. Rev. Genet. 36: 721-750 Go to original source...
  48. ZHANG D.X. 2004: Lepidopteran microsatellite DNA: Redundant but promising. Trends Ecol. Evol. 19: 507-509 Go to original source...
  49. ZHOU Y.H., GU H.N. & DORN S. 2005: Isolation of microsatellite loci in the codling moth, Cydia pomonella (Lepidoptera: Tortricidae). Mol. Ecol. Notes 5: 226-227 Go to original source...
  50. ZIMMERMANN M. 2000: Biodiversite au Sein des Melitees (Lepidoptera: Nymphalidae): Phylogenie et Genetique des Populations chez Euphydryas aurinia. PhD thesis, Universite Aix-Marseille I, France, 316 pp

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