Unprecedented long-term genetic monomorphism in an endangered relict butterfly species

Conservation Genetics

Volumn 10, Issue 6, 2009, Pages 1659-1665

  Habel, Jan Christian ^a,b   Zachos, Frank Emmanuel ^c   Finger, Aline ^a,b,d   Meyer, Marc ^a   Louy, Dirk ^b   Assmann, Thorsten ^e   Schmitt, Thomas ^b  

^a Musée National d'histoire Naturelle Section Zoologie des Invertébrés   (Germany)

^b UNIVERSITY OF TRIER   (Germany)

^c UNIVERSITY OF KIEL   (Germany)

^d ETH ZURICH   (Switzerland)

^e LEUPHANA UNIVERSITY OF LÜNEBURG   (Germany)

Author keywords

Allozymes; Climate change; Collection samples; Genetic diversity; Microsatellites; Parnassius apollo vinningensis; Population genetics; Purging

Indexed keywords

ALLOZYME; BUTTERFLY; CITES; CLIMATE CHANGE; ENDANGERED SPECIES; GENETIC MARKER; GENETIC VARIATION; MUSEUM; POLYMORPHISM;

CALIFORNIA; CHANNEL ISLANDS [CALIFORNIA]; NORTH AMERICA; SAN NICOLAS ISLAND; UNITED STATES;

ANIMALIA; PAPILIONOIDEA; PARNASSIINAE; PARNASSIUS APOLLO; UROCYON LITTORALIS;

EID: 71349083479     PISSN: 15660621     EISSN: 15729737     Source Type: Journal    
DOI: 10.1007/s10592-008-9744-5     Document Type: Article

References (61)

1. Aguilar A, Roemer G, Debenham S, Binns M, Garcelon D, Wayne RK (2004) High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci USA 3490-3494. doi: 10. 1073/pnas. 0306582101.
2. Allendorf FW, Luikart G (2006) Conservation and the genetics of populations. Blackwell, London.
3. Assmann T, Nolte O, Reuter H (1994) Postglacial colonization of middle Europe by Carabus auronitens as revealed by population genetics (Coleoptera, Carabidae). In: Desender K, Dufrêne M, Loreau M, Luff M, Maelfait JP (eds) Carabid Beetles: Ecology and Evolution. Kluwer Academic Publishers, Dordrecht.
4. 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. doi: 10. 1111/j. 1439-0469. 2005. 00305. x.
5. Besold J, Schmitt T, Tammaru T, Cassel-Lundhagen A (2008) Strong genetic impoverishment from the centre of distribution in southern Europe to peripheral baltic and isolated Scandinavian populations of the pearly heath butterfly. J Biogeogr 35: 2090-2101.
6. Besold J, Huck S, Schmitt T (2008b) Allozyme polymorphisms in the small heath Coenonympha pamphilus: recent ecological selection or old biogeographical signal? Ann Zool Fenn 45: 217-228.
7. 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. doi: 10. 1023/A: 1021884832122.
8. De Lattin G (1967) Grundriß der Zoogeographie. Verlag Gustav Fischer, Jena.
9. Debinski DM (1994) Genetic diversity assessment in a metapopulation of the butterfly Euphydryas gillettii. Heredity 70: 25-30.
10. Descimon H (1995) La conservation des Parnassius en France: aspects zoogéographiques, écologiques, démographiques et génétiques. Editions OPIE 1: 1-54.
11. Figurny-Puchalska E, Gadeberg RME, Boomsma JJ (2000) Comparison of genetic population structure of the large blue butterfly Maculinea nausithous and M. teleius. Biodivers Conserv 9: 419-432. doi: 10. 1023/A: 1008970232079.
12. Finger A, Zachos FE, Schmitt T, Meyer M, Assmann T, Habel JC (2008) The genetic status of the Violet Copper Lycaena helle-a relict of the cold past in times of global warming. Ecography (in press).
13. Frankham R, Gilligan DM, Morris D, Briscoe DA (2001) Inbreeding and extinction: effects of purging. Conserv Genet 2: 279-285. doi: 10. 1023/A: 1012299230482.
14. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge.
15. Gadeberg RME, Boomsma JJ (1997) Genetic population structure of the large blue butterfly Maculinea alcon in Denmark. J Insect Conserv 1: 99-111. doi: 10. 1023/A: 1018439211244.
16. Habel JC, Schmitt T, Müller P (2005) The fourth paradigm pattern of postglacial range expansion of European terrestrial species: the phylogeography of the Marbled White butterfly (Satyrinae, Lepidoptera). J Biogeogr 32: 1489-1497.
17. Habel JC, Meyer M, Schmitt T, Assmann T (2008) Polymorphic microsatellite loci in the endangered butterfly Lycaena helle (Lepidoptera: Lycaenidae). Eur J Entomol 105: 361-362.
18. Hanski I (1999) Metapopulation ecology. Oxford University Press, Oxford.
19. Hansson B, Westerberg L (2002) On the correlation between heterozygosity and fitness in natural populations. Mol Ecol 11: 2467-2474. doi: 10. 1046/j. 1365-294X. 2002. 01644. x.
20. Harris H, Hopkinson DA (1978) Handbook of enzyme electrophoresis in human genetics. North-Holland, Amsterdam.
21. Haubrich K, Schmitt T (2007) Cryptic differentiation in alpine-endemic, high altitude butterflies reveals down-slope glacial refugia. Mol Ecol 16: 3643-3658. doi: 10. 1111/j. 1365-294X. 2007. 03424. x.
22. Hebert PDN, Beaton MJ (1993) Methodologies for allozyme analysis using cellulose acetat electrophoresis. Helena Laboratories, Beaumont.
23. Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58: 247-276.
24. IUCN (1996) The 1996 IUCN red list of threatened animals. IUCN Publications Service Unit, Cambridge.
25. Kawamura K, Kubota M, Furukawa M, Harada Y (2007) The genetic structure of endangered indigenous populations of the amago salmon, Oncorhynchus masou ishikawae, in Japan. Conserv Genet 8: 1163-1176. doi: 10. 1007/s10592-006-9271-1.
26. Kinkler H, Löser S, Rehnelt K (1987) 10 Jahre Erforschung des Moselapollofalters (Parnassius apollo vinningensis STICHEL 1899, Lepidoptera, Papilionidae) im modernen Weinbaugebiet der Mosel-ein Beitrag zu seiner Rettung. Mitt Arbeitsgem rh-westf Lepid V/2: 53-100.
27. Kudrna O (2002) The distribution atlas of European butterflies. Oedippus 20: 1-342.
28. Lesica P, Allendorf FW (1995) When peripheral populations are valuable for conservation. Conserv Biol 9: 753-760. doi: 10. 1046/j. 1523-1739. 1995. 09040753. x.
29. Löser S, Rehnelt K (1983) Das rezente Verbreitungsareal von Parnassius apollo vinningensis Stichel, 1899 (Lepidoptera, Papilionidae) im modernen Weinbaugebiet der Mosel. Verh SIEEC X, Budapest.
30. Louy D, Habel JC, Schmitt T, Assmann T, Meyer M, Müller P (2007) Strongly diverging population genetic patterns of three skipper species: the role of habitat fragmentation and dispersal ability. Conserv Genet 8: 671-681.
31. Mandrioli M, Borsatti F, Mola L (2006) Factors affecting DNA preservation from museum-collected lepidopteran specimens. Entomol Exp Appl 120: 239-244. doi: 10. 1111/j. 1570-7458. 2006. 00451. x.
32. Meglécz E, Solignac M (1998) Microsatellite loci for Parnassius mnemosyne (Lepidoptera). Hereditas 128: 179-180. doi: 10. 1111/j. 1601-5223. 1998. 00179. x.
33. Meglécz E, Petenian F, Danchin E, Coer D'Acier A, Rasplus J-Y, Faure E (2004) High similarity between flanking regions of different microstatellites detected within each of two species of Lepidoptera: Parnassius apollo and Euphydrias aurinia. Mol Ecol 13: 1693-1700. doi: 10. 1111/j. 1365-294X. 2004. 02163. x.
34. Melbourne BA, Hastings A (2008) Extinction risk depends strongly on factors contributing to stochasticity. Nature 454: 100-103. doi: 10. 1038/nature06922.
35. Nakonieczny M, Kedziorski A, Michalczyk K (2007) Apollo Butterfly (Parnassius apollo L.) in Europe-its history, decline and perspectives of conservation. Funct Ecosyst Comm 1: 56-79.
36. Petenian F, Meglécz 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. doi: 10. 1111/j. 1471-8286. 2005. 00891. x.
37. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17: 230-237. doi: 10. 1046/j. 1523-1739. 2003. 01236. x.
38. Reimann T, Assmann T, Nolte O, Reuter H, Huber C, Weber F (2002) The paleo-ecology of Carabus auronitens Fabricius: characterization and localization of glacial refugia in southern France and reconstruction of postglacial expansion routes by means of allozyme polymorphisms. Abh Naturwissenschaftl Ver Hamburg NF 35: 1-151.
39. Ridgway T (2005) Allozyme electrophoresis still represents a powerful technique in the management of coral reefs. Biodivers Conserv 14: 135-149. doi: 10. 1007/s10531-005-4054-4.
40. Schmitt T, Haubrich K (2008) The genetic strucutre of the mountain forest butterfly Erebia euryale unravels the late Pleistocene and postglacial history of the mountain coniferous forest biome in Europe. Mol Ecol 17: 2194-2207. doi: 10. 1111/j. 1365-294X. 2007. 03687. x.
41. Schmitt T, Hewitt GM (2004a) The genetic pattern of population threat and loss: a case study of butterflies. Mol Ecol 13: 21-31. doi: 10. 1046/j. 1365-294X. 2004. 02020. x.
42. Schmitt T, Hewitt GM (2004b) Molecular Biogeography of the arctic-alpine disjunct burnet moth species Zygaena exulans (Zygaenidae, Lepidoptera) in the Pyrenees and Alps. J Biogeogr 31: 885-893. doi: 10. 1111/j. 1365-2699. 2004. 01079. x.
43. Schmitt T, Müller P (2007) Limited hybridization along a large contact zone between two genetic lineages of the butterfly Erebia medusa (Satyrinae, Lepidoptera) in Central Europe. J Zool Syst Evol Res 45: 39-46. doi: 10. 1111/j. 1439-0469. 2006. 00404. x.
44. Schmitt T, Seitz A (2004) Low diversity but high differentiation: the population genetics of Aglaope infausta (Zygaenidae: Lepidoptera). J Biogeogr 31: 137-144. doi: 10. 1111/j. 1365-2699. 2004. 01079. x.
45. Schmitt T, Gießl A, Seitz A (2003) Did Polyommatus icarus (Lepidoptera: Lycaenidae) have distinct glacial refugia in southern Europe? Evidence from population genetics. Biol J Linn Soc 80: 529-538. doi: 10. 1046/j. 1095-8312. 2003. 00261. x.
46. Schmitt T, Röber S, Seitz A (2005a) Is the last glaciation the only relevant event for the present genetic population structure of the Meadow Brown butterfly Maniola jurtina (Lepidoptera: Nymphalidae)? Biol J Linn Soc 85: 419-431. doi: 10. 1111/j. 1095-8312. 2005. 00504. x.
47. Schmitt T, Varga Z, Seitz A (2005b) Are Polyommatus hispana and Polyommatus slovacus bivoltine Polyommatus coridon (Lepidoptera: Lycaenidae)? The discriminatory value of genetics in the taxonomy. Org Divers Evol 5: 297-307. doi: 10. 1016/j. ode. 2005. 01. 001.
48. Schmitt T, Cizek O, Konvicka M (2005c) Genetics of a butterfly relocation: large, small and introduced populations of the mountain endemic Erebia epiphron silesiana. Biol Conserv 123: 11-18. doi: 10. 1016/j. biocon. 2004. 09. 018.
49. Schmitt T, Hewitt GM, Müller P (2006a) Disjunct distributions during glacial and interglacial periods in mountain butterflies: Erebia epiphron as an example. J Evol Biol 19: 108-113. doi: 10. 1111/j. 1420-9101. 2005. 00980. x.
50. Schmitt T, Habel JC, Zimmermann M, Müller P (2006b) Genetic differentiation of the Marbled White butterfly, Melanargia galathea, accounts for glacial distribution patterns and postglacial range expansion in southeastern Europe. Mol Ecol 15: 1889-1901. doi: 10. 1111/j. 1365-294X. 2006. 02900. x.
51. Schmitt T, Rákosy L, Abadjiev S, Müller P (2007) Multiple differentiation centres of a non-Mediterranean butterfly species in south-eastern Europe. J Biogeogr 34: 939-950. doi: 10. 1111/j. 1365-2699. 2006. 01684. x.
52. Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9: 615-629. doi: 10. 1111/j. 1461-0248. 2006. 00889. x.
53. Steward JR, Lister AM (2001) Cryptic northern refugia and the origins of the modern biota. Trends Ecol Evol 16: 608-613. doi: 10. 1016/S0169-5347(01)02338-2.
54. Thévenon S, Couvet D (2002) The impact of inbreeding depression on population survival depending on demographic parameters. Anim Conserv 5: 53-60.
55. Tolman T, Lewington R (1997) Field guide butterflies of Britain and Europe. Harper Collins, London.
56. van Swaay CAM, Warren M (1999) Red Data Book of European butterflies (Rhopalocera). Nature and environment 99. Council of Europe Publishing, Strasbourg.
57. Watts PC, Saccheri J, Kemp SJ, Thompson DJ (2006) Population structure and the impact of regional and local habitat isolation upon levels of genetic diversity of the endangered damselfly Coenagrion mercuriale (Odonata: Zygoptera). Freshw Biol 51: 193-205. doi: 10. 1111/j. 1365-2427. 2005. 01478. x.
58. Watts PC, Thompson DJ, Allen KA, Kemp SJ (2007) How useful is DNA extracted from the legs of archieved insects for microsatellite-based population genetic analyses? J Insect Conserv 11: 195-198. doi: 10. 1007/s10841-006-9024-y.
59. Williams BL, Brawn JD, Paige KN (2003) Landscape scale genetic effects of habitat fragmentation on a high gene flow species: Speyeria idalia (Nymphalidae). Mol Ecol 12: 11-20. doi: 10. 1046/j. 1365-294X. 2003. 01700. x.
60. Zachos FE, Althoff C, v Steynitz Y, Eckert I, Hartl GB (2007) Genetic analysis of an isolated red deer (Cervus elaphus) population showing signs of inbreeding depression. Eur J Wildl Res 53: 61-67. doi: 10. 1007/s10344-006-0065-z.
61. Zhang D-X (2004) Lepidopteran microsatellite DNA: redundant but promising. Trends Ecol Evol 19: 507-509. doi: 10. 1016/j. tree. 2004. 07. 020.