Conservation Genetics

, Volume 13, Issue 1, pp 247–255 | Cite as

Landscape genetics of a recent population extirpation in a burnet moth species

  • Jan Christian Habel
  • Jan O. Engler
  • Dennis Rödder
  • Thomas Schmitt
Research Article


The intensification of agricultural land use over wide parts of Europe has led to the decline of semi-natural habitats, such as extensively used meadows, with those that remain often being small and isolated. These rapid changes in land use during recent decades have strongly affected populations inhabiting these ecosystems. Increasing habitat deterioration and declining permeability of the surrounding landscape matrix disrupt the gene flow within metapopulations. The burnet moth species Zygaena loti has suffered strongly from recent habitat fragmentation, as reflected by its declining abundance. We have studied its population genetic structure and found a high level of genetic diversity in some of the populations analysed, while others display low genetic diversity and a lack of heterozygosity. Zygaena loti was formerly highly abundant in meadows and along the skirts of forests. However, the species is currently restricted to isolated habitat remnants, which is reflected by the high genetic divergence among populations (FST: 0.136). Species distribution modelling as well as the spatial examination of panmictic clusters within the study area strongly support a scattered population structure for this species. We suggest that populations with a high level of genetic diversity still represent the former genetic structure of interconnected populations, while populations with low numbers of alleles, high FIS values, and a lack of heterozygosity display the negative effects of reduced interconnectivity. A continuous exchange of individuals is necessary to maintain high genetic variability. Based on these results, we draw the general conclusion that more common taxa with originally large population networks and high genetic diversity suffer stronger from sudden habitat fragmentation than highly specialised species with lower genetic diversity which have persisted in isolated patches for long periods of time.


Habitat fragmentation Population bottleneck Land-use change Allozyme electrophoresis Species Distribution Modelling Zygaena loti 


  1. Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell, MaldenGoogle Scholar
  2. 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 43:157–165CrossRefGoogle Scholar
  3. Binzenhöfer B, Schröder B, Strauss B, Biedermann R, Settele J (2005) Habitat models and habitat connectivity analysis for butterflies and burnet moths—the example of Zygaena carniolica and Coenonympha arcania. Biol Conserv 126:247–259CrossRefGoogle Scholar
  4. Bourn NAD (1995) The ecology, conservation and population genetics of three species of Zygaenid moths, Zygaena lonicerae, Zygaena purpuralis and Zygaena filipendulae in north west Scotland. PhD thesis. University of Aberdeen, AberdeenGoogle Scholar
  5. Britten HB, Brussard PF, Murphy DD, Austin GT (1994) Colony isolation and isozyme variability of the western seep fritillary, Speyeria nokomis apacheana (Nymphalidae), in the western Great Basin. Great Basin Nat 54:97–105Google Scholar
  6. Butaye J, Adriaens D, Honnay O (2005) Conservation and restoration of calcareous grasslands: a concise review of the effects of fragmentation and management on plant species. Biotechnol Agron Soc Environ 9:111–118Google Scholar
  7. Collinge SK (2000) Effect of grassland fragmentation on insect species loss, colonization and movement patterns. Ecology 81:66–84CrossRefGoogle Scholar
  8. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  9. Debinski DM (1994) Genetic diversity assessment in a metapopulation of the butterfly Euphydryas gillettii. Heredity 70:25–30Google Scholar
  10. Elith J, Graham CH, Anderson RP, Dudík M, Ferrier S, Guisan A, Hijmans RJ et al (2006) Novel methods improve prediction of species’ distributions form occurrence data. Ecography 29:129–151CrossRefGoogle Scholar
  11. Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57CrossRefGoogle Scholar
  12. Föhst P (1992) Beiträge zur Kenntnis der Schmetterlingsfauna (Insecta: Lepidotera) des Hunsrück-Nahe-Gebiets (BRD, Rheinland-Pfalz). Fauna Flora Rheinland-Pfalz 3:1–336Google Scholar
  13. Frankham R, Ballou JD, Briscoe DA (2008) Introduction to conservation genetics. University Press, CambridgeGoogle Scholar
  14. Gadeberg RME, Boomsma J (1997) Genetic population structure of the large blue butterfly Maculinea alcon in Denmark. J Insect Conserv 1:99–111CrossRefGoogle Scholar
  15. Goldberg CS, Waits LP (2010) Comparative landscape genetics of two pond-breeding amphibian species in a highly modified agricultural landscape. Mol Ecol 19:3650–3663PubMedCrossRefGoogle Scholar
  16. Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J. Hered 86:485–486Google Scholar
  17. Guillot G, Santos F (2009) A computer program to simulate multilocus genotype data with spatially auto-correlated allele frequencies. Mol Ecol Res 9:1112–1120CrossRefGoogle Scholar
  18. Guillot G, Santos F, Estoup A (2008) Analysing georeferenced population genetics data with Geneland: a new algorithm to deal with null alleles and a friendly graphical user interface. Bioinformatics 24:1406–1407PubMedCrossRefGoogle Scholar
  19. Habel JC, Meyer M, El Mousadik A, Schmitt T (2008) Africa goes Europa: The complete phylogeography of the Marbled White butterfly species complex Melanargia galathea/lachesis. Org Divers Evol 8:121–129Google Scholar
  20. Habel JC, Finger A, Meyer M, Louy D, Zachos F, Assmann T, Schmitt T (2009a) Unprecedented long-term genetic monomorphism in an endangered relict butterfly species. Conserv Genet 10:1659–1665CrossRefGoogle Scholar
  21. Habel JC, Meyer M, Schmitt T (2009b) The genetic consequence of differing ecological demands of a generalist and a specialist butterfly species. Biodivers Conserv 18:1895–1908CrossRefGoogle Scholar
  22. Habel JC, Dieker P, Schmitt T (2009c) Biogeographical connections between the Maghreb and the Mediterranean peninsulas of southern Europe. Biol J Linn Soc 98:693–703CrossRefGoogle Scholar
  23. Habel JC, Schmitt T, Meyer M, Finger A, Rödder D, Assmann T, Zachos FE (2010) Biogeography meets conservation: The genetic structure of the endangered lycaenid butterfly Lycaena helle (Denis & Schiffermüller, 1775)Google Scholar
  24. Hanski IA, Gaggiotti OE (eds) (2004) Ecology, genetics, and evolution of metapopulations. Academic Press, San DiegoGoogle Scholar
  25. Harris H, Hopkinson DA (1978) Handbook of enzyme electrophoresis in human genetics. North-Holland, AmsterdamGoogle Scholar
  26. Hebert PDN, Beaton MJ (1993) Methodologies for allozyme analysis using cellulose acetate electrophoresis. Helena Laboratories, BeaumontGoogle Scholar
  27. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:965–1978Google Scholar
  28. Hofmann A (1994) Zygaenidae. In: Ebert G, Rennwald E (eds) Die Schmetterlinge Baden-Württembergs 3. Verlag Eugen Ulmer, Stuttgart, pp 196–335Google Scholar
  29. Honnay O, Baguette M, Roldan-Ruiz I (2006) Conservation and restoration of fragmented biodiversity hotspots: calcareous grasslands of south-Belgium (Biocore). Scientific support plan for a sustainable development policy (SPSD II). Final report. Belgian Science Policy, BrusselsGoogle Scholar
  30. Kadlec T, Vrba P, Kepka P, Schmitt T, Konvicka M (2010) Tracking the decline of the once-common butterfly: delayed oviposition, demography and population genetics in the hermit Chazara briseis. Anim Conserv 13:172–183CrossRefGoogle Scholar
  31. Ladle RJ, Whittaker RJ (2010) Conservation biogeography. Wiley, New YorkGoogle Scholar
  32. Louis EJ, Dempster ER (1987) An exact test for Hardy-Weinberg and multiple alleles. Biometrics 43:805–811PubMedCrossRefGoogle Scholar
  33. Louy D, Habel JC, Schmitt T, Assmann T, Meyer M, Müller P (2007) Strongly diverging population genetic patterns of three skipper species: isolation, restricted gene flow and panmixis. Conserv Genet 8:671–681CrossRefGoogle Scholar
  34. Luikart G, Cornuet J-M (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237CrossRefGoogle Scholar
  35. Melbourne BA, Hastings A (2008) Extinction risk depends strongly on factors contributing to stochasticity. Nature 454:100–103PubMedCrossRefGoogle Scholar
  36. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedGoogle Scholar
  37. Phillips SJ, Dudík M (2008) Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31:161–175CrossRefGoogle Scholar
  38. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Mod 190:231–259CrossRefGoogle Scholar
  39. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959Google Scholar
  40. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237CrossRefGoogle Scholar
  41. Richardson BJ, Baverstock PR, Adams M (1986) Allozyme electrophoresis: a handbook for animal systematics and populations studies. Academic Press, SydneyGoogle Scholar
  42. Safner T, Miller MP, McRae BH, Fortin M-J, Manel S (2011) Comparison of Bayesian clustering and edge detection methods for inferring boundaries in landscape genetics. Int J Mol Sci 12:865–889PubMedCrossRefGoogle Scholar
  43. Schmidt-Koehl W (1977) Die Gross-Schmetterlinge des Saarlandes (Insecta, Lepidoptera), Diurna (Rhopalocera und Grypocera) Tagfalter Bombycidae und Sphingida Spinner und Schwärmer Monographischer Katalog. Abh Arbgemeinsch tier pflgeogr Heimatforsch Saarland 7:1–234Google Scholar
  44. Schmitt T, Hewitt GM (2004) Molecular biogeography of the arctic-alpine disjunct burnet moth species Zygaena exulans (Zygaenidae, Lepidoptera) in the Pyrenees and Alps. J Biogeogr 31:885–893CrossRefGoogle Scholar
  45. Schmitt T, Seitz A (2004) Low diversity but high differentiation: the population genetics of Aglaope infausta (Zygaenidae: Lepidoptera). J Biogeogr 31:137–144CrossRefGoogle Scholar
  46. 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 80:529–538CrossRefGoogle Scholar
  47. Schmitt T, Röber S, Seitz A (2005) 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 85:419–431CrossRefGoogle Scholar
  48. Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.000—A software for population genetics data analysis. Department of Anthropology, University of Geneva, GenevaGoogle Scholar
  49. Swets K (1988) Measuring the accuracy of diagnostic systems. Science 240:1285–1293PubMedCrossRefGoogle Scholar
  50. Vandewoestijne S, Polus E, Baguette M (2005) Fragmentation and insects: theory and application to calcareous grasslands. Biotechnol Agron Soc Environ 9:139–142Google Scholar
  51. Wallis DeVries MF, Poschlod P, Willems JH (2002) Challenges for the conservation of calcareous grasslands in north-western Europe: integrating the requirements of flora and fauna. Biol Conserv 104:265–273CrossRefGoogle Scholar
  52. Weir BS (1991) Genetic data analysis. Sinauer, SunderlandGoogle Scholar
  53. Wenzel M, Schmitt T, Weitzel M, Seitz A (2006) The severe decline of butterflies on western German calcareous grasslands during the last 30 years: a conservation problem. Biol Conserv 128:542–552CrossRefGoogle Scholar
  54. Wood BC, Pullin AS (2002) Persistence of species in a fragmented urban landscape: the importance of dispersal ability and habitat availability for grassland butterflies. Biodiv Conserv 11:1451–1468CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Jan Christian Habel
    • 1
  • Jan O. Engler
    • 2
    • 3
  • Dennis Rödder
    • 3
  • Thomas Schmitt
    • 2
  1. 1.Invertebrate BiologyNatural History Museum LuxembourgLuxembourgLuxembourg
  2. 2.Department of BiogeographyTrier UniversityTrierGermany
  3. 3.Zoological Research Museum Alexander KoenigBonnGermany

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