Skip to main content

Advertisement

Log in

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

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

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 (F ST: 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 F IS 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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell, Malden

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 126:247–259

    Article  Google Scholar 

  • 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, Aberdeen

  • 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 54:97–105

    Google Scholar 

  • 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 9:111–118

    Google Scholar 

  • Collinge SK (2000) Effect of grassland fragmentation on insect species loss, colonization and movement patterns. Ecology 81:66–84

    Article  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed  CAS  Google Scholar 

  • Debinski DM (1994) Genetic diversity assessment in a metapopulation of the butterfly Euphydryas gillettii. Heredity 70:25–30

    Google Scholar 

  • 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 29:129–151

    Article  Google Scholar 

  • Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57

    Article  Google Scholar 

  • Föhst P (1992) Beiträge zur Kenntnis der Schmetterlingsfauna (Insecta: Lepidotera) des Hunsrück-Nahe-Gebiets (BRD, Rheinland-Pfalz). Fauna Flora Rheinland-Pfalz 3:1–336

    Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2008) Introduction to conservation genetics. University Press, Cambridge

    Google Scholar 

  • Gadeberg RME, Boomsma J (1997) Genetic population structure of the large blue butterfly Maculinea alcon in Denmark. J Insect Conserv 1:99–111

    Article  Google Scholar 

  • Goldberg CS, Waits LP (2010) Comparative landscape genetics of two pond-breeding amphibian species in a highly modified agricultural landscape. Mol Ecol 19:3650–3663

    Article  PubMed  Google Scholar 

  • Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J. Hered 86:485–486

    Google Scholar 

  • Guillot G, Santos F (2009) A computer program to simulate multilocus genotype data with spatially auto-correlated allele frequencies. Mol Ecol Res 9:1112–1120

    Article  CAS  Google Scholar 

  • 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 24:1406–1407

    Article  PubMed  CAS  Google Scholar 

  • 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 8:121–129

    Google Scholar 

  • 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 10:1659–1665

    Article  Google Scholar 

  • Habel JC, Meyer M, Schmitt T (2009b) The genetic consequence of differing ecological demands of a generalist and a specialist butterfly species. Biodivers Conserv 18:1895–1908

    Article  Google Scholar 

  • Habel JC, Dieker P, Schmitt T (2009c) Biogeographical connections between the Maghreb and the Mediterranean peninsulas of southern Europe. Biol J Linn Soc 98:693–703

    Article  Google Scholar 

  • 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)

  • Hanski IA, Gaggiotti OE (eds) (2004) Ecology, genetics, and evolution of metapopulations. Academic Press, San Diego

    Google Scholar 

  • Harris H, Hopkinson DA (1978) Handbook of enzyme electrophoresis in human genetics. North-Holland, Amsterdam

    Google Scholar 

  • Hebert PDN, Beaton MJ (1993) Methodologies for allozyme analysis using cellulose acetate electrophoresis. Helena Laboratories, Beaumont

    Google Scholar 

  • Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:965–1978

    Google Scholar 

  • Hofmann A (1994) Zygaenidae. In: Ebert G, Rennwald E (eds) Die Schmetterlinge Baden-Württembergs 3. Verlag Eugen Ulmer, Stuttgart, pp 196–335

    Google Scholar 

  • 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, Brussels

  • 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 13:172–183

    Article  Google Scholar 

  • Ladle RJ, Whittaker RJ (2010) Conservation biogeography. Wiley, New York

  • Louis EJ, Dempster ER (1987) An exact test for Hardy-Weinberg and multiple alleles. Biometrics 43:805–811

    Article  PubMed  CAS  Google Scholar 

  • 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 8:671–681

    Article  Google Scholar 

  • Luikart G, Cornuet J-M (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237

    Article  Google Scholar 

  • Melbourne BA, Hastings A (2008) Extinction risk depends strongly on factors contributing to stochasticity. Nature 454:100–103

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    PubMed  CAS  Google Scholar 

  • Phillips SJ, Dudík M (2008) Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31:161–175

    Article  Google Scholar 

  • Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Mod 190:231–259

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

  • Richardson BJ, Baverstock PR, Adams M (1986) Allozyme electrophoresis: a handbook for animal systematics and populations studies. Academic Press, Sydney

  • 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 12:865–889

    Article  PubMed  CAS  Google Scholar 

  • 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 7:1–234

    Google Scholar 

  • 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 31:885–893

    Article  Google Scholar 

  • Schmitt T, Seitz A (2004) Low diversity but high differentiation: the population genetics of Aglaope infausta (Zygaenidae: Lepidoptera). J Biogeogr 31:137–144

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 85:419–431

    Article  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.000—A software for population genetics data analysis. Department of Anthropology, University of Geneva, Geneva

  • Swets K (1988) Measuring the accuracy of diagnostic systems. Science 240:1285–1293

    Article  PubMed  CAS  Google Scholar 

  • Vandewoestijne S, Polus E, Baguette M (2005) Fragmentation and insects: theory and application to calcareous grasslands. Biotechnol Agron Soc Environ 9:139–142

    Google Scholar 

  • 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 104:265–273

    Article  Google Scholar 

  • Weir BS (1991) Genetic data analysis. Sinauer, Sunderland

    Google Scholar 

  • 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 128:542–552

    Article  Google Scholar 

  • 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 11:1451–1468

    Article  Google Scholar 

Download references

Acknowledgements

We acknowledge a grant from the German Science Foundation DFG (grant nr. SCHM 1659/3-1 and 3-2), from the German Academic Exchange Service (DAAD) and a scholarship “Arten- und Biotopschutz” from the Ministry of Rhineland-Palatinate to JCH. We are grateful to the governments of Rhineland-Palatinate and Luxembourg for the sampling permits.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jan Christian Habel.

Appendix

Appendix

  Allele frequencies of all polymorphic loci of all populations of Z. loti analysed

Rights and permissions

Reprints and permissions

About this article

Cite this article

Habel, J.C., Engler, J.O., Rödder, D. et al. Landscape genetics of a recent population extirpation in a burnet moth species. Conserv Genet 13, 247–255 (2012). https://doi.org/10.1007/s10592-011-0280-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-011-0280-3

Keywords

Navigation