Skip to main content

Advertisement

SpringerLink
Log in

Strongly diverging population genetic patterns of three skipper species: the role of habitat fragmentation and dispersal ability

  • Original Paper
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

The fragmentation of landscapes has an important impact on the conservation of biodiversity, and the genetic diversity is an important factor for a populations viability, influenced by the landscape structure. However, different species with differing ecological demands react rather different on the same landscape pattern. To address this feature, we studied three skipper species with differing habitat requirements (Lulworth Skipper Thymelicus acteon: a habitat specialist with low dispersal ability, Small Skipper Thymelicus sylvestris: a habitat generalist with low dispersal ability, Essex Skipper Thymelicus lineola: a habitat generalist with higher dispersal ability). We analysed 18 allozyme loci for 1,063 individuals in our western German study region with adjoining areas in Luxembourg and north-eastern France. The genetic diversity of all three species were intermediate in comparison with other butterfly species. The F ST was relatively high for T. acteon (5.1%), low for T. sylvestris (1.6%) and not significant for T. lineola. Isolation by distance analyses revealed a significant correlation for T. sylvestris explaining 20.3% of its differentiation, but no such structure was found for the two other species. Most likely, the high dispersal ability of T. lineola in comparison with T. sylvestris leads to a more or less panmictic structure and hence impedes isolation by distance. On the other hand, the isolation of the populations of T. acteon seems to be so strict that the populations develop independently. Although no general genetic impoverishing was observed for the endangered T. acteon, small populations had significantly lower genetic diversities than big populations, and therefore the high degree of isolation among populations might threaten its local and regional survival.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Asher J, Warren M, Fox R, Harding P, Jeffcoate G, Jeffcoate S (2001) The millennium atlas of butterflies in Britain and Ireland. Oxford University Press, Oxford

    Google Scholar 

  • Billington HL (1991) Effects of population size on genetic variation in a dioecious conifer Halocarpus bidwillii. Conserv Biol 5:115–119

    Article  Google Scholar 

  • Bink FA (1992) Ecologische Atlas van de Dagvlinders van Noordwest-Europa. Schuyt & Co. Uitgevers en Importeurs, Haarlem

    Google Scholar 

  • Bossart JL, Scriber JM (1995) Maintenance of ecologically significant genetic variation in the tiger swallowtail butterfly through differential selection and gene flow. Evolution 49:1163–1171

    Article  Google Scholar 

  • 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 

  • Britten HB, Brussard PF, Murphy DD, Ehrlich PR (1995) A test for isolation-by-distance in Central Rocky Mountain and Great Basin populations of Edith’s Checkerspot Butterfly (Euphydryas editha). J Heredity 86:204–210

    Google Scholar 

  • Brookes MI, Graneau YA, King P, Rose OC, Thomas CD, Mallet JLB (1997) Genetic analysis of founder bottlenecks in the rare british butterfly Plebejus argus. Conserv Biol 11:648–661

    Article  Google Scholar 

  • Buza L, Young A, Thrall P (2000) Genetic erosion, inbreeding and reduced fitness in fragmented populations of the endangered tetraploid pea Swainsona recta. Biol Conserv 93:177–186

    Article  Google Scholar 

  • Bryant EH, Backus VL, Clark ME, Reed DH (1999) Experimental tests of captive breeding for endangered species. Conserv Biol 13:1487–1496

    Article  Google Scholar 

  • Daly JC, Gregg P (1985) Genetic variation in Heliothis in Australia: species identification and gene flow in the two pest species H. armigera (Hübner) and H. punctigera Wallengren (Lepidoptera: Noctuidae). Bull Entomol Res 75:169–184

    Article  Google Scholar 

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

    Google Scholar 

  • Eanes WF, Koehn RK (1978) An analysis of genetic structure in the monarch butterfly, Danaus plexippus L. Evolution 32:784–797

    Article  Google Scholar 

  • Ebert G, Rennwald E (Hrsg.) (1991) Die Schmetterlinge Baden-Württembergs, Band 2. Verlag Eugen Ulmer, Stuttgart

  • Felsenstein J (1993) PHYLIP (Phylogeny inference package) Ver. 3.5.c. Department of Genetics, University of Washington, Seattle, Washington

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Google Scholar 

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

    Google Scholar 

  • Goulson D (1993) Allozyme variation in the butterfly Maniola jurtina (Lepidoptera: Satyrinae) (L.): evidence for selection. Heredity 71:386–393

    CAS  Google Scholar 

  • Graur D (1985) Gene diversity in Hymenoptera. Evolution 39:190–199

    Article  Google Scholar 

  • Hanski I (1999) Metapopulation ecology. Oxford University Press, Oxford

    Google Scholar 

  • Hansson B, Westerberg L (2002) On the correlation between heterozygosity and fitness in natural populations. Mol Ecol 11:2467–2474

    Article  PubMed  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 acetat electrophoresis. Helena Laboratories, Beaumont, TX

    Google Scholar 

  • Hudson QJ, Wilkins RJ, Waas JR, Hogg ID (2000) Low genetic variability in small populations of New Zealand kokako Callaeas cinerea wilsoni. Biol Conserv 96:105–112

    Article  Google Scholar 

  • Hughes JM, Zalucki MP (1984) Genetic variation in a continuously breeding population of Danaus plexippus L. (Lepidoptera: Nymphalidae). Heredity 52:1–7

    Google Scholar 

  • Jäggi C, Wirth T, Baur B (2000) Genetic variability in subpopulations of the asp viper (Vipera aspis) in the Swiss Jura mountains: implications for a conservation strategy. Biol Conserv 94:69–77

    Article  Google Scholar 

  • Johannesen J, Veith M, Seitz A (1996) Population genetic structure of the butterfly Melitaea didyma (Nymphalidae) along a northern distribution range border. Mol Ecol 5:259–267

    Article  Google Scholar 

  • Johannesen J, Samietz J, Wallaschek M, Seitz A, Veith M (1999) Patch connectivity and genetic variation in two congeneric grasshopper species with different habitat preferences. J Insect Conserv 3:201–209

    Article  Google Scholar 

  • Keller I, Largiadèr CR (2003) Recent habitat fragmentation caused by major roads leads to reduction of gene flow and loss of genetic variability in ground beetles. Proc Roy Soc London B, Biol Sci 270:417–423

    Article  CAS  Google Scholar 

  • Korman AK, Mallet J, Goodenough JL, Graves JB, Hayes JL, Hendricks DE, Luttrell R, Pair SD, Wall M (1993) Population structure in Heliothis virescens (Lepidoptera: Noctuidae): an estimation of gene flow. Ann Entomol Soc Am 86:182–188

    Google Scholar 

  • Kraus W (1993) Verzeichnis der Großschmetterlinge (Insecta: Lepidoptera) der Pfalz. Pollichia Buch 27 Selbstverlag der Pollichia, Bad Dürkheim

  • Lelièvre T (1992) Phylogenie des Polyommatinae et structure génétique de six espèces du genre Lysandra, HEMMING (Lépidoptères Lycaenidae). Doktorarbeit (Université de Provence), unpublished data, 221 S

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

    Article  PubMed  CAS  Google Scholar 

  • Luijten SH, Dierick A, Gerard J, Oostermeijer B, Raijmann LEL, Den Nijs HCM (2000) Population size, genetic variation, and reproductive success in a rapidly declining, self-compatible perennial (Arnica montana) in The Netherlands. Conserv Biol 14:1776–1787

    Article  Google Scholar 

  • Madsen T, Olsson M, Wittzell H, Stille B, Gullberg A, Shine R, Andersson S, Tegelström H (2000) Population size and genetic diversity in sand lizards (Lacerta agilis) and adders (Vipera berus). Biol Conserv 94:257–262

    Article  Google Scholar 

  • Madsen T, Shine R,Olsson M, Wittzell H (1999) Restoration of an inbred adder population. Nature 402:34–35

    Article  CAS  Google Scholar 

  • Marchi A, Addis G, Hermosa VE, Crnjar R (1996) Genetic divergence and evolution of Polyommatus coridon gennargenti (Lepidoptera, Lycaenidae) in Sardinia. Heredity 77:16–22

    Article  CAS  Google Scholar 

  • Meagher S (1999) Genetic diversity and Capillaria hepatica (Nematoda) prevalence in Michigan deer mouse populations. Evolution 53:1318–1324

    Article  Google Scholar 

  • Menken SBJ (1987) Is the extremely low heterozygosity level in Yponomeuta rorellus caused by bottlenecks? Evolution 41:630–637

    Article  Google Scholar 

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

    PubMed  Google Scholar 

  • Negedank J (1974) Trier und Umgebung. In: Gwinner M. (Hrsg.) Sammlung geologischer Führer 60. Gebrüder Borntraeger, Berlin

  • Nève G, Barascud B, Descimon H, Baguette M (2000) Genetic structure of Proclossiana eunomia populations at the regional scale (Lepidoptera, Nymphalidae). Heredity 84:657–666

    Article  PubMed  CAS  Google Scholar 

  • Nibouche S, Buès R, Toubon JF, Poitout S (1998) Allozyme polymorphism in the cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae): comparision of African and European populations. Heredity 80:438–445

    Article  CAS  Google Scholar 

  • Packer L, Taylor JS, Savignano DA, Bleser CA, Lane CP, Sommers LA (1998) Population biology of an endangered butterfly, Lycaeides melissa samuelis (Lepidoptera; Lycaenidae): genetic variation, gene flow, and taxonomic status. Can J Zool 76:320–329

    Article  Google Scholar 

  • Pedersen AA, Loeschcke V (2001) Conservation genetics of peripheral populations of the mygalomorph spider Atypus affinis (Atypidae) in northern Europe. Mol Ecol 10:1133–1142

    Article  PubMed  CAS  Google Scholar 

  • Pelz V (1995) Biosystematik der europäischen Arten des Tribus Melitaeini Newman, 1870. Oedippus 11:1–62

    Google Scholar 

  • Peterson MA (1995) Phenological isolation, gene flow and developmental differences among low- and high-elevation populations of Euphilotes enoptes (Lepidoptera: Lycaenidae). Evolution 49:446–455

    Article  Google Scholar 

  • Porter AH, Geiger H (1995) Limitations to the inference of gene flow at regional geographioc scales – an example from the Pieris napi group (Lepidoptera: Pieridae) in Europe. Biol J Linnean Soc 54:329–348

    Article  Google Scholar 

  • Porter AH, Schneider RW, Price BA (1995) Wing pattern and allozyme relationship in the Coenonympha arcania group, emphasising the C. gardetta-darwiniana contact area at Bellwald, Switzerland (Lepidoptera, Satyridae). Nota Lepidopterologica 17:155-174

    Google Scholar 

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

    Article  Google Scholar 

  • Richardson B, Baverstock PR, Adams M (1986) Allozyme electrophoresis. A handbook for animal systematics and population studies. Academic Press, San Diego

    Google Scholar 

  • Rosenzweig ML (1995) Species diversity in space and time. Cambridge University Press, Cambridge

    Google Scholar 

  • Rowe G, Beebee TJC, Burke T (1999) Microsatellite heterozygosity, fitness, and demography in natterjack toads Bufo calamita. Animal Conserv 2:85–92

    Article  Google Scholar 

  • Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494

    Article  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Schmidt-Koehl W (1977) Die Groß-Schmetterlinge des Saarlandes (Insecta, Lepidoptera): Tagfalter, Spinner und Schwärmer. Abhandlungen der Arbeitsgemeinschaft für tier- und pflanzengeografische Heimatforschung im Saarland 7:1–231

    Google Scholar 

  • Schmitt T, Hewitt G (2004) The genetic pattern of population threat and loss: a case study of butterflies. Mol Ecol 13:21–31

    Article  PubMed  CAS  Google Scholar 

  • Schmitt T, Seitz A (2001) Allozyme variation in Polyommatus coridon (Lepidoptera: Lycaenidae): identification of ice-age refugia and reconstruction of post-glacial expansion. J Biogeogr 28:1129–1136

    Article  Google Scholar 

  • Schmitt T, Seitz A (2002) Influence of habitat fragmentation on the genetic structure of Polyommatus coridon (Lepidoptera: Lycaenidae): implications for conservation. Biol Conserv 107:291–297

    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 (2002) Postglacial colonisation of western Central Europe by Polyommatus coridon (Poda 1761) (Lepidoptera: Lycaenidae): evidence from population genetics. Heredity 88:26–34

    Article  PubMed  CAS  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 Linnean 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 Linnean 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. Anthropology, University of Genève

  • Settele J, Feldmann R, Reinhardt R (1999) Die Tagfalter Deutschlands – Ein Handbuch für Freilandökologen, Umweltplaner und Naturschützer. Ulmer, Stuttgart

  • Siegismund HR (1993) G-Stat, ver. 3, Genetical statistical programs for the analysis of population data. The Arboretum, Royal Veterinary and Agricultural University, Horsholm, Denmark

  • Tolman T, Lewington R (1998) Die Tagfalter Europas und Nordwestafrikas. Franckh-Kosmos Verlag, Stuttgart

    Google Scholar 

  • Újvári B, Madsen T, Kotenko T, Olsson M, Shine R, Wittzell H (2002) Low genetic diversity threatens imminent extinction for the Hungarian meadow viper (Vipera ursinii rakosiensis). Biol Conserv 105:127–130

    Article  Google Scholar 

  • Vandewoestijne S, Nève G, Baguette M (1999) Spatial and temporal population genetic structure of the butterfly Aglais urticae L. (Lepidoptera, Nymphalidae). Mol Ecol 8:1539–1543

    Article  PubMed  Google Scholar 

  • van Swaay CAM, Warren M (1999) Red data book of European butterflies (Rhopalocera). Nature and environment 99, Council of Europe Publishing, Strasbourg

    Google Scholar 

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

    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 

  • Westemeier RL, Brawn JD, Simpson SA, Esker TL, Jansen RW, Walk JW, Eric L, Kershner EL, Bouzat JL, Paige KN (1998) Tracking the long-term decline and recovery of an isolated population. Science 282:1695–1698

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418

    Article  Google Scholar 

  • Zalucki MP, Hughes JM, Cater PA (1987) Genetic variation in Danaus plexippus L.: habitat selection or differences in activity time? Heredity 59:213–221

    Google Scholar 

Download references

Acknowledgements

This work was supported by the German Science Foundation (Deutsche Forschungsgemeinschaft, Grant No. SCHM 1659/3-1 and 3-2). We also acknowledge the scholarship for D. Louy of the Ministry for the environment and forests of the Rhineland-Palatinate and local authorities in Saarbrücken, Koblenz, Luxembourg and Metz for the permits to collect butterflies and to work in several protected areas. We thank D. Kime (La Fontaine) for the correction of our English.

Author information

Authors and Affiliations

  1. Biogeography, Fachbereich VI, University Trier, Am Wissenschaftspark 25-27, D-54296, Trier, Germany

    Dirk Louy, Jan Christian Habel, Thomas Schmitt & Paul Müller

  2. Institut of Ecology and Environmental Chemistry, University Lueneburg, D-21335, Lueneburg, Germany

    Dirk Louy & Thorsten Assmann

  3. Museum of natural history Luxembourg, L-2160, Luxembourg, Luxembourg

    Marc Meyer

Authors
  1. Dirk Louy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jan Christian Habel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas Schmitt
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thorsten Assmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marc Meyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Paul Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dirk Louy.

Appendix

Appendix

Table 5 Five parameters of genetic diversity for all populations analysed of Thymelicus acteon: Mean number of alleles per locus (A), percentage of expected heterozygosity (H e), percentage of observed heterozygosity (H o), total percentage of polymorphic loci (P tot), percentage of polymorphic loci with the most commonest allele not exceeding 95% (P 95), the number of individuals analysed (N) and the dates of capture. Values in parenthesis refer to the first 20 individuals of the respective sample. The “average 20” gives the average of the first 20 individuals of each sample
Full size table
Table 6 Five parameters of genetic diversity for all populations analysed of Thymelicus lineola. The data for the out group Vallée des Glaciers (F) is given separately at the bottom of the table. For further information see Appendix Table 5
Full size table
Table 7 Five parameters of genetic diversity for all populations analysed of Thymelicus sylvestris. The data for the out group Kresna Gorge (BG) is given separately at the bottom of the table. For further information see Appendix Table 5
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Louy, D., Habel, J.C., Schmitt, T. et al. Strongly diverging population genetic patterns of three skipper species: the role of habitat fragmentation and dispersal ability. Conserv Genet 8, 671–681 (2007). https://doi.org/10.1007/s10592-006-9213-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-006-9213-y

Keywords

Search

Navigation