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.
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
Billington HL (1991) Effects of population size on genetic variation in a dioecious conifer Halocarpus bidwillii. Conserv Biol 5:115–119
Bink FA (1992) Ecologische Atlas van de Dagvlinders van Noordwest-Europa. Schuyt & Co. Uitgevers en Importeurs, Haarlem
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
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
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
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
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
Bryant EH, Backus VL, Clark ME, Reed DH (1999) Experimental tests of captive breeding for endangered species. Conserv Biol 13:1487–1496
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
Debinski DM (1994) Genetic diversity assessment in a metapopulation of the butterfly Euphydryas gillettii. Heredity 70: 25–30
Eanes WF, Koehn RK (1978) An analysis of genetic structure in the monarch butterfly, Danaus plexippus L. Evolution 32:784–797
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
Gadeberg RME, Boomsma JJ (1997) Genetic population structure of the large blue butterfly Maculinea alcon in Denmark. J Insect Conserv 1:99–111
Goulson D (1993) Allozyme variation in the butterfly Maniola jurtina (Lepidoptera: Satyrinae) (L.): evidence for selection. Heredity 71:386–393
Graur D (1985) Gene diversity in Hymenoptera. Evolution 39:190–199
Hanski I (1999) Metapopulation ecology. Oxford University Press, Oxford
Hansson B, Westerberg L (2002) On the correlation between heterozygosity and fitness in natural populations. Mol Ecol 11:2467–2474
Harris H, Hopkinson DA (1978) Handbook of enzyme electrophoresis in human genetics. North-Holland, Amsterdam
Hebert PDN, Beaton MJ (1993) Methodologies for allozyme analysis using cellulose acetat electrophoresis. Helena Laboratories, Beaumont, TX
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
Hughes JM, Zalucki MP (1984) Genetic variation in a continuously breeding population of Danaus plexippus L. (Lepidoptera: Nymphalidae). Heredity 52:1–7
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
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
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
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
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
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
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
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
Madsen T, Shine R,Olsson M, Wittzell H (1999) Restoration of an inbred adder population. Nature 402:34–35
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
Meagher S (1999) Genetic diversity and Capillaria hepatica (Nematoda) prevalence in Michigan deer mouse populations. Evolution 53:1318–1324
Menken SBJ (1987) Is the extremely low heterozygosity level in Yponomeuta rorellus caused by bottlenecks? Evolution 41:630–637
Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590
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
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
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
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
Pelz V (1995) Biosystematik der europäischen Arten des Tribus Melitaeini Newman, 1870. Oedippus 11:1–62
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
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
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
Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237
Richardson B, Baverstock PR, Adams M (1986) Allozyme electrophoresis. A handbook for animal systematics and population studies. Academic Press, San Diego
Rosenzweig ML (1995) Species diversity in space and time. Cambridge University Press, Cambridge
Rowe G, Beebee TJC, Burke T (1999) Microsatellite heterozygosity, fitness, and demography in natterjack toads Bufo calamita. Animal Conserv 2:85–92
Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
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
Schmitt T, Hewitt G (2004) The genetic pattern of population threat and loss: a case study of butterflies. Mol Ecol 13:21–31
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
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
Schmitt T, Seitz A (2004) Low diversity but high differentiation: the population genetics of Aglaope infausta (Zygaenidae: Lepidoptera). J Biogeogr 31:137–144
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
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
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
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
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
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
van Swaay CAM, Warren M (1999) Red data book of European butterflies (Rhopalocera). Nature and environment 99, Council of Europe Publishing, Strasbourg
Weir BS (1991) Genetic data analysis. Sinauer, Sunderland, MA
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
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
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
Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418
Zalucki MP, Hughes JM, Cater PA (1987) Genetic variation in Danaus plexippus L.: habitat selection or differences in activity time? Heredity 59:213–221
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
Corresponding author
Appendix
Appendix
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-006-9213-y