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The genetic consequences of different dispersal behaviours in Lycaenid butterfly species

Published online by Cambridge University Press:  19 February 2009

J.C. Habel  and
T. Schmitt
J.C. Habel*
Affiliation:
Biogeographie, Universität Trier, D – 54296 Trier, Germany Musée national d'histoire naturelle Luxembourg, L-2160 Luxembourg
T. Schmitt
Affiliation:
Biogeographie, Universität Trier, D – 54296 Trier, Germany
*
*Author for correspondence Fax: 00352475152 E-mail: [email protected]
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Abstract

Many studies in population ecology have shown that related species have different dispersal behaviours. Species with sedentary and migratory behaviour exist in butterflies. While the genetic responses to population isolation are well studied, the effects of different dispersal behaviours of species are widely unknown. Therefore, we analysed 19 allozyme loci of two lycaenid butterflies, Cupido minimus as a sedentary butterfly and Aricia agestis as a mobile and expansive species. We collected 594 individuals (280 of C. minimus and 314 of A. agestis) in a western German study region with adjacent areas in Luxembourg and northeastern France. The genetic differentiation among populations of A. agestis (FST=3.9%) was lower than in C. minimus (FST=5.6%). Both species built up an isolation-by-distance system, which is more pronounced in A. agestis than in C. minimus. The genetic diversity in C. minumus populations (e.g. Ptot=73.5%) is higher for all analysed parameters than in A. agestis (e.g. Ptot=52.1%). Both species show specific genetic characteristics fitting with their different dispersal behaviours and respective ecological strategies. In the light of conservation genetics, we deduce that highly fragmented populations do not necessarily have a high extinction probability, but this risk depending much more on specific population genetic structures. In the studied species, C. minimus preserves a complex genetic constitution by high population densities. The patchily distributed A. agestis represents less rare alleles, present only in some populations, and holds up genetic diversity by high mobility.

Keywords

Aricia agestisCupido minimusLepidopteradispersalallozyme electrophoresisgenetic diversityconservation genetics
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 99 , Issue 5 , October 2009 , pp. 513 - 523
Copyright
Copyright © 2009 Cambridge University Press

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References

Asher, J., Warren, M., Fox, R., Harding, P., Jeffcoate, G. & Jeffcoate, S. (2001) The Millennium Atlas of Butterflies in Britain and Ireland. 456 pp. Oxford, UK, Oxford University Press.Google Scholar
Baguette, M. (2003) Long distance dispersal and landscape occupancy in a metapopuation of the cranberry fritillary butterfly. Ecography 26, 153–160.CrossRefGoogle Scholar
Baguette, M., Petit, S. & Quéva, F. (2000) Population spatial structure and migration of three butterfly species within the same habitat network: consequences for conservation. Journal of Applied Ecology 37, 100–108.CrossRefGoogle 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. Journal of Zoological Systematics and Evolution Research 43, 157–165.CrossRefGoogle Scholar
Bink, F.A. (1992) Ecologische Atlas van de Dagvlinders van Noordwest-Europa. 512 pp. Haarlem, The Netherlands, Schuyt & Co., Uitgevers en Importeurs.Google Scholar
Bourn, N.A. de & Thomas, J.A. (1993) The ecology and conservation of the brown argus butterfly Aricia agestis in Britain. Biological Conservation 63, 67–74.CrossRefGoogle Scholar
Braman, S.K., Latimer, J.G., Oetting, R.D., McQueen, R.D., Eckberg, T.B. & Prinster, M. (2000) Management strategy, shade and landscape composition effects on urban landscape plant quality and arthropod abundance. Journal of Economic Entomology 93, 1464–1472.CrossRefGoogle ScholarPubMed
Brookes, M.I., Graneau, Y.A., King, P., Rose, O.C., Thomas, C.D. & Mallet, J.L.B. (1997) Genetic analysis of founder bottlenecks in the rare british butterfly Plebejus argus. Conservation Biology 11, 648–661.CrossRefGoogle Scholar
Chen, J., Franklin, J.F. & Spies, T.A. (1995) Growing-season microclimatic gradients from clearcut edges into old-growth Douglas-fir forests. Ecological Applications 5, 74–86.CrossRefGoogle Scholar
Collinge, S.K. (2000) Effects of grassland fragmentation on insect species loss, colonization and movement patterns. Ecology 81, 66–84.CrossRefGoogle Scholar
Conradt, L., Roper, T.J. & Thomas, C.D. (2001) Dispersal behaiour of individuals in metapopulations of two British butterflies. Oikos 95, 416–424.CrossRefGoogle Scholar
Cowley, M.J.R., Thomas, C.D., Roy, D.B., Wilson, R.J., Léon-Cortés, J.L., Guitiérrez, D., Bulman, C.R., Quinn, R.M., Moss, D. & Gastzzon, K.J. (2001) Density–distribution relationships in British butterflies, the effect of mobility and spatial scale. Journal of Animal Ecology 70, 410–425.CrossRefGoogle Scholar
Dennis, R.L.H. & Eales., H. (1997) Patch occupancy in Coenonympha tullia (Müller 1764) (Lepidoptera: Satyrinae): Habitat quality matters as much as patch size and isolation. Journal of Insect Conservation 1, 167–176.CrossRefGoogle Scholar
Descimon, H. (1995) La conservation des Parnassius en France: aspects zoogéographiques, écologiques, démographiques et génétiques. Editions OPIE 1, 1–54.Google Scholar
Ebert, G. & Rennwald, E. (Ed.) (1991) Die Schmetterlinge Baden-Württembergs, Vol. 2. 535 pp. Stuttgart, Germany, Eugen Ulmer.Google Scholar
Fernández-Rubio, F. (1991) Guia de mariposas diurnas de la Peninsular Ibérica, Baleares, Canarias, Azores y Madeira (Libytheidae, Nymphalidae, Riodinidae y Lycaenidae). Madrid, Spain, Ediciones Pirámide.Google Scholar
Figurny-Puchalska, E., Gadeberg, R.M.E. & Boomsma, J.J. (2000) Comparison of genetic population structure of the large blue butterfly Maculinea nausithous and M. teleius. Biodiversity and Conservation 9, 419–432.CrossRefGoogle Scholar
Frankham, R. (1995) Conservation genetics. Annual Reviews in Genetics 29, 305–327.CrossRefGoogle ScholarPubMed
Gadeberg, R.M.E. & Boomsma, J.J. (1997) Genetic population structure of the large blue butterfly Maculinea alcon in Denmark. Journal of Insect Conservation 1, 99–111.CrossRefGoogle Scholar
Goodman, D. (1987) The demography of change extinction. pp. 11–43in Soulé, M.E. (Ed.) Viable Populations for Conservation. Cambridge, UK, Cambridge University Press.CrossRefGoogle Scholar
Habel, J.C., 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). Journal of Biogeography 32, 1489–1497.CrossRefGoogle Scholar
Habel, J.C., Schmitt, T., Härdtle, W., Lütkepohl, M. & Assmann, T (2007) Dynamics in a butterfly-plant-ant system: influence of habitat characteristics on turnover rates of the endangered lycaenid Maculinea alcon. Ecological Entomology 32, 536–543.CrossRefGoogle Scholar
Hanski, I. (1991) Single species metapopulation dynamics: concepts, models, and observations. Biological Journal of the Linnean Society 42, 17–38.CrossRefGoogle Scholar
Hanski, I. (1994) Patch-occupancy dynamics in fragmented landscapes. Trends in Ecology and Evolution 9, 131–135.CrossRefGoogle ScholarPubMed
Hanski, I. (1999) Metapopulation Ecology. 313 pp. Oxford, UK, Oxford University Press.CrossRefGoogle Scholar
Hanski, I. & Gyllenberg, M. (1993) Two general metapopulation models and the corre-satellite species hypothesis. Nature 142, 17–41.Google Scholar
Hanski, I. & Singer, M.C. (2001) Extinction, colonization dynamics and host-plant choice in butterfly metapopulations. American Naturalist 158, 341–353.CrossRefGoogle ScholarPubMed
Harris, H. & Hopkinson, D.A. (1978) Handbook of Enzyme Electrophoresis in Human Genetics. 310 pp. Amsterdam, The Netherlands, University of Amsterdam.Google Scholar
Harrison, S. (1991) Local extinction in a metapopulation context: an empirical evaluation. Biologial Journal of the Linean Society 42, 73–88.CrossRefGoogle Scholar
Harrison, S. & Hastings, A. (1996) Genetic and evolutionary consequences of metapopulation structure. Trends in Ecology and Evolution 11, 180–183.CrossRefGoogle ScholarPubMed
Hebert, P.D.N. & Beaton, M.J. (1993) Methodologies for Allozyme Analysis using Cellulose Acetat Electrophoresis. 43 pp. Beaumont, Texas, USA, Helena Laboratories.Google Scholar
Hedrick, P.W. & Kalinowski., S.T. (2000) Inbreeding Depressision in Conservation Biology. Annual Review of Ecology and Systematics 31, 139–162.CrossRefGoogle Scholar
Holzhauer, S.I.J., Ekschmitt, K., Sanders, A.-C., Dauber, J. & Wolters, V. (2005) Effect of historic landscape change on the genetic structure of the bush-cricket Metrioptera roeseli. Landscape Ecology 34, 23–35.Google Scholar
Honnay, O., Coart, E., Butaye, J., Adriaens, D., Van Glabeke, S. & Roldán-Ruiz, I. (2006) Low impact of present and historical landscape configuration on the genetics of fragmented Anthyllis vulneraria populations. Biological Conservation 127, 411–419.CrossRefGoogle Scholar
Johannesen, J., Schwing, U., Seufert, W., Seitz, A. & Veith, M. (1997) Analysis of gene flow and habitat patch network for Chazara briseis (Lepidoptera: Satyridae) in an agricultural landscape. Biochemical Systematics and Ecology 25, 419–427.CrossRefGoogle Scholar
Johannesen, J., Veith, M. & Seitz, A. (1996) Population genetic structure of the butterfly Melitaea didyma (Nymphalidae) along a northern distribution range border. Molecular Ecology 5, 259–267.CrossRefGoogle Scholar
Keller, L.F. & Waller, D.M. (2002) Inbreededing effects in wild populations. Trends in Ecology and Evolution 17, 230–241.CrossRefGoogle Scholar
Krauss, J., Schmitt, T., Seitz, A., Steffan-Dewenter, I. & Tscharntke, T. (2004a) Effects of habitat fragmentation on the genetic structure of the monophagous butterfly Polyommatus coridon along its northern range margin. Molecular Ecology 13, 311–320.CrossRefGoogle ScholarPubMed
Krauss, J., Steffan-Dewenter, I. & Tscharntke, T. (2004b) Landscape occupancy and local population size depends on host plant distribution in the butterfly Cupido minimus. Biological Conservation 120, 355–361.CrossRefGoogle Scholar
Kruess, A. & Tscharntke, T. (2000) Species richness and parasitism in a fragmented landscape: experiments and field studies with insects on Vicia sepium. Oecologia 122, 129–137.CrossRefGoogle Scholar
Kuussaari, M., Hanski, I. & Singer, M. (2000) Local speciation and landscape-level influence on host use in an herbivorous insect. Ecology 81, 2177–2187.CrossRefGoogle Scholar
Lacy, R.C. (1987) Loss of genetic diversity from managed populations: Interacting effects of drift, mutation, immigration, selection and population subdivision. Conservation Biology 1, 143–158.CrossRefGoogle Scholar
León-Cortés, J.L., Lennon, J.J. & Tomas, C.D. (2003) Ecological dynamics of extinct species in empty habitat networks, 2, The role of host plant dynamics. Oikos 102, 465–477.CrossRefGoogle Scholar
Lewis, O.T. & Bryant, S.R. (2002) Butterflies on the move. Trends in Ecology and Evolution 17, 351–352.CrossRefGoogle Scholar
Louis, E.J. & Dempster, E.R. (1987) An exact test for Hardy-Weinberg and multiple alleles. Biometrics 43, 805–811.CrossRefGoogle ScholarPubMed
Louy, D., Habel, J.C., Schmitt, T., Assmann, T., Meyer, M. & Müller, P. (2007) Strongly diverging population genetic patterns of three skipper species: isolation, restricted gene flow and panmixis. Conservation Genetics 8, 671–681.CrossRefGoogle Scholar
Maes, D., Vanreuse, W., Talloen, W. & Van Dyck, H. (2004) Functional conservation units for the endangered Alcon Blue butterfly Maculinea alcon in Belgium (Lepidoptera: Lycaenidae). Biological Conservation 120, 229–241.CrossRefGoogle Scholar
Meglecz, E., Pecsenye, K., Peregovits, L. & Varga, Z. (1997) Allozyme variation in Parnassius mnemosyne (L.) (Lepidoptera) populations in North-East Hungary: variation within a subspecies group. Genetica 101, 59–66.CrossRefGoogle ScholarPubMed
Mousson, L., Nève, G. & Baguette, M. (1999) Metapopulation structure and conservation of the the dramberry fritillary Boloria aquilonaris (Lepidoptera, Nymphalidae) in Belgium. Biological Conservation 87, 285–293.CrossRefGoogle Scholar
Nei, M. (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583–590.CrossRefGoogle ScholarPubMed
Nève, G., Barascud, B., Hughes, R., Aubert, J., Descimon, H., Lebrun, P. & Baguette, M. (1996) Dispersal, colonization power and metapopulation structure in the vulnerable butterfly Proclossiana eunomia (Lepidoptera: Nymphalidae). Journal of Applied Ecology 33, 14–22.CrossRefGoogle Scholar
Oostermeijer, J.G.B., Brugman, M.L., Den Boer, E.R. & Den Nijs, H.C.M. (1996) Temporal and spatial variation in the demography of Gentiana pneumonanthe, a rare perennial herb. Journal of Ecology 84, 166–174.CrossRefGoogle Scholar
Packer, L., Taylor, J.S., Savignano, D.A., Bleser, C.A., Lane, C.P. & Sommers, L.A. (1998) Population biology of an endangered butterfly, Lycaeides melissa samuelis (Lepidoptera; Lycaenidae): genetic variation, gene flow and taxonomic status. Canadian Journal of Zoology 76, 320–329.CrossRefGoogle Scholar
Pelz, V. (1995) Biosystematik der europäischen Arten des Tribus Melitaeini Newman, 1870. Oedippus 11, 1–62.Google Scholar
Peterson, M.A. (1995) Phenological isolation, gene flow and developmental differences among low- and high-elevation populations of Euphilotes enoptes (Lepidoptera: Lycaenidae). Evolution 49, 446–455.Google ScholarPubMed
Porter, A.H. & Geiger, H. (1988) Genetic and phenotypic population structure of the Coenonympha tullia complex (Lepidoptera: Nymphalidae: Satyrinae) in California: no evidence for species boundaries. Canandian Journal of Zoology 66, 2751–2765.CrossRefGoogle Scholar
Porter, A.H. & Geiger, H. (1995) Limitations to the inference of gene flow at regional geographic scales – an example from the Pieris napi group (Lepidoptera: Pieridae) in Europe. Biological Journal of the Linnean Society 54, 329–348.Google Scholar
Porter, A.H. & Shapiro, A.M. (1989) Genetics and Biogeography of the Oeneis chryxus Complex (Satyrinae) in California. The Journal of Research on the Lepidoptera 28, 263–276.CrossRefGoogle Scholar
Radeloff, V.C., Mladenoff, D.J. & Boyce, M.S. (2000) The changing relation of landscape patterns and jack pine budworm populations during an outbreak. Oikos 90, 417–430.CrossRefGoogle Scholar
Reed, D.H. & Frankham, R. (2003) Correlation between fitness and genetic diversity. Conservation Biology 17, 230–237.CrossRefGoogle Scholar
Richardson, B.J., Baverstock, P.R. & Adams, M. (1986) Allozyme Electrophoresis: A Handbook for Animal Systematics and Population Studies. 420 pp. San Diego, CA, Academic Press.Google Scholar
Saunders, D.A., Hobbs, R.J. & Margules, C.R. (1991) Biological consequences of ecosystem fragmentation: a review. Conservation Biology 5, 18–32.CrossRefGoogle Scholar
Schmitt, T. & Seitz, A. (2001a) Intraspecific allozymatic differentiation reveals the glacial refugia and the postglacial expansions of European Erebia medusa (Lepidoptera: Nymphalidae). Biological Journal of the Linnean Society 74, 429–458.Google Scholar
Schmitt, T. & Seitz, A. (2001b) Allozyme variation in Polyommatus coridon (Lepidoptera: Lycaenidae): identification of ice-age refugia and reconstruction of post-glacial expansion. Journal of Biogeography 28, 1129–1136.CrossRefGoogle Scholar
Schmitt, T. & Seitz, A. (2002) Influence of habitat fragmentation on the genetic structure of Polyommatus coridon (Lepidoptera: Lycaenidae): implications for conservation. Biological Conservation 107, 291–297.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Schmitt, T., Gießl, A. & Seitz, A. (2003) Did Polyommatus icarus (Lepidoptera: Lycaenidae) have distinct glacial refugia in southern Europe? – Evidence from population genetics. Biological Journal of the Linnean Society 80, 529–538.CrossRefGoogle 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)? Biological Journal of the Linnean Society 85, 419–431.CrossRefGoogle Scholar
Schmitt, T., Habel, J.C., Besold, J., Becker, T., Johnen, L., Knolle, M., Rzepecki, A., Schultze, J. & Zapp, A. (2006) The Chalk-hill Blue Polyommatus coridon (Lycaenidae, Lepidoptera) in a highly fragmented landscape: How sedentary is a sedentary butterfly? Journal of Insect Conservation 10, 311–316.CrossRefGoogle Scholar
Schneider, S., Roessli, D. & Excoffier, L. (2000) Arlequin ver. 2.000 – A software for population genetics data analysis. Genève, Switzerland, Anthropology, University of Genève.Google Scholar
Settele, J., Feldmann, R. & Reinhardt, R. (1999) Die Tagfalter Deutschlands – Ein Handbuch für Freilandökologen, Umweltplaner und Naturschützer. 452 pp. Stuttgart, Germany, Ulmer.Google Scholar
Siegismund, H.R. (1993) G-Stat, ver. 3, Genetical statistical programs for the analysis of population data. The Arboretum, Royal Veterinary and Agricultural University, Denmark.Google Scholar
Thomas, J.A., Bourn, N.A.D., Clarke, R.T., Stewart, K.E., Simcox, D.J., Pearman, G.S., Curtis, R. & Goodger, B. (2001) The quality and isolation of habitat patches both determine where butterflies persist in fragmented landscapes. Proceedings of the Royal Society of London, Series B 268, 1791–1796.CrossRefGoogle ScholarPubMed
Vandewoestijne, S., Martin, T., Liégeois, S. & Baguette, M. (2004) Dispersal, landscape occupnacy and popualtion structure in the butterfly Melanargia galathea. Basic and Applied Ecology 5, 581–591.CrossRefGoogle Scholar
Van Swaay, C.A.M. (2002) The importance of calcareous grasslands for butterflies in Europe. Biological Conservation 104, 315–318.CrossRefGoogle Scholar
Wallis DeVries, M.F. (2004) From habitat quality assessment to conservation measures: a quantitative approach for the endangered butterfly Maculinea alcon. Conservation Biology 18, 489–499.CrossRefGoogle Scholar
Weidemann, H.-J. (1988) Tagfalter, Band 2. 372 pp. Melsungen, Germany, Verlag J. Neumann-Neudamm.Google Scholar
Weir, B.S. (1991) Genetic Data Analysis. 400 pp. Sunderland, MA, USA, Sinauer.Google Scholar
Wilcox, B.A. & Murphy, D.D. (1985) Conservation strategy: the effects of fragmentation on extinction. American Naturalist 125, 879–887.CrossRefGoogle Scholar
Wynhoff, I. (2001) At home on foreign meadows, the reintroduction of two Maculinea butterfly species. PhD thesis, Wageningen Agricultural University, The Netherlands.Google Scholar
Wynne, I.R., Wilson, R.J., Burke, A.S., Simpson, F., Pullin, A.S., Thomas, C.D. & Mallet, J. (2008) The effect of metapopulation processes on the spatial scale of adaptation in Aricia butterflies across an environmental gradient. Available online at http://www.ucl.ac.uk/taxome/jim/pap/wynne03.pdf, August 2008.Google Scholar
Young, A., Boyle, T. & Brown, T. (1996) The population genetic consequences of habitat fragmentation for plants. Trends in Ecology and Evolution 11, 413–419.CrossRefGoogle ScholarPubMed