Molecular biogeography of the arctic-alpine disjunct burnet moth species Zygaena exulans (Zygaenidae, Lepidoptera) in the Pyrenees and Alps
Corresponding Author
Thomas Schmitt
Institut für Biogeographie, Universität Trier, Trier, Germany
Thomas Schmitt, Institut für Biogeographie, Fachbereich VI, Wissenschaftspark Trier-Petrisberg, Universität Trier, D-54286 Trier, Germany.E-mail: [email protected]Search for more papers by this author
Godfrey M. Hewitt
Biological Sciences, University of East Anglia, Norwich, UK
Search for more papers by this authorCorresponding Author
Thomas Schmitt
Institut für Biogeographie, Universität Trier, Trier, Germany
Thomas Schmitt, Institut für Biogeographie, Fachbereich VI, Wissenschaftspark Trier-Petrisberg, Universität Trier, D-54286 Trier, Germany.E-mail: [email protected]Search for more papers by this author
Godfrey M. Hewitt
Biological Sciences, University of East Anglia, Norwich, UK
Search for more papers by this authorAbstract
Aim The phylogeography of ‘southern’ species is relatively well studied in Europe. However, there are few data about ‘northern’ species, and so we studied the population genetic structure of the arctic-alpine distributed burnet moth Zygaena exulans as an exemplar.
Location and methods The allozymes of 209 individuals from seven populations (two from the Pyrenees, five from the Alps) were studied by electrophoresis.
Results All 15 analysed loci were polymorphic. The mean genetic diversities were moderately high (A: 1.99; He: 11.5; P: 65%). Mean genetic diversities were significantly higher in the Alps than in the Pyrenees in all cases. FST was 5.4% and FIS was 10%. Genetic distances were generally low with a mean of 0.022 between large populations. About 62% of the variance between populations was between the Alps and the Pyrenees. The two samples from the Pyrenees had no significant differentiation, whereas significant differentiation was detected between the populations from the Alps (FST = 2.8%, P = 0.02).
Main conclusion Zygaena exulans had a continuous distribution between the Alps and the Pyrenees during the last ice age. Most probably, the species was not present in Iberia, and the samples from the Pyrenees are derived from the southern edge of the glacial distribution area and thus became genetically impoverished. Post-glacial isolation in Alps and Pyrenees has resulted in a weak genetic differentiation between these two disjunct high mountain systems.
References
- Bernatchez, L. & Wilson, C.C. (1998) Comparative phylogeography of nearctic and palearctic fishes. Molecular Ecology, 7, 431–452.
- Britten, H.B., Brussard, P.F., Murphy, D.D. & Austin, G.T. (1994) Colony isolation and isozyme variability of the western seep fritillary, Speyeria nokomis apacheana (Nymphalidae), in the western Great Basin. The Great Basin Naturalist, 54, 97–105.
- Britten, H.B., Brussard, P.F., Murphy, D.D. & Ehrlich, P.R. (1995) A test for isolation-by-distance in Central Rocky Mountain and Great Basin populations of Edith's Checkerspot Butterfly (Euphydryas editha). Journal of Heredity, 86, 204–210.
- Bryant, E.H., Backus, V.L., Clark, M.E. & Reed, D.H. (1999) Experimental tests of captive breeding for endangered species. Conservation Biology, 13, 1487–1496.
- Buza, L., Young, A. & Thrall, P. (2000) Genetic erosion, inbreeding and reduced fitness in fragmented populations of the endangered tetraploid pea Swainsona recta. Biological Conservation, 93, 177–186.
- Comes, H.P. & Kadereit, J.W. (1998) The effect of Quarternary climatic changes on plant distribution and evolution. Trends in Plant Sciences, 3, 432–438.
- Coope, G.R. (1970) Interpretation of Quaternary insect fossils. Annual Review in Entomology, 15, 97–120.
- Coope, G.R. (1978) Constancy of insect species versus inconstancy of Quarternary environments. Diversity of insect faunas (Symp. R. ent. Soc. 9) (ed. by L.A. Mound and N. Waloff), pp. 176–187. Blackwell, Oxford.
- Coope, G.R. (1994) The response of insect faunas to glacial-interglacial climatic fluctuations. Philosophical Transactions of the Royal Society of London B, 344, 19–26.
- Debinski, D.M. (1994) Genetic diversity assessment in a metapopulation of the butterfly Euphydryas gillettii. Heredity, 70, 25–30.
- Descimon, H. (1995) La conservation des Parnassius en France: aspects zoogéographiques, écologiques, démographiques et génétiques. Editions OPIE, 1, 1–54.
- Elenga, H., Peyron, O., Bonnefille, R., Jolly, D., Cheddadi, R., Guiot, J., Andrieu, V., Bottema, S., Buchet, G., de Beaulieu, J.-L., Hamilton, A.C., Maley, J., Marchant, R., Perez-Obiol, R., Reille, M., Riollet, G., Scott, L., Straka, H., Taylor, D., Van Campo, E., Vincens, A., Laarif, F. & Jonson, H. (2000) Pollen-based biome reconstruction for southern Europe and Africa 18,000 yr BP. Journal of Biogeography, 27, 621–634.
- Emelianov, I., Mallet, J. & Baltensweiler, W. (1995) Genetic differentiation in Zeiraphera diniana (Lepidoptera: Tortricidae, the larch budmoth): polymorphism, host races or sibling species? Heredity, 75, 416–424.
- Fedorov, V.B. & Stenseth, N.C. (2001) Glacial survival of the Norwegian lemming (Lemmus lemmus) in Scandianavia: inference from mitochondrial DNA variation. Proceedings of the Royal Society of London B, 268, 809–814.
- Fedorov, V.B. & Stenseth, N.C. (2002) Multiple glacial refugia in North American Arctic: inference from phylogeography of the collared lemming (Dicrostonyx groenlandicus). Proceedings of the Royal Society of London B, 269, 2071–2077.
- Fedorov, V.B., Goropashnaya, A.V., Jaarola, M. & Cook, J.A. (2003) Phylogeography of lemmings (Lemmus): no evidence for postglacial colonization of Arctic from the Beringian refugium. Molecular Ecology, 12, 725–731.
- Felsenstein, J. (1993) PHYLIP (Phylogeny Inference Package) Ver. 3.5.c. Department of Genetics, University of Washington, Seattle, WA.
- Fischer, M. & Matthies, D. (1998) RAPD variation in relation to population size and plant fitness in the rare Gentianella germanica (Gentianaceae). American Journal of Botany, 85, 811–819.
- Fleming, M.A. & Cook, J.A. (2002) Phylogeography of endemic ermine (Mustela erminea) in southeast Alaska. Molecular Ecology, 11, 795–807.
- Harris, H. & Hopkinson, D.A. (1978) Handbook of enzyme electrophoresis in human genetics. North-Holland, Amsterdam.
- Harrison, R.G., Wintermeyer, S.F. & Odell, T.M. (1983) Patterns of genetic variation within an among gypsy moth, Lymantria dispar (Lepidoptera: Lymantriidae), populations. Annals of the Entomological Society of America, 76, 652–656.
- Hebert, P.D.N. & Beaton, M.J. (1993) Methodologies for allozyme analysis using cellulose acetate electrophoresis. Helena Laboratories, Beaumont, TX.
- Hewitt, G.M. (1988) Hybrid zones – natural laboratories for evolutionary studies. Trends in Ecology and Evolution, 3, 158–167.
- Hewitt, G.M. (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society of London, 58, 247–276.
- Hewitt, G.M. (1999) Post-glacial re-colonization of European biota. Biological Journal of the Linnean Society of London, 68, 87–112.
- Hewitt, G.M. (2000) The genetic legacy of the Quaternary ice ages. Nature, 405, 907–913.
- Hewitt, G.M. (2001) Speciation, hybrid zones and phylogeography – or seeing genes in space and time. Molecular Ecology, 10, 537–549.
- Hewitt, G.M. (2004) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society B, 359, 183–195.
- Holderegger, R., Stehlik, R. & Abbott, R.J. (2002) Molecular analysis of the Pleistocene history of Saxifragia oppositifolia in the Alps. Molecular Ecology, 11, 1409–1418.
- Huntley, B. & Birks, H.J.B. (1983) An atlas of past and present pollen maps of Europe: 0–130000 years ago. Cambridge University Press, Cambridge.
- Jaarola, M. & Searle, J.B. (2002) Phylogeography of field voles (Microtus agrestis) in Eurasia inferred from mitochondrial DNA sequences. Molecular Ecology, 11, 2613–2621.
- Jiggins, C.D. & Davies, N. (1998) Genetic evidence for a sibling species of Heliconis charithonia (Lepidoptera; Nymphalidae). Biological Journal of the Linnean Society, 64, 57–67.
- Knowles, L.L. (2001) Did the Pleistocene glaciations promote divergence? Tests of explicit refugial models in montane grasshoppers. Molecular Ecology, 10, 691–701.
- de Lattin, G. (1967) Grundriß der Zoogeographie. Gustav Fischer, Jena.
- Louis, E.J. & Dempster, E.R. (1987) An exact test for Hardy-Weinberg and multiple alleles. Biometrics, 43, 805–811.
- Luijten, S.H., Dierick, A., Gerard, J., Oostermeijer, B., Raijmann, L.E.L. & Den Nijs, H.C.M. (2000) Population size, genetic variation, and reproductive success in a rapidly declining, self-compatible perennial (Arnica montana) in The Netherlands. Conservation Biology, 14, 1776–1787.
- Lutz, E., Schneller, J.J. & Holderegger, R. (2000) Understanding population history for conservation purposes: population genetics of Saxifraga aizoides (Saxifragaceae) in the lowlands and lower mountains north of the Alps. American Journal of Botany, 87, 583–590.
- Madsen, T., Shine, R., Olsson, M. & Wittzell, H. (1999) Restoration of an inbred adder population. Nature, 402, 34–35.
- Marchi, A., Addis, G., Hermosa, V. E. & 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.
- Naumann, C.M., Tarmann, G.M. & Tremewan, W.G. (1999) The western palaearctic Zygaenidae. Apollo Books, Stenstrup.
10.1163/9789004631731 Google Scholar
- Nei, M. (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89, 583–590.
- Newman, D. & Pilson, D. (1997) Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution, 51, 354–362.
- Oostermeijer J.G.B., van Eijck, M.W., van Leeuwen, N.C. & den Nijs, J.C.M. (1995) Analysis of the relationship between allozyme heterozygosity and fitness in the rare Gentiana pneumonanthe L. Journal of Evolutionary Biology, 8, 739–759.
- Pelz, V. (1995) Biosystematik der europäischen Arten des Tribus Melitaeini Newman, 1870. Oedippus, 11, 1–62.
- Pfenninger, M., Bahl, A. & Streit, B. (1996) Isolation by distance in a population of a small land snail Trochoidea geyeri: evidence from direct and indirect methods. Proceedings of the Royal Society of London B, 263, 1211–1217.
- 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. Canadian Journal of Zoology, 66, 2751–2765.
- Porter, A.H. & 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. Biological Journal of the Linnean Society, 54, 329–348.
- 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.
- Porter, A.H., Schneider, R.W. & Price, B.A. (1995) Wing pattern and allozyme relationships in the Coenonympha arcania group, emphasising the C. gardetta-darwiniana contact area at Bellwald, Switzerland (Lepidoptera, Satyridae). Nota lepidopterologica, 17, 155–174.
- Raymond, M. & Rousset, F. (1995) An exact test for population differentiation. Evolution, 49, 1280–1283.
- Redenbach, Z. & Taylor, E.B. (1999) Zoogeographical implications of variation in mitochondrial DNA of Arctic grayling (Thymallus arcticus). Molecular Ecology, 8, 23–35.
- Reiss, R.A., Ashworth, A.C. & Schwert, D.P. (1999) Molecular genetic evidence for the post-Pleistocene divergence of populations of the arctic-alpine ground beetle Amara alpina (Paykull) (Coleoptera: Carabidae). Journal of Biogeography, 26, 785–794.
- Richardson, B.J., Baverstock, P.R. & Adams, M. (1986) Allozyme electrophoresis. A handbook for animal systematics and population studies. Academic Press, San Diego, CA.
- Rowe, G., Beebee, T.J.C. & Burke, T. (1999) Microsatellite heterozygosity, fitness, and demography in natterjack toads Bufo calamita. Animal Conservation, 2, 85–92.
- Saitou, N. & Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425.
- 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.
- 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.
- Schmitt, T. & Seitz, A. (2002a) Postglacial distribution area expansion of Polyommatus coridon (Lepidoptera: Lycaenidae) from its Ponto-Mediterranean glacial refugium. Heredity, 89, 20–26.
- Schmitt, T. & Seitz, A. (2002b) Influence of habitat fragmentation on the genetic structure of Polyommatus coridon (Lepidoptera: Lycaenidae): implications for conservation. Biological Conservation, 107, 291–297.
- Schmitt, T. & Seitz, A. (2004) Low diversity but high differentiation: the population genetics of Aglaope infausta (Zygaenidae: Lepidoptera). Journal of Biogeography, 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. Biological Journal of the Linnean Society, 80, 529–538.
- Schneider, S., Roessli, D. & Excoffier, L. (2000) Arlequin ver. 2.000 – a software for population genetics data analysis. Anthropology, University of Genève, Geneva.
- Selander, R.K. & Hudson, R.O. (1976) Animal population structure under close inbreeding: the land snail Rumina in southern France. American Naturalist, 110, 695–718.
- Siegismund, H.R. (1993) G-Stat, ver. 3, genetical statistical programs for the analysis of population data. The Arboretum, Royal Veterinary and Agricultural University, Horsholm, Denmark.
- Stehlik, I., Schneller, J.J. & Bachmann, K. (2001) Resistence or emigration: response of the high-alpine plant Eritrichium nanum (L.) Gaudin to the ice age within the Central Alps. Molecular Ecology, 10, 357–370.
- Taberlet, P., Fumagalli, L., Wust-Saucy, A.-G. & Cosson, J.-F. (1998) Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology, 7, 453–464.
- Tarasov, P.E., Volkova, V.S., Webb, T., III, Guiot, J., Andreev, A.A., Bezusko, L.G., Bezusko, T.V., Bykova, G.V., Dorofeyuk, N.I., Kvavadze, E.V., Osipova, I.M., Panova, N.K. & Sevastyanov, D.V. (2000) Last glacial maximum biomes reconstructed from pollen and plant macrofossil data from northern Eurasia. Journal of Biogeography, 27, 609–620.
- Tremblay, N.O. & Schoen, D.J. (1999) Molecular phylogeography of Dryas integrifolia: glacial refugia and postglacial recolonization. Molecular Ecology, 8, 1187–1198.
- Varga, Z. (2003) The geographical distribution of high mountain macrolepidoptera in Europe. Alpine biodiversity in Europe (ed. by L. Nagy, G. Grabherr, C. Körner and D.B.A. Thompson), pp. 239–257. Springer, Berlin, Heidelberg.
10.1007/978-3-642-18967-8_13 Google Scholar
- Weir, B.S. (1991) Genetic data analysis. Sinauer, Sunderland, MA.
- Westemeier, R.L., Brawn, J.D., Simpson, S.A., Esker, T.L., Jansen, R.W., Walk, J.W., Eric, L. Kershner, E.L., Bouzat, J.L. & Paige, K.N. (1998) Tracking the long-term decline and recovery of an isolated population. Science, 282, 1695–1698.
- Wiemers, M. (1998) Coenonympha darwiniana– a hybrid taxon? New insights through allozyme electrophoresis (Lepidoptera, Nymphalidae, Satyrinae). Memorias de la Société royal belge de l'Entomologie, 38, 41–69.
- Williams, D., Dunkerley, D., DeDecker, P., Kershaw, P. & Chappell, M. (1998) Quaternary environments. Arnold, London.