Skip to main content Skip to main navigation menu Skip to site footer
Article
Published: 2018-06-27

Phylogeography, genetic structure and wing pattern variation of Erebia pronoe (Esper, 1780) (Lepidoptera: Nymphalidae) in Europe

Institute of Biology and Ecology, Department of Zoology, Faculty of Science, P. J. Šafárik University in Košice, Šrobárova 2, 041 54 Košice, Slovakia.
Institute of Biology and Ecology, Department of Zoology, Faculty of Science, P. J. Šafárik University in Košice, Šrobárova 2, 041 54 Košice, Slovakia.
Institute of Biology and Ecology, Department of Cell Biology, Faculty of Science, P. J. Šafárik University in Košice, Šrobárova 2, 041 54 Košice; Slovakia.
Institute of Biology and Ecology, Department of Animal Physiology, Faculty of Science, P. J. Šafárik University in Košice, Šrobárova 2, 041 54 Košice; Slovakia. Department of Biology, Faculty of Humanities and Natural Sciences, University of Prešov, 17. novembra 15, 080 01 Prešov; Slovakia.
Institute of Biology and Ecology, Department of Zoology, Faculty of Science, P. J. Šafárik University in Košice, Šrobárova 2, 041 54 Košice, Slovakia.
Lepidoptera biogeography Erebia European mountains genetic differentiation mtDNA morphometrics Western Carpathians

Abstract

The distribution of genetic diversity within Erebia pronoe (Esper, 1780) populations in relation to biogeographic ranges is essential for understanding the processes of evolution, speciation and phylogeography in this species. A certain degree of genetic variability was expected because of the species’ linkage solely to calcareous soils. These ideas were focused on the water ringlet E. pronoe, a European endemic montane butterfly distributed over a narrow area of mountains, with its occurrence dependent on nutrient plants. Therefore, the origin, occurrence, phylogeography and variability are described in defined mountain localities in Europe in the light of glaciation events that occurred during the Quaternary (Pleistocene) period. The species’ phylogeography is based on a combination of two mitochondrial genes (COI, CR) and morphology (wing morphometry). The study comprised samples from the Western Carpathians, Pyrenees, Alps, South-Eastern Carpathians (Romania) and Southern Limestone Alps (Slovenia). Moreover, the species’ remarkable phylogeographic structure was observed, including four morphologic lineages and divergent genetic lineages. These lineages cover the Carpathian Mountains as well as the Western European mountains (Spanish populations) with no apparent gene flow between most regions, even across distances of only hundreds of kilometres.

 

References

  1. Avise, J. (2000) Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, 447 pp.

    Berns, A.R. (2014) A geometric morphometric analysis of wing shape variation in monarch butterflies Danaus plexippus. Ph.D dissertation, University of Michigan, Ann Arbor, MI, 38 pp.

    Besold, J. & Schmitt, T. (2015) More northern than ever thought: refugia of the Woodland Ringlet butterfly Erebia medusa (Nymphalidae: Satyrinae) in Northern Central Europe. Journal of Zoological Systematics and Evolutionary Research, 53 (1), 67–75.
    https://doi.org/10.1111/jzs.12076

    Borkhausen, M.B. (1788) Naturgeschichte der Europäischen Schmetterlinge nach systematischer Ordnung. Erster Theil. Tagschmetterlinge. Varrentrapp & Wenner, Frankfurt, 476 pp.

    Clement, M., Posada, D. & Crandall, K. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9 (10), 1657–1660.
    https://doi.org/10.1046/j.1365-294x.2000.01020.x

    Dincă, V., Cuvelier, S., Zakharov, E.V., Hebert, P.D.N. & Vila, R. (2010) Biogeography, ecology and conservation of Erebia oeme (Hübner) in the Carpathians (Lepidoptera: Nymphalidae: Satyrinae). Annales de la Société Entomologique de France, 46 (3–4), 486–498.
    https://doi.org/10.1080/00379271.2010.10697686

    Dincă, V., Runquist, M., Nilsson, M. & Vila, R. (2013) Dispersal, fragmentation, and isolation shape the phylogeography of the European lineages of Polyommatus (Agrodiaetus) ripartii (Lepidoptera: Lycaenidae). Biological Journal of the Linnean Society, 109 (4), 817–829.
    https://doi.org/10.1111/bij.12096

    Dincă, V., Montagud, S., Talavera, G., Hernández-Roldán, J., Munguira, M., García-barros, E., Hebert, P.D.N. & Vila, R. (2015) DNA barcode reference library for Iberian butterflies enables a continental-scale preview of potential cryptic diversity. Scientific Reports, 5, 12395.
    https://doi.org/10.1038/srep12395

    Esper, E.J.C. (1780) Der europäischen Schmetterlinge ersten Theils zweyter Band welcher die Fortsetzungen der Tagschmetterlinge von Tab. Wolfgang Walthers, Erlangen, 190 pp.

    Esper, E.J.C. (1805) Die Schmetterlinge in Abbildungen nach der Natur mit Beschreibungen. Erster Supplement-Band. Europäische Schmetterlinge. Walther, Erlangen,24 pp.

    Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3 (5), 294–299.

    Fruhstorfer, H. (1920) Altes und Neues über Erebien. Archiv für Naturgeschichte, 84 (A), 7, 83–108.

    Hall, T. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

    Hammer, Ø., Harper, D.A.T. & Ryan, P.D. (2001) PAST Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4 (1), 1–9.

    Herbst, J.F.W. (1796) Natursystem aller bekannten in- und ausländischen Insekten als eine Fortsezzung der von Büffonschen Naturgeschichte: Nach dem System des Ritters Carl von Linne bearbeitet von Carl Gustav Jablonsky. Pauli, Berlin, 304 pp.

    Kalivoda, H. & Víťaz, Ľ. (2015) Očkáň fatranský—Erebia pronoe (Esper, 1780). Available from: http://www.lepidoptera.sk/erebia_pronoe (accessed 1 June 2015)

    Klingenberg, C.P. (2011) MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources, 11 (2), 353–357.
    https://doi.org/10.1111/j.1755-0998.2010.02924.x

    Klingenberg, CH. (2016) Size, shape, and form: concepts of allometry in geometric morphometrics. Development Genes and Evolution, 226 (3), 113–37.
    https://doi.org/10.1007/s00427-016-0539-2

    Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16 (2), 111–120.
    https://doi.org/10.1007/BF01731581

    Kudrna, O., Pennerstorfer, J. & Lux, K. (2015) Distribution atlas of European butterflies and skippers. Wissenschaftlicher Verlag Peks i.K., Schwanfeld, 632 pp.

    Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33 (7), 1870–1874.
    https://doi.org/10.1093/molbev/msw054

    Librado, P. & Rozas, J. (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25 (11), 1451–1452.
    https://doi.org/10.1093/bioinformatics/btp187

    Linnæus, C. (1758) Systema naturæ per regna tria naturæ, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima. Salvius, Holmiæ, 824 pp.

    Lohman, D.J., Peggie, D., Pierce, N.E. & Meier, R. (2008) Phylogeography and genetic diversity of a widespread Old World butterfly, Lampides boeticus (Lepidoptera: Lycaenidae). BMC Evolutionary Biology, 8, 301.
    https://doi.org/10.1186/1471-2148-8-301

    Louy, D., Habel, J.CH., Ulrich, W. & Schmitt. T. (2013) Out of the Alps: The Biogeography of a Disjunctly Distributed Mountain Butterfly, the Almond-Eyed Ringlet Erebia alberganus (Lepidoptera, Satyrinae). Journal of Heredity, 105 (1), 28–38.
    https://doi.org/10.1093/jhered/est081

    Mortera, H. (2001) A new subspecies of Erebia pronoe (Esper, 1780) (Lepidoptera, Nymphalidae, Satyridae) from Picos de Europa (Asturias, Spain). Boletín SEA, 28, 63–65.

    Mutanen, M., & Kaitala, A. (2006) Genital variation in a dimorfic moth Selenia tetralunaria (Lepidoptera, Geometridae). Biological Journal of the Linnean Society, 87 (2), 297–307.
    https://doi.org/10.1111/j.1095-8312.2006.00578.x

    Mutanen, M., Kaitala, A. & Mönkkönen, M. (2006) Genital variation within and between three closely related Euxoa moth species: testing the lock-and-key hypotheses. Journal of Zoology, 268 (2), 109–119.
    https://doi.org/10.1111/j.1469-7998.2005.00029.x

    Panigaj, Ľ., Šemeláková, M. & Pristaš, P. (2015) The phylogenetic relationship of Western Carpathians Erebia spp. (Lepidoptera: Nymphalidae) based on mitochondrial cytochrome oxidase subunit I sequence analysis. Biologia, 70 (3), 393–399.
    https://doi.org/10.1515/biolog-2015-0045

    Paučulová, L., Šemeláková, M., Mutanen, M., Pristaš, P. & Panigaj, Ľ. (2017) Searching for the glacial refugia of Erebia euryale (Lepidoptera, Nymphalidae)—insights from mtDNA- and nDNA-based phylogeography in the Western Carpathians. Journal of Zoological Systematics and Evolutionary Research, 55 (2), 118–128.
    https://doi.org/10.1111/jzs.12156

    Rohlf, F.J. (2013) TPSUTIL, file utility program for Windows Version 1.56. Department of Ecology and Evolution, State University of New York, New York. [software]

    Schmitt, T. & Haubrich, K. (2008) The genetic structure of the mountain forest butterfly Erebia euryale unravels the late Pleistocene and postglacial history of the mountain coniferous forest biome in Europe. Molecular Biology, 17 (9), 2194–2207.
    https://doi.org/10.1111/j.1365-294X.2007.03687.x

    Schmitt, T. & Varga, Z. (2012) Extra-Mediterranean refugia: The rule and not the exception? Frontiers in Zoology, 9, 22.
    https://doi.org/10.1186/1742-9994-9-22

    Schmitt, T. (2014) Molecular biogeography of terrestrial insects in Europe: case studies in butterflies. In: Ujvárosi, L. & Marko, B. (Eds.), Romanian Carpathians, genetic centres or barriers in the process of postglacial isolation & speciation. Case studies in selected organisms. University Press, Cluj-Napoca, pp. 51–82.

    Schmitt, T., Louy, D., Zimmermann, E. & Habel, J.CH. (2016) Species radiation in the Alps: multiple range shifts caused diversification in Ringlet butterflies in the European high mountains. Organisms Diversity & Evolution, 16 (4), 791–808.
    https://doi.org/10.1007/s13127-016-0282-6

    Sielezniew, M., Patricelli, D., Rutkowski, R., Witek, M., Bonelli, S. & Buś, M.M. (2015) Population genetics of the endangered obligatorily myrmecophilous butterfly Phengaris (=Maculinea) arion in two areas of its European range. Insect Conservation and Diversity, 8 (6), 505–516.
    https://doi.org/10.1111/icad.12129

    Slamka, F. (2004) Die Tagfalter Mitteleuropas—östliche Teil: Bestimmung, Biotope und Bionomie, Verbreitung, Gefaehrdung. Slamka, Bratislava, 288 pp.

    Sonderegger, P. (2005) Die Erebien der Schweiz. Eigenverlag Peter Sonderegger, Brügg, 712 pp.

    Staudinger, O. (1861) Ueber einige neue und bisher verwechselte Lepidopteren. Entomologische Zeitung, 22, 287–293.

    Stöver, B.C., Müller, K.F. (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. Bioinformatics, 11, 7.
    https://doi.org/10.1186/1471-2105-11-7

    Šemeláková, M., Pristaš, P. & Panigaj, Ľ. (2013) Phylogenetic relatedness of Erebia medusa and E. epipsodea (Lepidoptera: Nymphalidae) confirmed. European Journal of Entomology, 110 (2), 379–382.
    https://doi.org/10.14411/eje.2013.049

    Tajima, F. (1989) Statistical method for testing the neutral mutationhypothesis by DNA polymorphism. Genetics, 123 (3), 585–595.

    Templeton, A.R., Crandall, K.A. & Sing, C.F. (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation, Genetics, 132 (2), 619–633.

    Tóth, J.P., Varga, K., Végvári, Z. & Varga, Z. (2012) Distribution of the Eastern knapweed fritillary (Melitaea ornata Christoph, 1893) (Lepidoptera: Nymphalidae): past, present and future. Journal of Insect Conservation, 17 (2), 245–255.
    https://doi.org/10.1007/s10841-012-9503-2

    van Swaay, C., Wynhoff, I., Verovnik, R., Wiemers, M., López Munguira, M., Maes, D., Sasic, M., Verstrael, T., Warren, M. & Settele, J. (2010) Erebia pronoe. The IUCN Red List of Threatened Species.
    https://doi.org/10.2305/IUCN.UK.2010-1.RLTS.T173253A6980361.en

    Varga, Z. (2008) Mountain coniferous forests, refugia and butterflies. Molecular Ecology, 17 (9), 2101–2103.
    https://doi.org/10.1111/j.1365-294X.2008.03744.x

    Vila, M. & Björklund, M. (2004) The utility of the neglected mitochondrial control region for evolutionary studies in Lepidoptera (Insecta). Journal of Molecular Evolution, 58 (3), 280–290.
    https://doi.org/10.1007/s00239-003-2550-2

    Vila, M., Marí-Mena, N., Guerrero, A. & Schmitt, T. (2010) Some butterflies do not care much about topography: a single genetic lineage of Erebia euryale (Nymphalidae) along the northern Iberian mountains. Journal of Zoological Systematics and Evolutionary Research, 49 (2), 119–132.
    https://doi.org/10.1111/j.1439-0469.2010.00587.x

    Viscosi, V. & Cardini, A. (2011) Leaves, taxonomy and geometric morphometrics: A simplified protocol for beginners. PLoS ONE, 6.
    https://doi.org/10.1371/journal.pone.0025630

    Warren, B.C.S. (1933) Notes on Erebiid Species. Entomologist’s Record, 45, 40–41.

    Zelditch, M.L., Swiderski, D.L., Sheets, H.D. & Fink, W.L. (2004) Geometric Morphometrics for Biologists. Elsevier Academic Press, Amsterdam, 488 pp.

How to Cite

PAUČULOVÁ, L., DZURINKA, M., ŠEMELÁKOVÁ, M., CSANÁDY, A., & PANIGAJ, ĽUBOMÍR. (2018). Phylogeography, genetic structure and wing pattern variation of <em>Erebia</em> <em>pronoe</em> (Esper, 1780) (Lepidoptera: Nymphalidae) in Europe. Zootaxa, 4441(2), 279–297. https://doi.org/10.11646/zootaxa.4441.2.5