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Contrasting genetic structure in cuckoo and predatory Maculinea butterflies

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Abstract

In Europe, both Maculinea alcon and M. teleius frequently co-occur inhabiting humid meadows. Although their parasitic life cycle is similar, ecological differences have been demonstrated between them: (i) spatial distribution of their eggs is different, and (ii) M. alcon is a cuckoo species, while M. teleius is predatory. The aim of the present study is to identify the genetic consequences of the ecological differences between these two butterfly species. To do so, we studied the genetic structure in samples from 9 M. alcon and 16 M. teleius sites obtained from the Carpathian Basin using 16 polymorphic enzyme markers. Both species exhibited relatively low enzyme polymorphism compared to other lycaenid species. Nevertheless, all measures of variation were significantly higher in M. teleius than in M. alcon. Genetic differentiation, however, was generally higher among M. alcon populations as compared to M. teleius. Moreover, the results of Bayesian clustering indicated a clear regional pattern with three well-defined cluster regions in M. alcon. In contrast, the regional pattern was less evident in M. teleius where we found three comparatively less distinct cluster regions. Putatively adaptive genetic differences were detected among cluster regions exploiting different host ants in M. alcon, while they were less evident in M. teleius. These results conform to our predictions on the differences between the utilization of their host ants. Since the pattern of genetic differentiation is different in the two Maculinea species, conservation strategies need also to differ in their cases.

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References

  • Aagaard K, Hindar K, Pullin AS, James CH, Hammarstedt O, Balstad T, Hanssen O (2002) Phylogenetic relationships in brown argus butterflies (Lepidoptera: Lycaenidae: Aricia) from north-western Europe. Biol J Linn Soc 75:27–37

    Article  Google Scholar 

  • Als TD, Nash DR, Boomsma JJ (2002) Geographical variation in host-ant specificity of the parasitic butterfly Maculinea alcon in Denmark. Ecol Entomol 27:403–414

    Article  Google Scholar 

  • Als TD, Vila R, Kandul NP, Nash DR, Yen SH, Hsu YF, Mignault AA, Boomsma JJ, Pierce NE (2004) The evolution of alternative parasitic life histories in large blue butterflies. Nature 432:386–390

    Article  CAS  PubMed  Google Scholar 

  • Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a F(st)-outlier method. BMC Bioinform 9:323

    Article  Google Scholar 

  • Barbero F, Jeremy A, Thomas JA, Bonelli S, Balletto E, Schönrogge K (2009) Queen ants make distinctive sounds that are mimicked by a butterfly social parasite. Science 323:782–785

    Article  CAS  PubMed  Google Scholar 

  • Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond Ser B-Biol Sci 263:1619–1626

    Article  Google Scholar 

  • Bereczki J, Pecsenye K, Peregovics L, Varga Z (2005) Pattern of genetic differentiation in the Maculinea alcon species group (Lepidoptera, Lycaenidae) in Central Europe. J Zool Syst Evol Res 43:157–165

    Article  Google Scholar 

  • Bereczki J, Pecsenye K, Varga Z (2006) Geographical versus food plant differentiation in populations of Maculinea alcon (Lepidoptera: Lycaenidae) in Northern Hungary. Eur J Entomol 103:725–732

    Article  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(3):648–661

    Article  Google Scholar 

  • Casacci LP, Barbero F, Balletto E (2014) The “evolutionarily significant unit” concept and its applicability in biological conservation. Ital J Zool 81(2):182–193

    Article  Google Scholar 

  • Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Am J Hum Genet 19:233–257

    CAS  PubMed Central  PubMed  Google Scholar 

  • Czekes Z, Markó B, Nash DR, Ferencz M, Lázár B, Rákosy L (2014) Differences in oviposition strategies between two ecotypes of the endangered myrmecophilous butterfly Maculinea alcon (Lepidoptera: Lycaenidae) under unique syntopic conditions. Insect Conserv Divers 7:122–131

    Article  Google Scholar 

  • de Guia APO, Saitoh T (2007) The gap between the concept and definitions in the evolutionarily significant unit: the need to integrate neutral genetic variation and adaptive variation. Ecol Res 22:604–612

    Article  Google Scholar 

  • Dupont P (2010) Plan national d’actions en faveur des Maculinea. OPIE, Document de travail, p 131

    Google Scholar 

  • Earl DA, von Holdt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources. doi:10.1007/s12686-011-9548-7

    Google Scholar 

  • Ebert G, Renwald E (1991) Die Schmetterlinge Baden-Württembergs. Eugen Ulmer GmbH, Stuttgart

    Google Scholar 

  • Elmes GW, Thomas JA (1987) Die gattung Maculinea. In: Gieger W (ed) Tagfalter und ihre Lebensräume: Arten, Gefährdung, Schutz. Schweizerische Bund für Naturschutz, Basel, pp 354–368

    Google Scholar 

  • Elmes GW, Thomas JA (1992) Complexity of species conservation in managed habitats—Interaction between Maculinea Butterflies and their ant hosts. Biodivers Conserv 1:155–169

    Article  Google Scholar 

  • Elmes GW, Thomas JA, Wardlaw JC (1991a) Larvae of Maculinea-rebeli, a large-blue butterfly, and their Myrmica host ants—wild adoption and behavior in ant-nests. J Zool 223:447–460

    Article  Google Scholar 

  • Elmes GW, Wardlaw JC, Thomas JA (1991b) Larvae of Maculinea-rebeli, a large-blue butterfly and their Myrmica host ants—patterns of caterpillar growth and survival. J Zool 224:79–92

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Figurny E, Woyciechowski M (1998) Flowerhead selection for oviposition by females of the sympatric butterfly species Maculinea teleius and M nausithous (Lepidoptera: Lycaenidae). Entomologia Generalis 23:215–222

    Article  Google Scholar 

  • Figurny-Puchalska E, Gadeberg RME, Boomsma JJ (2000) Comparison of genetic population structure of the large blue butterflies Maculinea nausithous and M-teleius. Biodivers Conserv 9:419–432

    Article  Google Scholar 

  • Francis B, Green M, Payne C (1994) GLIM 4. The statistical system of generalized linear interactive modelig. Oxford University Press, New York

    Google Scholar 

  • Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752

    Article  CAS  PubMed  Google Scholar 

  • Fric Z, Wahlberg N, Pech P, Zrzavy J (2007) Phylogeny and classification of the Phengaris-Maculinea clade (Lepidoptera: Lycaenidae): total evidence and phylogenetic species concepts. Syst Entomol 32:558–567

    Article  Google Scholar 

  • Funk WC, McKay JK, Paul A, Hohenlohe PA, Allendorf FW (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27(9):489–496

    Article  PubMed Central  PubMed  Google Scholar 

  • Fürst MA, Nash DR (2010) Host ant independent oviposition in the parasitic butterfly Maculinea alcon. Biol Lett 6:174–176

    Article  PubMed Central  PubMed  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

    Article  Google Scholar 

  • Goudet J (1995) Fstat version 1.2: a computer program to calculate F-statistics. J Hered 86:485

    Google Scholar 

  • Habel JC, Schmitt T (2009) The genetic consequences of different dispersal behaviours in Lycaenid butterfly species. Bull Entomol Res 99:513–523

    Article  CAS  PubMed  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2006) PAST—Paleontological Statistics, version 1.56 Web site <http://folk.uio.no/ohammer/past>

  • Hochberg ME, Clarke RT, Elmes GW, Thomas JA (1994) Population dynamic consequences of direct and indirect interactions involving a large blue butterfly and its plant and red ant hosts. J Anim Ecol 63:375–391

    Article  Google Scholar 

  • Hollós A, Pecsenye K, Bereczki J, Bátori E, Varga Z (2012) Pattern of genetic and morphometric differentiation in Maculinea nausithous (Lepidoptera: Lycaenidae) in the Carpathian Basin. Acta Zool Hung 58:87–103

    Google Scholar 

  • Höttinger H, Schlick-Steiner BC, Steiner FM (2003) The Alcon blue Maculinea alcon (Lepidoptera: Lycaenidae) in eastern Austria: status and conservation measures. Ekol-Bratisl 22:107–118

    Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241

    Article  Google Scholar 

  • Kirsmann A (2000) Eiablageverhalten von Maculinea alcon ([D. and Sch.] 1775) an Gentiana pneumonanthe und Gentiana asclepiadea UFZ-Bericht, Leipzig

  • Kőrösi A, Örvössy N, Batáry P, Kövér S, Peregovits L (2008) Restricted within-habitat movement and time-constrained egg laying of female Maculinea rebeli butterflies. Oecologia 156:455–464

    Article  PubMed  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  • Munguira ML, Martin J (1999) Action plan for the Maculinea butterflies in Europe. Council of Europe, Strasbourg

    Google Scholar 

  • Nash DR, Als TD, Maile R, Jones GR, Boomsma JJ (2008) Mosaic of chemical coevolution in a large blue butterfly. Science 319:88–90

    Article  CAS  PubMed  Google Scholar 

  • Nash DR, Als TD, Boomsma JJ (2011) Survival and growth of parasitic Maculinea alcon caterpillars (Lepidoptera, Lycaenidae) in laboratory nests of three Myrmica ant species. Insectes Soc 58:391–401

    Article  Google Scholar 

  • Nice CC, Shapiro AM (1999) Molecular and morphological divergence in the butterfly genus Lycaeides (Lepidoptera: Lycaenidae) in North America: evidence of recent speciation. J Evol Biol 12:936–950

    Article  CAS  Google Scholar 

  • Nowicki P, Witek M, Skorka P, Woyciechowski M (2005) Oviposition patterns in the myrmecophilous butterfly Maculinea alcon Denis and Schiffermuller (Lepidoptera: Lycaenidae) in relation to characteristics of foodplants and presence of ant hosts. Pol J Ecol 53:409–417

    Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pech P, Fric Z, Konvicka M, Zrzavy J (2004) Phylogeny of Maculinea blues (Lepidoptera: Lycaenidae) based on morphological and ecological characters: evolution of parasitic myrmecophily. Cladistics-the Int J Willi Hennig Soc 20:362–375

    Article  Google Scholar 

  • Pecsenye K, Bereczki J, Tihanyi B, Tóth A, Peregovits L, Varga Z (2007a) Genetic differentiation among the Maculinea species (Lepidoptera, Lycaenidae) in eastern Central Europe. Biol J Linn Soc 91:11–21

    Article  Google Scholar 

  • Pecsenye K, Bereczki J, Szilágyi M, Varga Z (2007b) High level of genetic variation in Aricia artaxerxes issekutzi (Lepidoptera: Lycaenidae) populations in Northern Hungary. Nota Lepideptorol 30:225–234

    Google Scholar 

  • Pritchard JK, Wen W (2004) Documentation for structure software: Version 2. Web site <http://pritch.bsd.uchicago.edu>

  • Pritchard JK, Stephens M, Donelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rakonczay Z (1989) Vörös Könyv. A Magyarországon kipusztult és veszélyeztetett növény- és állatfajok. Akadémiai Kiadó, Budapest

    Google Scholar 

  • Raymond M, Rousset F (1995) Genepop ver.1.2, a population genetics software for exact tests and ecumenicism. J Hered 86:246–249

    Google Scholar 

  • Schlick-Steiner BC, Steiner FM, Höttinger H, Nikiforov A, Mistrik R, Schafellner C, Baier P, Christian E (2004) A butterfly’s chemical key to various ant forts: intersection-odour or aggregate-odour multi-host mimicry? Naturwissenschaften 91:209–214

    Article  CAS  PubMed  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, Giessl A, Seitz A (2003) Did Polyommatus icarus (Lepidoptera: Lycaenidae) have distinct glacial refugia in southern Europe? Evidence from population genetics. Biol J Linn Soc 80:529–538

    Article  Google Scholar 

  • Schmitt T, Varga Z, Seitz A (2005) Are polyommatus hispana and polyommatus slovacus bivoltine polyommatus coridon (Lepidoptera: Lycaenidae)? The discriminatory value of genetics in taxonomy. Org Divers Evol 5:297–307

    Article  Google Scholar 

  • Schönrogge K, Wardlaw JC, Peters AJ, Everett S, Thomas JA, Elmes GW (2004) Changes in chemical signature and host specificity from larval retrieval to full social integration in the myrmecophilous butterfly Maculinea rebeli. J Chem Ecol 30(1):91–107

    Article  PubMed  Google Scholar 

  • Sielezniew M, Stankiewicz AM (2002) First data on host-ant specificity of parasitic butterfly Maculinea alcon (Den. and Schiff.) (Lepidoptera: Lycaenidae) in Poland and eastern Europe. Fragm Faun 45:123–130

    Article  Google Scholar 

  • Sielezniew M, Stankiewicz AM (2004) Simultaneous exploitation of Myrmica vandeli and M-scabrinodis (Hymenoptera: Formicidae) colonies by the endangered myrmecophilous butterfly Maculinea alcon (Lepidoptera: Lycaenidae). Eur J Entomol 101:693–696

    Article  Google Scholar 

  • Sielezniew M, Rutkowski R, Poikwicka-Tyszko D, Ratkiewicz M, Dziekanska I, Svitra G (2012) Differences in genetic variability between two ecotypes of the endangered myrmecophilous butterfly Phengaris (= Maculinea) alcon– the setting of conservation priorities. Insect Conserv Divers 5(3):223–236

    Article  Google Scholar 

  • Slatkin M (1985) Rare alleles as indicators of gene flow. Evolution 39:53–65

    Article  Google Scholar 

  • Sneath PH, Sokal RR (1973) Numerical Taxonomy. W. H. Freeman, San Francisco

    Google Scholar 

  • Stinchcombe JR, Hoekstra HE (2008) Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100:158–170

    Article  CAS  PubMed  Google Scholar 

  • Tartally A, Csősz S (2004) Adatok a Maculinea boglárkalepkék (Lepidoptera: Lycaenidae) kárpát-medencei hangyagazdáiról. Természetvédelmi közlemények 11:309–317

    Google Scholar 

  • Tartally A, Varga Z (2008) Host Ant Use of Maculinea Teleius in the Carpathian Basin (Lepidoptera: Lycaenidae). Acta Zool Acad Sci Hung 54:257–268

    Google Scholar 

  • Tartally A, Nash DR, Lengyel S, Varga Z (2008) Patterns of host ant use by sympatric populations of Maculinea alcon and M. ‘rebeli’ in the Carpathian Basin. Insectes Soc 55:370–381

    Article  Google Scholar 

  • Thomas JA (1976) The ecology of the large blue butterfly. In: Annual Report of the Instituteof Terrestrial Ecology, pp. 8–25

  • Thomas JA (1984) The behavior and Habitat requirements of Maculinea-Nausithous (the dusky large blue butterfly) and Maculinea-Teleius (the Scarce large blue) in France. Biol Conserv 28:325–347

    Article  Google Scholar 

  • Thomas JA (1995) The ecology and conservation of Maculinea arion and other European species of large blue butterfly. In: Piullin RI (ed) Ecology and conservation of butterflies. Chapman and Hall, London, pp 180–196

    Chapter  Google Scholar 

  • Thomas JA, Elmes GW (1998) Higher productivity at the cost of increased host-specificity when Maculinea butterfly larvae exploit ant colonies through trophallaxis rather than by predation. Ecol Entomol 23:457–464

    Article  Google Scholar 

  • Thomas JA, Elmes GW (2001) Food-plant niche selection rather than the presence of ant nests explains oviposition patterns in the myrmecophilous butterfly genus Maculinea. Proc R Soc Lond Ser B-Biol Sci 268:471–477

    Article  CAS  Google Scholar 

  • Thomas JA, Wardlaw JC (1992) The capacity of a Myrmica ant nest to support a predacious species of Maculinea butterfly. Oecologia 91:101–109

    Article  Google Scholar 

  • Thomas JA, Elmes GW, Wardlaw JC, Woyciechowski M (1989) Host specificity among Maculinea butterflies in Myrmica ant nests. Oecologia 79:452–457

    Article  Google Scholar 

  • Thomas JA, Munguira ML, Martin J, Elmes GW (1991) Basal Hatching by Maculinea butterfly eggs—a consequence of advanced myrmecophily. Biol J Linn Soc 44:175–184

    Article  Google Scholar 

  • Thomas JA, Clarke RT, Elmes GW, Hochberg ME (2000) Population dynamics in the genus Maculinea (Lepidoptera: Nymphalidae). In: Dempster JP, McLean FG (eds) Insect population dynamics. Chapman and Hall, London, pp 261–290

    Google Scholar 

  • Thomas JA, Elmes GW, Sielezniew M, Stankiewicz-Fiedurek A, Simcox DJ, Settele J, Schönrogge K (2015) Mimetic host shifts in an endangered social parasite of ants. Proc R Soc B 280:20122336

    Article  Google Scholar 

  • Ugelvig LV, Nielsen PS, Boomsma JJ, Nash DR (2011a) Reconstructing eight decades of genetic variation in an isolated Danish population of the large blue butterfly Maculinea arion. BMC Evol Biol 11:201

    Article  PubMed Central  PubMed  Google Scholar 

  • Ugelvig LV, Vila R, Pierce NE, Nash DR (2011b) A phylogenetic revision of the glaucopsyche section (Lepidoptera: Lycaenidae), with special focus on the phengaris-Maculinea clade. Mol Phylogenet Evol 61:237–243

    Article  CAS  PubMed  Google Scholar 

  • Vályi Nagy M, Csősz S (2007) Host ant specificity of the Large Blue butterfly, Maculinea alcon (Denis and Schiffermüller, 1775), in the Carpathian Basin (Hymenoptera: Formicidae; Lepidoptera Lycaenidae). Myrmecol News 10:124

    Google Scholar 

  • van Dyck H, Oostermeijer JGB, Talloen W, Vivian Feenstra V, van der Hidde A, Wynhoff I (2000) Does the presence of ant nests matter for oviposition to a specialized myrmecophilous Maculinea butterfly? Proc R Soc Lond Ser B-Biol Sci 267:861–866

    Article  Google Scholar 

  • Weir BS (1996) Data analysis II: methods for discrete population genetic data. Sinauer Assoc, Inc

    Google Scholar 

  • Witek M, Nowicki P, Sliwinska EB, Skórka P, Settele J, Schönrogge K, Woyciechowski M (2010) Local host ant specificity of Phengaris (Maculinea) teleius butterfly, an obligatory social parasite of Myrmica ants. Ecol Entomol 35:557–564

    Article  Google Scholar 

  • Witek M, Skórka P, Sliwinska EB, Nowicki P, Moron D, Settele J, Woyciechowski M (2011) Development of parasitic Maculinea teleius (Lepidoptera, Lycaenidae) larvae in laboratory nests of four Myrmica ant host species. Insectes Soc 58:403–411

    Article  PubMed Central  PubMed  Google Scholar 

  • Wright S (1978) Evolution and the genetics of populations. University of Chicago Press, Chicago

    Google Scholar 

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Acknowledgments

The study was supported by the MacMan EVK2-CT-2001-00126, NKFP-3 B/023/2004 and OTKA K84071, K109223 projects. Prof. L. Rákosy effectively supported our field work in Transylvania. J. V. Sipos, L. Peregovits, S. Szabó and P. Kozma contributed to the Maculinea sampling at several sites. The technical assistance of V. Mester in the electrophoretic work is very much respected. The useful comments of Z. Végvári and P. Orozco ter Wengel are greatly valued. The support of the Nature Conservation Authorities of Hungary is highly appreciated. AT was supported by a Marie Curie Intra European Fellowship within the 7th European Community Framework Programme, by a Marie Curie Career Integration Grant within the 7th European Community Framework Programme and AT and BJ were supported by János Bolyai Scholarship of the Hungarian Academy of Sciences.

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Correspondence to Katalin Pecsenye.

Appendix

Appendix

See Tables 5, 6 and 7.

Table 5 Maculinea alcon (A) and M. teleius (B) sample sites
Table 6 Measures of polymorphism in the Hungarian populations of Maculinea alcon (M. alc.) and M. teleius (M. tel.)
Table 7 Summary results of Structure

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Pecsenye, K., Bereczki, J., Juhász, E. et al. Contrasting genetic structure in cuckoo and predatory Maculinea butterflies. Conserv Genet 16, 939–954 (2015). https://doi.org/10.1007/s10592-015-0713-5

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