Patterns of host use by brood parasitic Maculinea butterflies across Europe
Language English Country Great Britain, England Media print
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
30967080
PubMed Central
PMC6388033
DOI
10.1098/rstb.2018.0202
Knihovny.cz E-resources
- Keywords
- Phengaris, chemical mimicry, coevolution, geographic mosaic, local adaptation,
- MeSH
- Species Specificity MeSH
- Ants parasitology MeSH
- Nesting Behavior * MeSH
- Host-Parasite Interactions * MeSH
- Biological Coevolution * MeSH
- Butterflies physiology MeSH
- Symbiosis * MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Europe MeSH
The range of hosts exploited by a parasite is determined by several factors, including host availability, infectivity and exploitability. Each of these can be the target of natural selection on both host and parasite, which will determine the local outcome of interactions, and potentially lead to coevolution. However, geographical variation in host use and specificity has rarely been investigated. Maculinea (= Phengaris) butterflies are brood parasites of Myrmica ants that are patchily distributed across the Palæarctic and have been studied extensively in Europe. Here, we review the published records of ant host use by the European Maculinea species, as well as providing new host ant records for more than 100 sites across Europe. This comprehensive survey demonstrates that while all but one of the Myrmica species found on Maculinea sites have been recorded as hosts, the most common is often disproportionately highly exploited. Host sharing and host switching are both relatively common, but there is evidence of specialization at many sites, which varies among Maculinea species. We show that most Maculinea display the features expected for coevolution to occur in a geographic mosaic, which has probably allowed these rare butterflies to persist in Europe. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.
Amperstraße 13 80638 Munich Germany
Büro Geyer und Dolek Alpenblick 12 82237 Wörthsee Germany
Centre for Ecology and Hydrology Wallingford Maclean Building Benson Lane Wallingford OX10 8BB UK
Department of Life Sciences and Systems Biology University of Turin Turin 10123 Italy
Department of Zoology Hungarian Natural History Museum 1088 Budapest Baross u 13 Hungary
Department of Zoology University of Oxford Oxford OX1 3PS UK
Gevninge Bygade 10 4000 Roskilde Denmark
Institute of Biology University of Bialystok Ciołkowskiego 1 J 15 245 Białystok Poland
Institute of Environmental Sciences Jagiellonian University Gronostajowa 7 30 387 Kraków Poland
Lithuanian Entomological Society Akademijos 2 08412 Vilnius Lithuania
MTA ELTE MTM Ecology Research Group Pázmány Péter sétány 1 C Budapest H1117 Hungary
See more in PubMed
Lafferty KD, Kuris AM. 2002. Trophic strategies, animal diversity and body size. Trends Ecol. Evol. 17, 507–513. (10.1016/S0169-5347(02)02615-0) DOI
Whitlock MC. 1996. The red queen beats the jack-of-all-trades: the limitations on the evolution of phenotypic plasticity and niche breadth. Am. Nat. 148, S65–S77. (10.1086/285902) DOI
Forister ML, Dyer LA, Singer MS, Stireman JO III, Lill JT. 2012. Revisiting the evolution of ecological specialization, with emphasis on insect–plant interactions. Ecology 93, 981–991. (10.1890/11-0650.1) PubMed DOI
Futuyma DJ, Moreno G. 1988. The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19, 207–233. (10.1146/annurev.es.19.110188.001231) DOI
Combes C. 2001. Parasitism: the ecology and evolution of intimate interactions. Chicago, IL: University of Chicago Press.
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. Insect Soc. 58, 391–401. (10.1007/s00040-011-0157-y) PubMed DOI
Feeny P. 1976. Plant apparency and chemical defense. In Biochemical interaction between plants and insects: Proc. of the fifteenth annual meeting of the Phytochemical Society of North America (eds Wallace JW, Mansell RL), pp. 1–40. New York, NY: Plenum Press.
Schmid Hempel P. 2011. Evolutionary parasitology – the integrated study of infections, immunology, ecology, and genetics. Oxford, UK: Oxford University Press.
Beldomenico PM, Begon M. 2010. Disease spread, susceptibility and infection intensity: vicious circles? Trends Ecol. Evol. 25, 21–27. (10.1016/j.tree.2009.06.015) PubMed DOI
Little TJ, Watt K, Ebert D. 2006. Parasite-host specificity: experimental studies on the basis of parasite adaptation. Evolution 60, 31–38. (10.1111/j.0014-3820.2006.tb01079.x) PubMed DOI
Thompson JN. 1994. The coevolutionary process. Chicago, IL: University of Chicago Press.
Fox LR. 1988. Diffuse coevolution within complex communities. Ecology 69, 906–907. (10.2307/1941243) DOI
Janzen DH. 1980. When is it coevolution? Evolution 34, 611–612. (10.1111/j.1558-5646.1980.tb04849.x) PubMed DOI
Rothstein SI. 1990. A model system for coevolution: avian brood parasitism. Annu. Rev. Ecol. Syst. 21, 481–508. (10.1146/annurev.es.21.110190.002405) DOI
Kilner RM, Langmore NE. 2011. Cuckoos versus hosts in insects and birds: adaptations, counter-adaptations and outcomes. Biol. Rev. 86, 836–852. (10.1111/j.1469-185X.2010.00173.x) PubMed DOI
Thompson JN. 1999. Specific hypotheses on the geographic mosaic of coevolution? Am. Nat. 153, S1–S14. (10.1086/303208) DOI
Dawkins R, Krebs JR. 1979. Arms races between and within species. Proc. R. Soc. Lond. B 205, 489–511. (10.1098/rspb.1979.0081) PubMed DOI
Thompson JN. 2005. The geographic mosaic of coevolution. Chicago, IL: University of Chicago Press.
Thomas JA, Elmes GW, Wardlaw JC, Woyciechowski M. 1989. Host specificity among Maculinea butterflies in Myrmica ant nests. Oecologia 79, 452–457. (10.1007/Bf00378660) PubMed DOI
Elmes G, Thomas JA. 1987. Die Gattung Maculinea. In Tagfalter und ihre lebensräume: arten, gefährdung und schutz (ed. Geiger W.), pp. 354–368. Basel, Switzerland: Schweizerischer Bund für Naturschutz.
Thomas JA, Elmes GW, Wardlaw JC. 1998. Polymorphic growth in larvae of the butterfly Maculinea rebeli, a social parasite of Myrmica ant colonies. Proc. R. Soc. Lond. B 265, 1895–1901. (10.1098/rspb.1998.0517) DOI
Fiedler K. 2006. Ant-associates of Palaearctic lycaenid butterfly larvae (Hymenoptera: Formicidae; Lepidoptera: Lycaenidae) – a review. Myrmecol. News 9, 77–87.
Thomas JA, Elmes GW, Schönrogge K, Simcox DJ, Settele J. 2005. Primary hosts, secondary hosts and non-hosts: common confusions in the interpretation of host specificity in Maculinea butterflies and other social parasites of ants. In Studies on the ecology and conservation of butterflies in Europe (eds Settele J, Kühn E, Thomas JA), pp. 99–104. Sofia, Bulgaria: Pensoft.
Yamaguchi S. 1988. The life histories of five myrmecophilous lycaenid butterflies of Japan. Tokyo, Japan: Kodansha.
Hiraga S. 2003. Reidentifying of host ants of Maculinea arionides. Yadoriga 196, 31–34.
Maruyama M, Komatsu T, Kudo S, Shimada T, Kinomura K. 2013. The guests of Japanese ants. Minamiyana, Japan: Tokai University Press.
Ueda S, Komatsu T, Itino T, Arai R, Sakamoto H. 2016. Host-ant specificity of endangered large blue butterflies (Phengaris spp., Lepidoptera: Lycaenidae) in Japan. Sci. Rep. 6, 36364 (10.1038/srep36364) PubMed DOI PMC
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. (10.1111/j.1365-3113.2007.00387.x) DOI
Kőrösi Á, Örvössy N, Batáry P, Harnos A, Peregovits L. 2012. Different habitat selection by two sympatric Maculinea butterflies at small spatial scale. Ins. Conserv. Diver. 5, 118–126. (10.1111/j.1752-4598.2011.00138.x) DOI
Figurny E, Woyciechowski M. 1998. Flowerhead selection for oviposition by females of the sympatric butterfly species Maculinea teleius and M. nausithous (Lepidoptera : Lycaenidae). Entomol. Gen. 23, 215–222. (10.1127/entom.gen/23/1998/215) DOI
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. B 268, 471–477. (10.1098/rspb.2000.1398) PubMed DOI PMC
Thomas JA. 1984. The behaviour and habitat requirements of Maculinea nausithous (the dusky large blue butterfly) and M. teleius (the scarce large blue) in France. Biol. Conserv. 28, 325–347. (10.1016/0006-3207(84)90040-5) DOI
Thomas JA. 1995. The ecology and conservation of Maculinea arion and other European species of large blue butterfly. In Ecology and conservation of butterflies (ed. Pullin AS.), pp. 180–197. Berlin, Germany: Springer.
Elmes GW, Thomas JA, Wardlaw JC. 1991. 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. (10.1111/j.1469-7998.1991.tb04775.x) DOI
Frohawk FW. 1916. Further observations on the last stage of the larva of Lycaena arion. Trans. Entomol. Soc. Lond. 1915, 313–316. (10.1111/j.1365-2311.1916.tb02538.x) DOI
Als TD, Nash DR, Boomsma JJ. 2001. Adoption of parasitic Maculinea alcon caterpillars (Lepidoptera: Lycaenidae) by three Myrmica ant species. Anim. Behav. 62, 99–106. (10.1006/anbe.2001.1716) DOI
Thomas JA. 2002. Larval niche selection and evening exposure enhance adoption of a predacious social parasite, Maculinea arion (large blue butterfly), by Myrmica ants. Oecologia 132, 531–537. (10.1007/s00442-002-1002-9) PubMed DOI
Akino T, Knapp JJ, Thomas JA, Elmes GW. 1999. Chemical mimicry and host specificity in the butterfly Maculinea rebeli, a social parasite of Myrmica ant colonies. Proc. R. Soc. Lond. B 266, 1419–1426. (10.1098/rspb.1999.0796) DOI
Thomas JA, Elmes GW, Sielezniew M, Stankiewicz-Fiedurek A, Simcox DJ, Settele J, Schönrogge K. 2013. Mimetic host shifts in an endangered social parasite of ants. Proc. R. Soc. B 280, 20122336 (10.1098/rspb.2012.2336) PubMed DOI PMC
Elmes GW, Akino T, Thomas JA, Clarke RT, Knapp JJ. 2002. Interspecific differences in cuticular hydrocarbon profiles of Myrmica ants are sufficiently consistent to explain host specificity by Maculinea (large blue) butterflies. Oecologia 130, 525–535. (10.1007/s00442-001-0857-5) PubMed DOI
Nash DR, Als TD, Maile R, Jones GR, Boomsma JJ. 2008. A mosaic of chemical coevolution in a large blue butterfly. Science 319, 88–90. (10.1126/science.1149180) PubMed DOI
Casacci LP, Schönrogge K, Thomas JA, Balletto E, Bonelli S, Barbero F. 2019 Host specificity pattern and chemical deception in a social parasite of ants. Sci. Rep., 5913–4041. PubMed PMC
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. (10.1007/s00114-004-0518-8) PubMed DOI
Fiedler K. 1990. New information on the biology of Maculinea nausithous and M. teleius (Lepidoptera: Lycaenidae). Nota lepid 12, 246–256.
Sala M, Casacci LP, Balletto E, Bonelli S, Barbero F. 2014. Variation in butterfly larval acoustics as a strategy to infiltrate and exploit host ant colony resources. PLoS ONE 9, e94341 (10.1371/journal.pone.0094341) PubMed DOI PMC
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. (10.1046/j.1365-2311.1998.00153.x) DOI
Elfferich NW. 1998. New facts on the life history of the dusky large blue Maculinea nausithous (Lepidoptera: Lycaenidae) obtained by breeding with Myrmica ants in plaster nests. Deinsea 4, 97–102.
Thomas JA, Wardlaw JC. 1992. The capacity of a Myrmica ant nest to support a predacious species of Maculinea butterfly. Oecologia 91, 101–109. (10.1007/BF00317247) PubMed DOI
Wardlaw JC, Thomas JA, Elmes GW. 2000. Do Maculinea rebeli caterpillars provide vestigial mutualistic benefits to ants when living as social parasites inside Myrmica ant nests? Entomol. Exp. Appl. 95, 97–103. (10.1046/j.1570-7458.2000.00646.x) DOI
Witek M, Slipinski P, Naumiec K, Krupski A, Babik H, Walter B, Symonowicz B, Dubiec A. 2016. Performance of Myrmica ant colonies is correlated with the presence of social parasites. Ecol. Entomol. 41, 284–291. (10.1111/een.12299) DOI
Nash DR, Boomsma JJ. 2008. Communication between hosts and social parasites. In Sociobiology of communication - an interdisciplinary approach (eds d'Ettorre P, Hughes DP), pp. 55–79. Oxford, UK: Oxford University Press.
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, 91–107. (10.1023/B:JOEC.0000013184.18176.a9) PubMed DOI
Barbero F, Thomas JA, Bonelli S, Balletto E, Schonrogge K. 2009. Queen ants make distinctive sounds that are mimicked by a butterfly social parasite. Science 323, 782–785. (10.1126/science.1163583) PubMed DOI
Thomas JA, Schönrogge K, Bonelli S, Barbero F, Balletto E. 2010. Corruption of ant acoustical signals by mimetic social parasites: Maculinea butterflies achieve elevated status in host societies by mimicking the acoustics of queen ants. Commun. Integr. Biol. 3, 169–171. (10.4161/cib.3.2.10603) PubMed DOI PMC
Witek M, Skorka 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. (10.1007/s00040-011-0156-z) PubMed DOI PMC
Elmes GW, Wardlaw JC, Schonrogge K, Thomas JA, Clarke RT. 2004. Food stress causes differential survival of socially parasitic caterpillars of Maculinea rebeli integrated in colonies of host and non-host Myrmica ant species. Entomol. Exp. Appl. 110, 53–63. (10.1111/j.0013-8703.2004.00121.x) DOI
Fürst MA, Durey M, Nash DR. 2012. Testing the adjustable threshold model for intruder recognition on Myrmica ants in the context of a social parasite. Proc. R. Soc. B 279, 516–522. (10.1098/rspb.2011.0581) PubMed DOI PMC
Elmes GW, Thomas JA, Hammarstedt O, Munguira ML, Martín J, Van Der Made J. 1994. Differences in host-ant specificity between Spanish, Dutch and Swedish populations of the endangered butterfly, Maculinea alcon (Denis et Schiff.) (Lepidoptera). Memorabil. Zool. 48, 55–68.
Pech P, Fric Z, Konvicka M. 2007. Species-specificity of the Phengaris (Maculinea)--Myrmica host system: fact or myth? (Lepidoptera: Lycaenidae; Hymenoptera: Formicidae). Sociobiology 50, 983–1003.
Settele J, Thomas JA, Boomsma JJ, Kuehn E, Nash DR, Anton C, Woyciechowski M, Varga Z. 2002. MACulinea butterflies of the habitats directive and European red list as indicators and tools for conservation and MANagment (MacMan). Verh. Ges. Ökol 32, 63.
Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I. 1998. Inbreeding and extinction in a butterfly metapopulation. Nature 392, 491–494. (10.1038/33136) DOI
Thomas J. 1980. Why did the large blue become extinct in Britain? Oryx 15, 243–247. (10.1017/s0030605300024625) DOI
Wynhoff I. 1998. Lessons from the reintroduction of Maculinea teleius and M. nausithous in the Netherlands. J. Insect. Conserv. 2, 47–57. (10.1023/A:1009692723056) DOI
Van Swaay CAM, Warren MS. 1999. Red data book of European butterflies (Rhopalocera). Strasbourg, France: Council of Europe Publishing.
van Swaay C, et al. 2010. European Red list of butterflies. Luxembourg: Publications Office of the European Union.
van Swaay C, et al. 2011. Applying IUCN criteria to invertebrates: how red is the Red List of European butterflies? Biol. Conserv. 144, 470–478. (10.1016/j.biocon.2010.09.034) DOI
Thomas JA, Simcox DJ, Clarke RT. 2009. Successful conservation of a threatened Maculinea butterfly. Science 325, 80–83. (10.1126/science.1175726) PubMed DOI
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. (10.1038/nature03020) PubMed DOI
Sielezniew M, Rutkowski R, Ponikwicka-Tyszko D, Dzienkańska I, Švitra G. 2012. Differences in genetic variability between two ecotypes of the endangered myrmecophilous butterfly Phengaris (=Maculinea) alcon—the setting of conservation priorities. Insect Conserv. Diversity 5, 223–236. (10.1111/j.1752-4598.2011.00163.x). DOI
Koubínová D, Dinca V, Dapporto L, Voda R, Suchan T, Vila R, Alvarez N. 2017. Genomics of extreme ecological specialists: multiple convergent evolution but no genetic divergence between ecotypes of Maculinea alcon butterflies. Sci. Rep. 7, 13752 (10.1038/s41598-017-12938-8) PubMed DOI PMC
Tartally A, Kelager A, Furst MA, Nash DR. 2016. Host plant use drives genetic differentiation in syntopic populations of Maculinea alcon. Peerj 4, e1865 (10.7717/peerj.1865) PubMed DOI PMC
Ugelvig LV, Vila R, Pierce NE, Nash DR. 2011. A phylogenetic revision of the Glaucopsyche section (Lepidoptera: Lycaenidae), with special focus on the Phengaris–Maculinea clade. Mol. Phylogenet. Evol. 61, 237–243. (10.1016/j.ympev.2011.05.016) PubMed DOI
Schönrogge K, et al. In preparation. A tale of two species: chemical similarities and differences between two forms of Maculinea alcon. Insect Conserv. Diversity.
Bolt D, Neumeyer R, Rey A, Sohni V. 2010. Kleiner Moorbläuling (Lepidoptera: Lycaenidae: Phengaris alcon) und Echte Knotenameisen (Hymenoptera: Formicidae: Myrmica) am Pfannenstiel (Kanton Zürich, Schweiz). Entomol. Helvet. 3, 27–48.
Gros P. 2002. Nachweis von Maculinea rebeli (HIRSCHKE, 1904) aus dem Bundesland Salzburg (Lepidoptera: Lycaenidae). Z. Arb. Gem. Öst. Ent 54, 13–23.
Tessier M. 2012. Inventaire de l'Azuré des mouillères Maculinea alcon (DENIS & SCHIFFERMÜLLER, 1775) (Lepidoptera Lycaenidae) en Ariège. I. Résultats préliminaires. Bull. Soc. Linn. Bordeaux 147, 129–139.
Hirschke H. 1905. Eine neue hochalpine Form der Lycaena alcon F. aus den steirischen Alpen. Jahres-Bericht des Wiener Entomol Vereines 15, 1–3.
Kudrna O, Fric ZF. 2013. On the identity and taxonomic status of Lycaena alcon rebeli HIRSCHKE, 1905 — a long story of confusion and ignorance resulting in the fabrication of a ‘ghost species’ (Lepidoptera: Lycaenidae). Nachrichten des Entomologischen Vereins Apollo 34, 117–124.
Tartally A, Koschuh A, Varga Z. 2014. The re-discovered Maculinea rebeli (Hirschke, 1904): host ant usage, parasitoid and initial food plant around the type locality with taxonomical aspects (Lepidoptera, Lycaenidae). ZooKeys 406, 25–40. (10.3897/zookeys.406.7124). PubMed DOI PMC
Sliwinska EB, Nowicki P, Nash DR, Witek M, Settele J, Woyciechowski M. 2006. Morphology of caterpillars and pupae of European Maculinea species (Lepidoptera: Lycaenidae) with an identification table. Entomol. Fennica 17, 351–358.
Lex A, Gehlenborg N, Strobelt H, Vuillemot R, Pfister H. 2014. UpSet: visualization of intersecting sets. IEEE Trans. Vis. Comput. Graph 20, 1983–1992. (10.1109/TVCG.2014.2346248) PubMed DOI PMC
Lex A, Gehlenborg N. 2014. Points of view: sets and intersections. Nat. Methods 11, 779 (10.1038/nmeth.3033) DOI
Conway J, Lex A, Gehlenborg N. 2017. UpSetR: an R package for the visualization of intersecting sets and their properties. Bioinformatics 33, 2938–2940. (10.1093/bioinformatics/btx364) PubMed DOI PMC
R Core Team. 2018. R: A language and environment for statistical computing, 3.5.1 edn Vienna, Austria: R Foundation for Statistical Computing.
Wardlaw JC, Elmes GW, Thomas JA. 1998. Techniques for studying Maculinea butterflies: II. Identification guide to Myrmica ants found on Maculinea sites in Europe. J. Insect Conserv. 2, 119–127. (10.1023/a:1009621522615) DOI
Seifert B. 1996. Ameisen: beobachten, bestimmen. Augsburg, Germany: Naturbuch Verlag.
Czechowski W, Radchenko A, Czechowska W. 2002. The ants (hymenoptera, formicidae) of Poland. Warszawa, Poland: Museum and Institute of Zoology PAS.
Radchenko AG, Elmes GW. 2010. Myrmica ants (Hymenoptera: Formicidae) of the Old World Warszawa, Poland: Natura optima dux Foundation.
Elmes GW, Thomas JA, Wardlaw JC, Hochberg ME, Clarke RT, Simcox DJ. 1998. The ecology of Myrmica ants in relation to the conservation of Maculinea butterflies. J. Insect Conserv. 2, 67–78. (10.1023/A:1009696823965) DOI
Fraser AM, Tregenza T, Wedell N, Elgar MA, Pierce NE. 2002. Oviposition tests of ant preference in a myrmecophilous butterfly. J. Evol. Biol. 15, 861–870. (10.1046/j.1420-9101.2002.00434.x) DOI
Pierce NE, Elgar MA. 1985. The influence of ants on host plant-selection by Jalmenus evagoras, a Myrmecophilous Lycaenid butterfly. Behav. Ecol. Sociobiol. 16, 209–222. (10.1007/Bf00310983) DOI
Atsatt PR. 1981. Ant-dependent food plant selection by the mistletoe butterfly Ogyris amaryllis (Lycaenidae). Oecologia 48, 60–63. (10.1007/BF00346988) PubMed DOI
Fürst MA, Nash DR. 2010. Host ant independent oviposition in the parasitic butterfly Maculinea alcon. Biol. Lett. 6, 174–176. (10.1098/rsbl.2009.0730) PubMed DOI PMC
van Dyck H, Talloen W, Feenstra V, Wynhoff I. 2000. Does the presence of ant nests matter for oviposition to a specialized myrmecophilous Maculinea butterfly? Proc. R. Soc. Lond. B 267, 861–866. (10.1098/rspb.2000.1082) PubMed DOI PMC
Musche M, Anton C, Worgan A, Settele J. 2006. No experimental evidence for host ant related oviposition in a parasitic butterfly. J. Insect Behav. 19, 631–643. (10.1007/s10905-006-9053-0) DOI
Patricelli D, Barbero F, La Morgia V, Casacci LP, Witek M, Balletto E, Bonelli S. 2011. To lay or not to lay: oviposition of Maculinea arion in relation to Myrmica ant presence and host plant phenology. Anim. Behav. 82, 791–799. (10.1016/j.anbehav.2011.07.011) DOI
Wynhoff I, Grutters M, van Langevelde F. 2008. Looking for the ants: selection of oviposition sites by two myrmecophilous butterfly species. Anim. Biol. 58, 371–388. (10.1163/157075608X383683) DOI
Patricelli D, et al. 2015. Plant defences against ants provide a pathway to social parasitism in butterflies. Proc. R. Soc. B 282, 20151111 (10.1098/rspb.2015.1111) PubMed DOI PMC
Van Dyck H, Regniers S. 2010. Egg spreading in the ant-parasitic butterfly, Maculinea alcon: from individual behaviour to egg distribution pattern. Anim. Behav. 80, 621–627. (10.1016/j.anbehav.2010.06.021) DOI
Nash DR, Andersen A. 2015. Maculinea sommerfugle og stikmyrer på danske heder - coevolution i tid og rum. Flora og Fauna 121, 133–141.
Soares PO, Crespi AL, Rodrigues MC, Arnaldo PS. 2012. The habitat vegetational structure and the success of the blue alcon, Maculinea alcon (Denis & Schiffermuller). Plant Biosystems 146, 1–6. (10.1080/11263504.2011.558671) DOI
Sielezniew M, Stankiewicz-Fiedurek AM. 2013. Behavioural evidence for a putative oviposition-deterring pheromone in the butterfly, Phengaris (Maculinea) teleius (Lepidoptera: Lycaenidae). Eur. J. Entomol. 110, 71–80. (10.14411/eje.2013.009) DOI
Chao A. 1984. Nonparametric-estimation of the number of classes in a population. Scand. J. Stat. 11, 265–270.
Oksanen J, et al. 2018. vegan: Community Ecology Package. R package version 2.5–2 https://CRAN.R-project.org/package=vegan.
Thomas JA, Schönrogge K, Elmes GW. 2005. Specializations and host associations of social parasites of ants. In Insect evolutionary ecology: proceedings of the royal entomological society's 22nd symposium (eds Fellowes MDE, Holloway GJ, Rolff J), pp. 479–518. London, UK: Royal Entomological Society.
Larsson J.2018. eulerr: Area-Proportional Euler and Venn Diagrams with Ellipses. R package version 4.1.0. https://cran.r-project.org/package=eulerr .
Meirmans PG, Van Tienderen PH. 2004. GenoType and GenoDive: two programs for the analysis of genetic diversity of asexual organisms. Mol. Ecol. Notes 4, 792–794. (10.1111/j.1471-8286.2004.00770.x) DOI
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. Insect Soc. 55, 370–381. (10.1007/s00040-008-1015-4) DOI
Helmus MR, Bland TJ, Williams CK, Ives AR. 2007. Phylogenetic measures of biodiversity. Am. Nat. 169, E68–E83. (10.1086/511334) PubMed DOI
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO. 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463–1464. (10.1093/bioinformatics/btq166) PubMed DOI
Jansen G, Vepsäläinen K, Savolainen R. 2011. A phylogenetic test of the parasite–host associations between Maculinea butterflies (Lepidoptera: Lycaenidae) and Myrmica ants (Hymenoptera: Formicidae). Eur. J. Entomol. 108, 53–62. (10.14411/eje.2011.007) DOI
Ebsen JR, Boomsma JJ, Nash DR. Submitted. Phylogeography and cryptic speciation in the Myrmica scabrinodis (Nylander, 1846) species complex (Hymenoptera: Formicidae), and their conservation implications. Insect Conserv. Diver.
Jansen G, Savolainen R, Vepsalainen K. 2010. Phylogeny, divergence-time estimation, biogeography and social parasite–host relationships of the Holarctic ant genus Myrmica (Hymenoptera: Formicidae). Mol. Phylogenet. Evol. 56, 294–304. (10.1016/j.ympev.2010.01.029) PubMed DOI
Cushman JH, Lawton JH, Manly BF. 1993. Latitudinal patterns in European ant assemblages: variation in species richness and body size. Oecologia 95, 30–37. (10.1007/BF00649503) PubMed DOI
Witek M, Sliwinska EB, Skorka P, Nowicki P, Wantuch M, Vrabec V, Settele J, Woyciechowski M. 2008. Host ant specificity of large blue butterflies Phengaris (Maculinea) (Lepidoptera: Lycaenidae) inhabiting humid grasslands in East-central Europe. Eur. J. Entomol. 105, 871–877. (10.14411/eje.2008.115) DOI
Sielezniew M, Bystrowski C, Deoniziak K, Da Costa JM. 2015. An unexpected record of Myrmica schencki EMERY, 1895 as a secondary host ant of the hygrophilous form of a small and isolated population of the Alcon Blue butterfly Phengaris (=Maculinea) alcon (DENIS et SCHIFFERMÜLLER, 1775) (Lepidoptera, Lycaenidae) in NE Poland. Pol. J. Entomol. 84, 49–59. (10.1515/pjen-2015-0005) DOI
Jutzeler D. 1988. Fund von Maculinea rebeli (Hirschke, 1904) im Glarnerland (Lepidoptera, Lycaenidae). Mitt Entomol. Gesell Basel 384, 124–125.
Jutzeler D. 1989. Maculinea rebeli (HIRSCHKE): Ein Raupenfund im Glarnerland (Lepidoptera: Lycaenidae). Mitt Entomol. Gesell Basel 39, 92–93.
Sielezniew M, Rutkowski R. 2012. Population isolation rather than ecological variation explains the genetic structure of endangered myrmecophilous butterfly Phengaris (=Maculinea) arion. J. Insect Conserv. 16, 39–50. (10.1007/s10841-011-9392-9) DOI
Sielezniew M, Dziekańska I, Stankiewicz-Fiedurek AM. 2010a. Multiple host-ant use by the predatory social parasite Phengaris (=Maculinea) arion (Lepidoptera, Lycaenidae). J. Insect Conserv. 14, 141–149. (10.1007/s10841-009-9235-0) DOI
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. (10.2307/5555) DOI
Thomas JA, Elmes GW, Clarke RT, Kim KG, Munguira ML, Hochberg ME. 1997. Field evidence and model predictions of butterfly-mediated apparent competition between gentian plants and red ants. Acta Oecol. 18, 671–684. (10.1016/S1146-609x(97)80050-1) DOI
Ebsen JR, Nash DR, Boomsma JJ. 2005. Cryptic Myrmica species among the hosts of Maculinea butterflies. In Studies on the ecology and conservation of butterflies in Europe - Vol. 2: species ecology along a European gradient: Maculinea butterflies as a model (eds Settele J, Thomas J, Kühn E), p. 171 Sofia, Bulgaria: Pensoft.
de Assis RA, dos Santos Cecconello M, Casacci LP, Barbero F, de Assis LM, Venturino E, Bonelli S. 2018. A theory and a mathematical model for the evolution of single and multiple host behavior in a parasite-host system (Maculinea-Myrmica). Ecol. Complex 34, 178–187. (10.1016/j.ecocom.2017.11.007) DOI
Guillem RM, Drijfhout FP, Martin SJ. 2016. Species-specific cuticular hydrocarbon stability within European Myrmica ants. J. Chem. Ecol. 42, 1052–1062. (10.1007/s10886-016-0784-x) PubMed DOI PMC
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. (10.1046/j.1365-2311.2002.00427.x) DOI
van Wilgenburg E, Symonds MRE, Elgar MA. 2011. Evolution of cuticular hydrocarbon diversity in ants. J. Evol. Biol. 24, 1188–1198. (10.1111/j.1420-9101.2011.02248.x) PubMed DOI
Oldham NJ, Morgan ED, Agosti D, Wehner R. 1999. Species recognition from postpharyngeal gland contents of ants of the Cataglyphis bicolor group. J. Chem. Ecol. 25, 1383–1393. (10.1023/A:1020935011325) PubMed DOI
Beibl J, D'Ettorre P, Heinze J. 2007. Cuticular profiles and mating preference in a slave-making ant. Insect Soc. 54, 174–182. (10.1007/s00040-007-0929-6) DOI
Oppelt A, Spitzenpfeil N, Kroiss J, Heinze J. 2008. The significance of intercolonial variation of cuticular hydrocarbons for inbreeding avoidance in ant sexuals. Anim. Behav. 76, 1029–1034. (10.1016/j.anbehav.2008.05.020) DOI
Nowicki P, Vrabec V. 2011. Evidence for positive density-dependent emigration in butterfly metapopulations. Oecologia 167, 657–665. (10.1007/s00442-011-2025-x) PubMed DOI PMC
Bonelli S, Vrabec V, Witek M, Barbero F, Patricelli D, Nowicki P. 2013. Selection on dispersal in isolated butterfly metapopulations. Popul. Ecol. 55, 469–478. (10.1007/s10144-013-0377-2) DOI
Timuş N, Craioveanu C, Sitaru C, Rus A, Rákosy L. 2013. Differences in adult phenology, demography, mobility and distribution in two syntopic ecotypes of Maculinea alcon (cruciata vs. pneumonanthe) (Lepidoptera: Lycaenidae) from Transilvania (Romania). Entomol. Romanica 18, 21–30.
Kőrösi Á, Örvössy N, Batáry P, Kover S, Peregovits L. 2008. Restricted within-habitat movement and time-constrained egg laying of female Maculinea rebeli butterflies. Oecologia 156, 455–464. (10.1007/s00442-008-0986-1) PubMed DOI
Sielezniew M, Patricelli D, Rutkowski R, Witek M, Bonelli S, Bus MM. 2015. Population genetics of the endangered obligatorily myrmecophilous butterfly Phengaris (=Maculinea) arion in two areas of its European range. Insect Conserv. Diver. 8, 505–516. (10.1111/icad.12129) DOI
Andersen A, Simcox DJ, Thomas JA, Nash DR. 2014. Assessing reintroduction schemes by comparing genetic diversity of reintroduced and source populations: a case study of the globally threatened large blue butterfly (Maculinea arion). Biol. Conserv. 175, 34–41. (10.1016/j.biocon.2014.04.009) DOI
Ugelvig LV, Andersen A, Boomsma JJ, Nash DR. 2012. Dispersal and gene flow in the rare, parasitic Large Blue butterfly Maculinea arion. Mol. Ecol. 21, 3224–3236. (10.1111/j.1365-294X.2012.05592.x) PubMed DOI
Vanden Broeck A, Maes D, Kelager A, Wynhoff I, WallisDeVries MF, Nash DR, Oostermeijer JGB, Van Dyck H, Mergeay J. 2017. Gene flow and effective population sizes of the butterfly Maculinea alcon in a highly fragmented, anthropogenic landscape. Biol. Conserv. 209, 89–97. (10.1016/j.biocon.2017.02.001) DOI
Witek M, et al. 2013. Interspecific relationships in co-occurring populations of social parasites and their host ants. Biol. J. Linn Soc. 109, 699–709. (10.1111/bij.12074) DOI
Nuismer SL, Thompson JN. 2006. Coevolutionary alternation in antagonistic interactions. Evolution 60, 2207–2217. (10.1111/j.0014-3820.2006.tb01858.x) PubMed DOI
Feeney WE, Welbergen JA, Langmore NE. 2014. Advances in the study of coevolution between avian brood parasites and their hosts. Annu. Rev. Ecol. Evol. Syst. 45, 227–246. (10.1146/annurev-ecolsys-120213-091603) DOI
Moksnes A, Fossøy F, Røskaft E, Stokke BG. 2013. Reviewing 30 years of studies on the Common Cuckoo: accumulated knowledge and future perspectives. Chinese Birds 4, 3–14. (10.5122/cbirds.2013.0001) DOI
Soler JJ, Møller AP, Soler M. 1999. A comparative study of host selection in the European cuckoo Cuculus canorus. Oecologia 118, 265–276. (10.1007/s004420050727) PubMed DOI
Alvarez F. 2003. Parasitism rate by the common cuckoo Cuculus canorus increases with high density of host's breeding pairs. Ornis Fennica 80, 193–196.
Lindholm AK. 1999. Brood parasitism by the cuckoo on patchy reed warbler populations in Britain. J. Anim. Ecol. 68, 293–309. (10.1046/j.1365-2656.1999.00286.x) DOI
Stokke BG, et al. 2007. Host density predicts presence of cuckoo parasitism in reed warblers. Oikos 116, 913–922. (10.1111/j.2007.0030-1299.15832.x) DOI
Avilés JM, et al. 2011. The common cuckoo Cuculus canorus is not locally adapted to its reed warbler Acrocephalus scirpaceus host. J. Evol. Biol. 24, 314–325. (10.1111/j.1420-9101.2010.02168.x) PubMed DOI
Kleven O, Moksnes A, Røskaft E, Rudolfsen G, Stokke BG, Honza M. 2004. Breeding success of common cuckoos Cuculus canorus parasitising four sympatric species of Acrocephalus warblers. J. Avian Biol. 35, 394–398. (10.1111/j.0908-8857.2004.03359.x) DOI
Abernathy VE, Langmore NE. 2017. Factors affecting the rates of coevolution between obligate avian brood parasites and their hosts. In Avian brood parasitism: fascinating life sciences (ed. Soler M.), pp. 23–41. Cham, Switzerland: Springer International Publishing.
Gibbs HL, Sorenson MD, Marchetti K, Brooke MD, Davies NB, Nakamura H. 2000. Genetic evidence for female host-specific races of the common cuckoo. Nature 407, 183 (10.1038/35025058) PubMed DOI
Antonov A, Stokke BG, Vikan JR, Fossøy F, Ranke PS, Røskaft E, Moksnes A, Møller AP, Shykoff JA. 2010. Egg phenotype differentiation in sympatric cuckoo Cuculus canorus gentes. J. Evol. Biol. 23, 1170–1182. (10.1111/j.1420-9101.2010.01982.x) PubMed DOI
Gadeberg RME, Boomsma JJ. 1997. Genetic population structure of the large blue butterfly Maculinea alcon in Denmark. J. Insect Conserv. 1, 99–111. (10.1023/A:1018439211244) DOI
Pierce NE. 1995. Predatory and parasitic Lepidoptera: carnivores living on plants. J. Lepid Soc. 49, 412–453.
Pierce NE, Braby MF, Heath A, Lohman DJ, Mathew J, Rand DB, Travassos MA. 2002. The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annu. Rev. Entomol. 47, 733–771. (10.1146/annurev.ento.47.091201.145257) PubMed DOI
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