Skip to main content

Advertisement

SpringerLink
Log in

Ecological divergence of Chaetopteryx rugulosa species complex (Insecta, Trichoptera) linked to climatic niche diversification

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Climate is often considered to be an important, but indirect driver of speciation. Indeed, environmental factors may contribute to the formation of biodiversity, but to date this crucial relationship remains largely unexplored. Here we investigate the possible role of climate, geological factors, and biogeographical processes in the formation of a freshwater insect species group, the Chaetopteryx rugulosa species complex (Trichoptera) in the Western Balkans. We used multi-locus DNA sequence data to establish a dated phylogenetic hypothesis for the group. The comparison of the dated phylogeny with the geological history of the Western Balkans shows that lineage formation coincided with major past Earth surface and climatic events in the region. By reconstructing present-day habitat conditions (climate, bedrock geology), we show that the lineages of C. rugulosa species complex have distinct climatic but not bedrock geological niches. Without exception, all splits associated with Pliocene/Pleistocene transition led to independent, parallel split into ‘warm’ and ‘cold’ sister lineages. This indicates a non-random diversification on the C. rugulosa species complex associated with late Pliocene climate in the region. We interpreted the results as the diversification of the species complex were mainly driven by ecological diversification linked to past climate change, along with geographical isolation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • April, J., R. H. Hanner, A.-M. Dion-Côté & L. Bernatchez, 2013. Glacial cycles as an allopatric speciation pump in north-eastern American freshwater fishes. Molecular Ecology 22: 409–422.

    Article  CAS  PubMed  Google Scholar 

  • Bada, G., F. Horváth, S. Cloetingh, D. D. Coblentz & T. Tóth, 2001. Role of topography-induced gravitational stresses in basin inversion: the case study of the Pannonian basin. Tectonics 20: 343–363.

    Article  Google Scholar 

  • Bálint, M., S. Domisch, C. H. M. Engelhardt, P. Haase, S. Lehrian, J. Sauer, K. Theissinger, S. U. Pauls & C. Nowak, 2011. Cryptic biodiversity loss linked to global climate change. Nature Climate Change 1: 313–318.

    Article  Google Scholar 

  • Bănărescu, P. M., 2004. Distribution pattern of the aquatic fauna of the Balkan Peninsula. In Griffiths, H. I., B. Kryštufek & J. M. Reed (eds), Balkan Biodiversity. Springer, Netherlands: 203–217.

    Chapter  Google Scholar 

  • Bilandžija, H., B. Morton, M. Podnar & H. Ćetković, 2013. Evolutionary history of relict Congeria (Bivalvia: Dreissenidae): unearthing the subterranean biodiversity of the Dinaric Karst. Frontiers in Zoology 10: 5.

    Article  PubMed  PubMed Central  Google Scholar 

  • Blomberg, S. P. & T. Garland, 2002. Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods. Journal of Evolutionary Biology 15: 899–910.

    Article  Google Scholar 

  • Blomberg, S. P., T. Garland & A. R. Ives, 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57: 717–745.

    Article  PubMed  Google Scholar 

  • Bouckaert, R. R., 2010. DensiTree: making sense of sets of phylogenetic trees. Bioinformatics 26: 1372–1373.

    Article  CAS  PubMed  Google Scholar 

  • Brower, A. V., 1994. Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proceedings of the National Academy of Sciences of the United States of America 91: 6491–6495.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buckley, T. R., P. Arensburger, C. Simon & G. K. Chambers, 2002. Combined data, Bayesian phylogenetics, and the origin of the New Zealand cicada genera. Systematic Biology 51: 4–18.

    Article  PubMed  Google Scholar 

  • Burbank, D. W. & R. S. Anderson, 2012. Tectonic Geomorphology. Wiley, Chichester.

    Google Scholar 

  • Csontos, L., L. Benkovics, F. Bergerat, J.-L. Mansy & G. Wórum, 2002a. Tertiary deformation history from seismic section study and fault analysis in a former European Tethyan margin (the Mecsek–Villány area, SW Hungary). Tectonophysics 357: 81–102.

    Article  Google Scholar 

  • Csontos, L., E. Márton, G. Wórum & L. Benkovics, 2002b. Geodynamics of SW-Pannonian inselbergs (Mecsek and Villány Mts, SW Hungary): inferences from a complex structural analysis. Stephan Mueller Special Publication Series 3: 227–245.

    Article  Google Scholar 

  • deWaard, J. R., N. V. Ivanova, M. Hajibabaei & P. D. Hebert, 2008. Assembling DNA barcodes. Analytical protocols. Methods in Molecular Biology 410: 275–293.

    Article  CAS  PubMed  Google Scholar 

  • Dijkstra, K.-D. B., M. T. Monaghan & S. U. Pauls, 2014. Freshwater biodiversity and insect diversification. Annual Review of Entomology 59: 143–163.

    Article  CAS  PubMed  Google Scholar 

  • Dormann, C. F., B. Gruber, M. Winter & D. Herrmann, 2010. Evolution of climate niches in European mammals? Biology Letters 6: 229–232.

    Article  PubMed  Google Scholar 

  • Dormann, C. F., J. Elith, S. Bacher, C. Buchmann, G. Carl, G. Carré, J. R. García Marquéz, B. Gruber, B. Lafourcade, P. J. Leitão, T. Münkemüller, C. McClean, P. E. Osborne, B. Reineking, B. Schröder, A. K. Skidmore, D. Zurell & S. Lautenbach, 2013. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36: 27–46.

    Article  Google Scholar 

  • Drummond, A. J., S. Y. W. Ho, M. J. Phillips & A. Rambaut, 2006. Relaxed phylogenetics and dating with confidence. PLoS Biology 4: e88.

    Article  PubMed  PubMed Central  Google Scholar 

  • Drummond, A. J., B. Ashton, S. Buxton, M. Cheung, A. Cooper, C. Duran, M. Field, J. Heled, M. Kearse, S. Markowitz, R. Moir, S. Stones-Havas, S. Sturrock, T. Thierer & A. Wilson, 2011. Geneious v5.4 [available on internet at http://www.geneious.com/].

  • Elmer, K. R., T. K. Lehtonen, A. F. Kautt, C. Harrod & A. Meyer, 2010a. Rapid sympatric ecological ifferentiation of crater lake cichlid fishes within historic times. BMC Biology 8: 60.

    Article  PubMed  PubMed Central  Google Scholar 

  • Elmer, K. R., H. Kusche, T. Lehtonen & A. Meyer, 2010b. Local variation and parallel evolution: morphological and genetic diversity across a species complex of neotropical crater lake cichlid fishes. Philosophical Transactions of the Royal Society B 365: 1763–1782.

    Article  Google Scholar 

  • Espeland, M. & K. A. Johanson, 2010. The effect of environmental diversification on species diversification in New Caledonian caddisflies (Insecta: Trichoptera: Hydropsychidae). Journal of Biogeography 37: 879–890.

    Article  Google Scholar 

  • Espeland, M., K. A. Johanson & R. Hovmöller, 2008. Early Xanthochorema (Trichoptera, Insecta) radiations in New Caledonia originated on ultrabasic rocks. Molecular Phylogenetics and Evolution 48: 904–917.

    Article  CAS  PubMed  Google Scholar 

  • Evans, M. E. K., S. A. Smith, R. S. Flynn, J. Michael & M. J. Donoghue, 2009. Niche evolution, and diversification of the “bird-cage” evening primroses (Oenothera, sections Anogra and Kleinia). The American Naturalist 173: 225–240.

    Article  PubMed  Google Scholar 

  • Feder, J. L., 1998. The apple maggot fly, Rhagoletis pomonella: flies in the face of conventional wisdom about speciation? In Howard, D. & S. Berlocher (eds), Endless Forms: Species and Speciation. Oxford University Press, Oxford: 130–144.

    Google Scholar 

  • Ferreira, M. A. R. & M. A. Suchard, 2008. Bayesian analysis of elapsed times in continuous-time Markov chains. Canadian Journal of Statistics 36: 355–368.

    Article  Google Scholar 

  • Fisher, R. A., 1936. The use of multiple measurements in taxonomic problems. Annals of Eugenics 7: 179–188.

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Funk, D. J., P. Nosil & W. J. Etges, 2006. Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. Proceedings of the National Academy of Sciences of the United States of America 103: 3209–3213.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gómez, A. & D. Lunt, 2007. Refugia within refugia: patterns of phylogeographic concordance in the Iberian Peninsula. In Weiss, F. (ed.), Phylogeography of Southern European Refugia. Springer, Netherlands: 155–188.

    Chapter  Google Scholar 

  • Graham, C. H., S. R. Ron, J. C. Santos, C. J. Schneider & C. Moritz, 2004. Integrating phylogenetics and environmental niche models to explore speciation mechanisms in dendrobatid frogs. Evolution 58: 1781–1793.

    Article  PubMed  Google Scholar 

  • Griffiths, H. I., B. Krystufek & J. M. Reed (eds), 2004. Balkan Biodiversity: Pattern and Process in the European Hotspot. Springer, Netherlands.

    Google Scholar 

  • Hajibabaei, M., J. R. deWaard, N. V. Ivanova, S. Ratnasingham, R. T. Dooh, S. L. Kirk, P. M. Mackie & P. D. Hebert, 2005. Critical factors for assembling a high volume of DNA barcodes. Philosophical Transactions of the Royal Society of London B 360: 1959–1967.

    Article  CAS  Google Scholar 

  • Harzhauser, M., O. Mandic, T. A. Neubauer, E. Georgopoulou & A. Hassler, 2015. Disjunct distribution of the Miocene limpet-like freshwater gastropod genus Delminiella. Journal of Molluscan Studies 1: 8.

    Google Scholar 

  • Hebert, P. D. N., E. H. Penton, J. M. Burns, D. H. Janzen & W. Hallwachs, 2004. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America 101: 14812–14817.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heled, J. & A. J. Drummond, 2010. Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution 27: 570–580.

    Article  CAS  PubMed  Google Scholar 

  • Hewitt, G. M., 2000. The genetic legacy of the Quaternary ice ages. Nature 405: 907–913.

    Article  CAS  PubMed  Google Scholar 

  • Hewitt, G. M., 2011. Mediterranean Peninsulas: the evolution of hotspots. In Zachos, F. E. & J. C. Habel (eds), Biodiversity Hotspots. Springer, Berlin: 123–147.

    Chapter  Google Scholar 

  • Hijmans, R. J., S. E. Cameron, J. L. Parra, P. G. Jones & A. Jarvis, 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: 1965–1978.

    Article  Google Scholar 

  • Hijmans, R. J., S. Phillips, J. Leathwick & J. Elith, 2012. dismo: species distribution modeling. R package version 0.7–17 [available on internet at http://CRAN.R-project.org/package=dismo].

  • Hoffmann, A. A. & C. M. Sgro, 2011. Climate change and evolutionary adaptation. Nature 470: 479–485.

    Article  CAS  PubMed  Google Scholar 

  • Horváth, F. & S. Cloetingh, 1996. Stress-induced late-stage subsidence anomalies in the Pannonian basin. Tectonophysics 266: 287–300.

    Article  Google Scholar 

  • Huang, Y., X. Guo, S. Y. W. Ho, H. Shi, J. Li, J. Li, B. Cai & Y. Wang, 2013. Diversification and demography of the oriental garden lizard (Calotes versicolor) on Hainan Island and the adjacent mainland. PLoS ONE 8: e64754.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ivanova, N. V., J. R. Dewaard & P. D. N. Hebert, 2006. An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes 6: 998–1002.

    Article  CAS  Google Scholar 

  • Kalkvik, H. M., I. J. Stout, T. J. Doonan & C. L. Parkinson, 2012. Investigating niche and lineage diversification in widely distributed taxa: phylogeography and ecological niche modeling of the Peromyscus maniculatus species group. Ecography 35: 54–64.

    Article  Google Scholar 

  • Kautt, A. F., K. R. Elmer & A. Meyer, 2012. Genomic signatures of divergent selection and speciation patterns in a ‘natural experiment’, the young parallel radiations of Nicaraguan crater lake cichlid fishes. Molecular Ecology 21: 4770–4786.

    Article  PubMed  Google Scholar 

  • Keitt, T. H., R. Bivand, E. Pebesma & B. Rowlingson, 2010. rgdal: bindings for the geospatial data abstraction library [available on internet at http://CRAN.R-project.org/package=rgdal].

  • Kembel, S. W., P. D. Cowan, M. R. Helmus, W. K. Cornwell, H. Morlon, D. D. Ackerly, S. P. Blomberg & C. O. Webb, 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26: 1463–1464.

    Article  CAS  PubMed  Google Scholar 

  • Kováč, M., A. Andreyeva-Grigorovich, Z. Bajraktarević, R. Brzobohatý, S. Filipescu, L. Fodor, M. Fodor, A. Nagymarosy, N. Oszczypko, D. Pavelić, F. Rögl, B. Saftić, L. Sliva & B. Studencka, 2007. Badenian evolution of the Central Paratethys Sea: paleogeography, climate and eustatic sea-level changes. Geologica Carpathica 58: 579–606.

    Google Scholar 

  • Kučinić, M., I. Szivák, S. U. Pauls, M. Bálint, A. Delić & I. Vučković, 2013. Chaetopteryx bucari sp. n., a new species from the Chaetopteryx rugulosa group from Croatia (Insecta, Trichoptera, Limnephilidae) with molecular, taxonomic and ecological notes on the group. ZooKeys 320: 1–28.

    Article  Google Scholar 

  • Lehrian, S., M. Bálint, P. Haase & S. U. Pauls, 2010. Genetic population structure of an autumn emerging caddisfly with inherently low dispersal capacity and insights into its phylogeography. Journal of the North American Benthological Society 29: 1100–1118.

    Article  Google Scholar 

  • Legendre, P. & L. Legendre, 2012. Numerical Ecology, 3rd ed. Elsevier, Amsterdam.

    Google Scholar 

  • Levsen, N. D., P. Tiffin & M. S. Olson, 2012. Pleistocene speciation in the genus Populus (Salicaceae). Systematic Biology 61: 401–412.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lisiecki, L. E. & M. E. Raymo, 2005. A Pliocene–Pleistocene stack of 57 globally distributed benthic δ18O records. Paleoceanography 20: 1.

    Google Scholar 

  • Magyar, I., D. H. Geary & P. Müller, 1999. Paleogeographic evolution of the late Miocene Lake Pannon in Central Europe. Palaeogeography, Palaeoclimatology, Palaeoecology 147: 151–167.

    Article  Google Scholar 

  • Malicky, H., 1983. Chorological patterns and biome types of European Trichoptera and other freshwater insects. Archiv für Hydrobiologie 96: 223–244.

    Google Scholar 

  • Malicky, H., 1996. Das problem der allopatrischen arten bei europäischen köcherfliegen (Insecta: Trichoptera). Natura Croatica 5: 11–23.

    Google Scholar 

  • Malicky, H., 2004. Atlas of European Trichoptera. Springer, Dordrecht.

    Google Scholar 

  • Malicky, H., 2014. Comments on two recently published papers on Cheumatopsyche (Hydropsychidae) and Chaetopteryx (Limnephilidae). Baueria 41: 51–53.

    Google Scholar 

  • Malicky, H., 2016. Die mitteleuropäische Verbreitung zweirer Morphotypen von Allogamus auricollis (Trichoptera, Limnephilidae) mit phänologischen und bionomischen Notizen. Braueria 43: 29–38.

    Google Scholar 

  • Malicky, H. & S. U. Pauls, 2012. Cross-breeding of Chaetopteryx morettii and related species, with molecular and eidonomical results (Trichoptera, Limnephilidae). Annales de Limnologie 48: 13–19.

    Article  Google Scholar 

  • Malicky, H., C. Krusnik, G. Moretti & S. Nógrádi, 1986. Ein beitrag zur kenntnis der Chaetopteryx rugulosa Kolenati, 1848,—Gruppe (Trichoptera, Limnephilidae). Entomofauna 7: 1–27.

    Google Scholar 

  • Mandic, O., A. de Leeuw, J. Bulić, K. F. Kuiper, W. Krijgsman & Z. Jurišić-Polšak, 2012. Paleogeographic evolution of the Southern Pannonian Basin: 40Ar/39Ar age constraints on the Miocene continental series of Northern Croatia. International Journal of Earth Sciences 101: 1033–1046.

    Article  CAS  Google Scholar 

  • McKinnon, J. S., S. Mori, B. K. Blackman, L. David, D. M. Kingsley, L. Jamieson, J. Chou & D. Schluter, 2004. Evidence for ecology’s role in speciation. Nature 429: 294–298.

    Article  CAS  PubMed  Google Scholar 

  • McPeek, M. A. & G. A. Wellborn, 1998. Genetic variation and reproductive isolation among phenotypically divergent amphipod populations. Limnology and Oceanography 43: 1162–1169.

    Article  Google Scholar 

  • Mikes, T., M. Báldi-Beke, M. Kázmér, I. Dunkl & H. von Eynatten, 2008. Calcareous nannofossil age constraints on Miocene flysch sedimentation in the Outer Dinarides (Slovenia, Croatia, Bosnia-Herzegovina and Montenegro). Geological Society, London, Special Publications 298: 335–363.

    Article  Google Scholar 

  • Múrria, C., N. Bonada, M. A. Arnedo, C. Zamora-Muñoz, N. Prat & A. P. Vogler, 2012. Phylogenetic and ecological structure of Mediterranean caddisfly communities at various spatio-temporal scales. Journal of Biogeography 39: 1621–1632.

    Article  Google Scholar 

  • Nosil, P., 2012. Ecological Speciation. Oxford University Press, Oxford.

    Book  Google Scholar 

  • Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, R. B. O’Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens & H. Wagner, 2013. vegan: community ecology package [available on internet at http://CRAN.R-project.org/package=vegan].

  • Oláh, J. & T. Kovács, 2013. New species and new records of Balkan Trichoptera II. Folia Historico Naturalia Musei Matraensis 37: 109–121.

    Google Scholar 

  • Oláh, J., T. Kovács, I. Sivec, I. Szivák & G. Urbanic, 2012. Seven new species in the Chaetopteryx rugulosa species group: applying the phylogenetic species concept and the sexual selection theory (Trichoptera: Limnephilidae). Folia Historico Naturalia Musei Matraensis 36: 51–79.

    Google Scholar 

  • Oppold, A.-M., J. A. M. Pedrosa, M. Balint, J. B. Diogo, J. Ilkova, J. L. T. Pestana & M. Pfenninger, 2016. Support for the evolutionary speed hypothesis from intraspecific population genetic data in the non-biting midge Chironomus riparius. Proceedings of the Royal Society B 283: 20152413.

    Article  PubMed  PubMed Central  Google Scholar 

  • Papadopoulou, A., I. Anastasiou & A. P. Vogler, 2010. Revisiting the insect mitochondrial molecular clock: the mid-aegean trench calibration. Molecular Biology and Evolution 27: 1659–1672.

    Article  CAS  PubMed  Google Scholar 

  • Pauls, S. U., W. Graf, P. Haase, H. T. Lumbsch & J. Waringer, 2008. Grazers, shredders and filtering carnivores—the evolution of feeding ecology in Drusinae (Trichoptera: Limnephilidae): insights from a molecular phylogeny. Molecular Phylogenetics and Evolution 46: 776–791.

    Article  CAS  PubMed  Google Scholar 

  • Pauls, S. U., C. Nowak, M. Bálint & M. Pfenninger, 2013. The impact of global climate change on genetic diversity within populations and species. Molecular Ecology 22: 925–946.

    Article  PubMed  Google Scholar 

  • Pauls, S. U., M. Apl, M. Bálint, P. Bernabò, F. Čiampor Jr., Z. Čiamporová-Zaťovičová, D. S. Finn, J. Kohout, F. Leese, V. Lencioni, I. Paz-Vinas & M. T. Monagham, 2014. Integrating molecular tools into freshwater ecology: developments and opportunities. Freshwater Biology 59: 1559–1576.

    Article  Google Scholar 

  • Posada, D. & K. A. Crandall, 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818.

    Article  CAS  PubMed  Google Scholar 

  • Previšić, A., C. Walton, M. Kucinić, P. T. Mitrikeski & M. Kerovec, 2009. Pleistocene divergence of Dinaric Drusus endemics (Trichoptera, Limnephilidae) in multiple microrefugia within the Balkan Peninsula. Molecular Ecology 18: 634–647.

    Article  PubMed  Google Scholar 

  • Previšić, A., W. Graf, S. Vitecek, M. Kučinić, M. Bálint, L. Keresztes, S. U. Pauls & J. Waringer, 2014a. Cryptic diversity of caddisflies in the Balkans: the curious case of Ecclisopteryx species (Trichoptera: Limnephilidae). Arthropod Systematics & Phylogeny 72: 309–329.

    Google Scholar 

  • Previšić, A., J. Schnitzler, M. Kučinić, W. Graf, H. Ibrahimi, M. Kerovec & S. U. Pauls, 2014b. Micro-scale vicariance and diversification of Western Balkan caddisflies linked to karstification. Freshwater Science 33: 250–262.

    Article  PubMed  Google Scholar 

  • Previšić, A., A. Gelemanović, G. Urbanič & I. Ternjej, 2016. Cryptic diversity in the Western Balkan endemic copepod: four species in one? Molecular Phylogenetics and Evolution 100: 124–134.

    Article  PubMed  Google Scholar 

  • R Core Team, 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing.Vienna, Austria [available on internet at http://www.R-project.org/].

  • Rambaut, A. & A. J. Drummond, 2009. Tracer v1.5 [available on internet at http://beast.bio.ed.ac.uk/Tracer].

  • Ratnasingham, S. & P. D. N. Hebert, 2007. BOLD: the barcode of life data system. Molecular Ecology Notes 7: 355–364 [available on internet at http://www.barcodinglife.org].

  • Rissler, L. J. & J. J. Apodaca, 2007. Adding more ecology into species delimitation: ecological niche models and phylogeography help define cryptic species in the black salamander (Aneides flavipunctatus). Systematic Biology 56: 924–942.

    Article  PubMed  Google Scholar 

  • Ronquist, F., M. Teslenko, P. van der Mark, D. L. Ayres, A. Darling, S. Höhna, B. Larget, L. Liu, M. A. Suchard & J. P. Huelsenbeck, 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rundle, H. D. & P. Nosil, 2005. Ecological speciation. Ecology Letters 8: 336–352.

    Article  Google Scholar 

  • Rundle, H. D., L. Nagel, J. Wenrick Boughman & D. Schluter, 2000. Natural selection and parallel speciation in sympatric sticklebacks. Science 287: 306–308.

    Article  CAS  PubMed  Google Scholar 

  • Schluter, D., 2001. Ecology and the origin of species. Trends in Ecology & Evolution 16: 372–380.

    Article  CAS  Google Scholar 

  • Schluter, D., 2009. Evidence for ecological speciation and its alternative. Science 323: 737–741.

    Article  CAS  PubMed  Google Scholar 

  • Sebe, K., G. Csillag & G. Konrád, 2008. The role of neotectonics in fluvial landscape development in the Western Mecsek Mountains and related foreland basins (SE Transdanubia, Hungary). Geomorphology 102: 55–67.

    Article  Google Scholar 

  • Sotiropoulos, K., K. Eleftherakos, G. Dzukic, M. Kalezic, A. Legakis & R. Polymeni, 2007. Phylogeny and biogeography of the alpine newt Mesotriton alpestris (Salamandridae, Caudata), inferred from mtDNA sequences. Molecular Phylogenetics and Evolution 45: 211–226.

    Article  CAS  PubMed  Google Scholar 

  • Statzner, B. & S. Dolédec, 2011. Phylogenetic, spatial, and species-traits patterns across environmental gradients: the case of Hydropsyche (Trichoptera) along the Loire River. International Review of Hydrobiology 96: 121–140.

    Article  Google Scholar 

  • Ustaszewski, K., S. M. Schmid, B. Fügenschuh, M. Tischler, E. Kissling & W. Spakman, 2008. A map-view restoration of the Alpine–Carpathian–Dinaridic system for the Early Miocene. Swiss Journal of Geosciences 101: 273–294.

    Article  Google Scholar 

  • Venables, W. N. & B. D. Ripley, 2002. Modern Applied Statistics with S. Springer, New York.

    Book  Google Scholar 

  • Vitecek, S., M. Kučinić, J. Oláh, A. Previšić, M. Bálint, L. Keresztes, J. Waringer, S. U. Pauls & W. Graf, 2015. Description of two new filtering carnivore Drusus species (Limnephilidae, Drusinae) from the Western Balkans. Zookeys 513: 79–104.

    Article  Google Scholar 

  • Xie, W., P. O. Lewis, Y. Fan, L. Kuo & M. H. Chen, 2011. Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Systematic Biology 60: 150–160.

    Article  PubMed  Google Scholar 

  • Zhang, Y., C. Chen, L. Li, C. Zhao, W. Chen & Y. Huang, 2014. Insights from ecological niche modelling on the taxonomic distinction and niche differentiation between the black-spotted and red-spotted tokay geckoes (Gekko gecko). Ecology and Evolution 4: 3383–3394.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful to János Oláh, Hans Malicky, Ákos Uherkovich, Sára Nógrádi, Ana Previšić, Gorazd Urbanic, Marco Valle, Omar Lodovici, Antun Delić, Iva Mihoci, Aleksandar Popijač, and Matija Bučar who provided us with valuable specimens, location data, and general advice. We express our gratitude to Xin Zhou for handling the mitochondrial barcoding of our specimens within the Barcoding of Life initiative. I Sz was partially funded through an incoming research grant of the Biodiversity and Climate Research Centre in the frame of the research funding program Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz (LOEWE) of Hesse’s Ministry of Higher Education, Research, and the Arts. MB and SP are funded by the research funding program Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz (LOEWE) of Hesse’s Ministry of Higher Education, Research, and the Arts, as well as the Fonds zur Förderung der wissenschaftlichen Forschung (FWF) Grant P 23687-B17.

Author information

Author notes

    Authors and Affiliations

    1. Balaton Limnological Institute, MTA Centre for Ecological Research, Klebelsberg Kuno u. 3, 8237, Tihany, Hungary

      Ildikó Szivák

    2. Senckenberg Biodiversity and Climate Research Centre, Senckenberganlage 25, 60325, Frankfurt am Main, Germany

      Tamás Mikes, Steffen U. Pauls & Miklós Bálint

    3. Verven 38, 4014, Stavanger, Norway

      Tamás Mikes

    4. Life and Brain Center, University of Bonn Medical Center, Sigmund Freud Str. 25., 53127, Bonn, Germany

      Bálint Szalontai

    5. Department of Biology, University of Zagreb, Rooseveltov trg 6, 10000, Zagreb, Croatia

      Mladen Kučinić

    6. Civil and Arhitectural Dept., Environmental Protection and Waste Management, Elektroprojekt, Alexandra von Humbolta 4, 10000, Zagreb, Croatia

      Ivan Vučković

    7. Water Supply and Environmental Engineering Institute, College of Eötvös József, Bajcsy-Zsilinszky Endre u. 14., 6500, Baja, Hungary

      Edit Vadkerti

    8. Department of Medical Genetics, University of Pécs, Szigeti út 12, 7624, Pécs, Hungary

      Péter Kisfali

    Authors
    1. Ildikó Szivák
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Tamás Mikes
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Bálint Szalontai
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Mladen Kučinić
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Ivan Vučković
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Edit Vadkerti
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Péter Kisfali
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. Steffen U. Pauls
      View author publications

      You can also search for this author in PubMed Google Scholar

    9. Miklós Bálint
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding authors

    Correspondence to Ildikó Szivák or Miklós Bálint.

    Additional information

    Handling editor: Luigi Naselli-Flores

    Steffen U. Pauls and Miklós Bálint have equally contributed to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Table S1

    Collection data, Genbank and Barcoding of Life sequence accession codes and collector information of Chaetopteryx rugulosa species complex and outgroup specimens. Supplementary material 1 (PDF 224 kb)

    Table S2

    Locality data of all populations within C. rugulosa species complex. These localities were used to compile the climatic dataset. The table includes the bedrock geological characteristics of the habitats. Abbreviations: fgsed - Fine-grained sedimentary rocks, sand - Sandstone, lime - Limestone, dolomite, coal - Coal, volc – Volcanic and volcaniclastic rocks, felig - Felsic igneous rocks, intig - Intermediate igneous rocks, mafig - Mafic igneous rocks, mbas - Metapelitic rocks, mpel - Metabasic rocks. Supplementary material 2 (PDF 230 kb)

    Table S3

    Climatic data layers used to infer the climatic conditions in the habitats of populations within C. rugulosa species complex. Supplementary material 3 (PDF 139 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Szivák, I., Mikes, T., Szalontai, B. et al. Ecological divergence of Chaetopteryx rugulosa species complex (Insecta, Trichoptera) linked to climatic niche diversification. Hydrobiologia 794, 31–47 (2017). https://doi.org/10.1007/s10750-016-3068-0

    Download citation

    • Received:

    • Revised:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s10750-016-3068-0

    Keywords

    Search

    Navigation