Abstract
In this study we investigated genetic variability of the riffle beetle Elmis maugetii Latreille, 1802 (Coleoptera: Elmidae) in Europe and North Africa. The samples barcoded in the present study cover the following countries: the Netherlands, Croatia, Serbia, and Greece. The analysis also includes additional data from Austria, Germany, France, Spain, Slovakia, France, and North Africa (Morocco). mtDNA sequences of the newly barcoded E. maugetii specimens were compared to all sequences available for this species in the BOLD and NCBI GenBank databases. The present study also provides data on population genetic parameters of the species [haplotype diversity, nucleotide diversity, Theta (per site) from Eta, Tajima’s D value], minimum-spanning networks, phylogeographic structure, and possible corridors of its recolonization of the European continent in the Pleistocene. Genetic diversity of E. maugetii was found to be lower in northern regions of Europe. According to the proposed evolutionary history of E. maugetii, the colonization of northern latitudes most likely started from the Balkan Peninsula (suggested as the species´ main glacial refugium in Europe) and proceeded via Central, Northern, and Western Europe, finally reaching the Pyrenean Peninsula (Spain). The specimens from North Africa (Morocco) are slightly distinct from the European ones. To judge from data obtained on the genetic structure of populations of this riffle beetle species, it is characterized by shallow genetic structure within mitochondrial DNA in general.
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References
Aksu AE, Hiscot RN, Yaşar D (1999) Oscillating Quartenary water levels of the Marmara Sea and vigorous outflow into the Aegean Sea from the Marmara Sea-Black Sea drainage corridor. Mar Geol 153(1–4):275–302
Bilton DT, Freeland JR, Okamura B (2001) Dispersal in freshwater invertebrates. Annu Rev Ecol Syst 32:159–181. https://doi.org/10.1146/annurev.ecolsys.32.081501.114016
Boukal DS, Boukal M, Fikáček M, Hájek J, Klečka J, Skalický S, Šťastný J, Trávníček D (2007) Catalogue of water beetles of the Czech Republic (Coleoptera: Sphaeriusidae, Gyrinidae, Haliplidae, Noteridae, Hygrobiidae, Dytiscidae, Helophoridae, Georissidae. Klapalekiana 43(Suppl):1–289 [in Czech and English]. https://doi.org/10.1111/j.1365-294X.2005.02663.x
Brito PH (2005) The influence of Pleistocene glacial refugia on tawny owl genetic diversity and phylogeography in western Europe. Mol Ecol 14:3077–3094. https://doi.org/10.1111/j.1365-294X.2005.02663.x
Canestrelli D, Aloise G, Cecchetti S, Nascetti G (2010) Birth of a hotspot of intraspecific genetic diversity: notes from the underground. Mol Ecol 19:5432–5451. https://doi.org/10.1111/j.1365-294X.2010.04900.x
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660. https://doi.org/10.1046/j.1365-294x.2000.01020.x
Comes HP, Kadereit JW (1998) The effect of Quaternary climatic changes on plant distribution and evolution. Trends Plant Sci 3(11):432–438. https://doi.org/10.1016/S1360-1385(98)01327-2
Čiampor F Jr, Čiamporová-Zaťovičová Z, Kodada J (2009) Description of the larva of Oulimnius echinatus Berthélemy (Coleoptera: Elmidae: Elminae). Zootaxa 1984:57–60. https://doi.org/10.5281/zenodo.185385
Čiampor F Jr, Kodada J (2010) Taxonomy of the Oulimnius tuberculatus species group (Coleoptera: Elmidae) based on molecular and morphological data. Zootaxa 2670:59–68. https://doi.org/10.11646/zootaxa.2670.1.4
Drag L, Hauck D, Říčan O, Schmit T, Shovkoon D, Godunko R, Curletti G, Cižek L (2018) Phylogeography of the endangered saproxylic beetle Rosalia longicorn, Rosalia alpina (Coleoptera, Cerambycidae), corresponds with its main host, the European beech (Fagus sylvatica, Fagaceae). J Biogeogr 45(12):2631–2644. https://doi.org/10.1111/jbi.13429
Drovetski SV, Fadeevm IV, Rakovic M, Lopes RJ, Boano G, Pavia M, Koblik EA, Lohman YV, Red’kin YA, Aghayan SA, Reis SS, Drovetskaya SS, Voelker G (2018) A test of the European Pleistocene refugial paradigm, using a Western Palaearctic endemic bird species. Proc Biol Sci 285. https://doi.org/10.1098/rspb.2018.1606
Elliott JM (2008) The ecology of riffle beetles (Coleoptera: Elmidae). Freshw Rev 1:189 – 203. https://doi.org/10.1608/FRJ-1.2.4
Escudero M, Vargas P, Arens P, Ouborg NJ, Luceño M (2010) The east-west-north colonization history of the Mediterranean and Europe by the coastal plant Carex extensa (Cyperaceae). Mol Ecol 19(2):352–370. https://doi.org/10.1111/j.1365-294X.2009.04449.x
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. Mol Mar Biol Biotechnol 3:294–299
Friday LE (1988) A key to the adults of British water beetles. Field Studies Council, Darwin College, Cambridge, p 88
Garcia-Raventós A, Viza A, Múrria C (2021) Taxonomic turnover and northward phylogenetic clustering reveal evidence for environmental filtering in structuring Trichoptera communities across Europe. Freshw Biol 66(6):1060–1073. https://doi.org/10.1111/fwb.13699
Grigoropoulou A, Schmidt-Kloiber A, Múrria C (2022) Incongruent latitudinal patterns of taxonomic, phylogenetic and functional diversity reveal different drivers of caddisfly community assembly across spatial scales. Glob Ecol Biogeogr 00:1–15. https://doi.org/10.1111/geb.13479
Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc Biol Sci 270:313–322. https://doi.org/10.1098/rspb.2002.2218
Hering D, Verdonschot PFM, Moog O, Sandin L (2004) Overview and application of the AQEM assessment system. Hydrobiologia 516:1–20
Hewitt GM (1993) After the ice: parallelus meets erythropus in the Pyrenees. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, New York, pp 140–156
Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc Lond 58:247–276
Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc Lond 68:87–112. https://doi.org/10.1006/bijl.1999.0332
Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913. https://doi.org/10.1038/35016000
Hewitt G (2004) The structure of biodiversity - Insights from molecular phylogeography. Front Zool 1(1):4. https://doi.org/10.1186/1742-9994-1-4
Ibrahim K, Nichols R, Hewitt GM (1996) Spatial patterns of genetic variation generated by different forms of dispersal. Heredity (Edinb) 77(3):282–291. https://doi.org/10.1038/hdy.1996.142
Iversen LL, Jacobsen D, Sand-Jensen K (2016) Are latitudinal richness gradients in European freshwater species only structured according to dispersal and time? Ecography 39:1247–1249. https://doi.org/10.1111/ecog.02183
Jäch MA, Kodada J, Brojer M, Shepard WD, Čiampor F, Jr (2016) Coleoptera: Elmidae and Protelmidae. World Catalogue of Insects 14:318. Brill, Leiden XXI + pp. https://doi.org/10.1163/9789004291775
Kodada J, Jäch MA, Čiampor F, Jr (2016) Elmidae Curtis, 1830. In: Beutel RG, Leschen RAB (eds) Handbook of Zoology Vol 4, Part 38, 2nd edn. Coleoptera, Beetles, Volume 1: Morphology and Systematics (Archostemata, Adephaga, Myxophaga, Polyphaga partim), Walter de de Gruyter, Berlin, pp 561–589
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
Lomolino MV, Pijanowski BC, Gasc A (2015) The silence of biogeography. J Biogeogr 42:1187-1196. https://doi.org/10.1111/jbi.12525
Malicky H (2006) Mitteleuropäische (extra - mediterrane) Arealkerne des Dinodal am Beispiel von Köcherfliegen (Trichoptera). Beitr Entomol 56(2):347–359. https://doi.org/10.21248/contrib.entomol.56.2.347-359
Múrria C, Bonada N, Vellend M, Zamora-Muñoz C, Alba-Tercedor J, Sainz-Cantero CE, Garrido J, Acosta R, El Alami M, Barquín J, Derka T, Álvarez-Cabria M, Sáinz-Bariain M, Filipe FA, Vogler AP (2017) Local environment rather than past climate determines community composition of mountain stream macroinvertebrates across Europe. Mol Ecol 26(21):6085–6099
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York, 512 pp
Novaković BB (2020) Morfometrijska i filogenetska analiza vrsta familije Elmidae (Insecta: Coleoptera) Balkanskog poluostrva. Dissertation, University of Belgrade, Faculty of Biology, 192 pp [in Serbian]
Olmi M (1976) Coleoptera, Dryopidae, Elminthidae. Fauna d’ Italia, vol 12. Edizioni Calderini, Bologna, 280 pp. [in Italian]
Pauls SU, Lumbsch HT, Haase P (2006) Phylogeography of the montane caddisfly Drusus discolor: Evidence for multiple refugia and periglacial survival. Mol Ecol 15:2153–2169. https://doi.org/10.1111/j.1365-294X.2006.02916.x
Peter BM, Slatkin M (2015) The effective founder effect in a spatially expanding population. Evolution 69:721–734. https://doi.org/10.1111/evo.12609
Petit RJ, Aguinagalde I, de Beaulieu J-L, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohnty A, Müller-Starck G, Demesure-Musch B, Palmé A, Pedro Martin J, Rendell S, Vendramin GG (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565. https://doi.org/10.1126/science.1083264
Pons JM, Thibault JC, Aymí R, Grussu M, Muntaner J, Olioso G, Sunyer JR, Touihri M, Fuchs J (2016) The role of western Mediterranean islands in the evolutionary diversification of the spotted flycatcher Muscicapa striata, a long-distance migratory passerine species. J Avian Biol 47:386–398. https://doi.org/10.1111/jav.00859
Previšić A, Walton C, Kučinić M, Mitrikeski PT, Kerovec M (2009) Pleistocene divergence of Dinaric Drusus endemics (Trichoptera, Limnephilidae) in multiple microrefugia within the Balkan Peninsula. Mol Ecol 18:634–647. https://doi.org/10.1111/j.1365-294X.2008.04046.x
Raković M, Neto JM, Lopes RJ, Koblik EA, Fadeev IV, Lohman YV, Aghayan SA, Boano G, Pavia M, Perlman Y, Kiat Y, Ben Dov A, Martin Collinson J, Voelker G, Drovetski SV (2019) Geographic patterns of mtDNA and Z-linked sequence variation in the Common Chiffchaff and the ‘chiffchaff complex’. PLoS ONE 14(1). https://doi.org/10.1371/journal.pone.0210268
Ratnasingham S, Hebert PDN (2007) BOLD: The Barcode of Life Data System. Mol Ecol Notes 7:355–364. https://doi.org/10.1111/j.1471-8286.2007.01678.x
Ribera I (2008) Habitat constraints and the generation of diversity in freshwater macroinvertebrates. In: Lancaster J, Briers RA (eds) Aquatic Insects: Challenges to Populations. CAB International, Wallingford, pp 289–311
Schmitt T (2007) Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Front Zool 4:11. https://doi.org/10.1186/1742-9994-4-11
Salinas-Ivanenko S, Múrria C (2021) Macroecological trend ofincreasing values of intraspecific genetic diversity and populationstructure from temperate to tropical streams. Glob Ecol Biogeogr 30:1685–1697. https://doi.org/10.1111/geb.13344
Schmitt T, Seitz A (2001) Intraspecific allozymatic differentiation reveals the glacial refugia and the postglacial expansions of European Erebia medusa (Lepidoptera: Nymphalidae). Biol J Linn Soc 74:429–458. https://doi.org/10.1111/j.1095-8312.2001.tb01404.x
Schmitt T, Gießl A, Seitz A (2002) Postglacial colonisation of western Central Europe by Polyommatus coridon (Poda 1761) (Lepidoptera: Lycaenidae): evidence from population genetics. Heredity 88:26–34. https://doi.org/10.1038/sj.hdy.6800003
Schmitt T, Varga Z (2012) Extra-Mediterranean refugia: The rule and not the exception? Front Zool 9:22. https://doi.org/10.1186/1742-9994-9-22
Segal B (1933) The hind wings of some Dryopidae in relation to habitat (Coleoptera). Entomol News 44:85–88
Shepard W (2019) Flight wing polymorphisms in Elmidae and Dryopidae (Coleoptera: Byrrhoidea). Coleopt Bull 73(1):27–44. https://doi.org/10.1649/0010-065X-73.1.27
Short AEZ, Caterino MS (2009) On the validity of habitat as a predictor of genetic structure in aquatic systems: a comparative study using California water beetles. Mol Ecol 18:403–414. https://doi.org/10.1111/j.1365-294X.2008.04039.x
Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464. https://doi.org/10.1046/j.1365-294x.1998.00289.x.
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tajima F (1996) The amount of DNA polymorphism maintained in a finite population when the neutral mutation rate varies among sites. Genetics 143:1457–1465
Terrab A, Schönswetter P, Talavera S, Vela E, Stuessy TF (2008) Range-wide phylogeography of Juniperus thurifera L., a presumptive keystone species of western Mediterranean vegetation during cold stages of the Pleistocene. Mol Phylogenet Evol 48:94–102
Tzedakis PC (2004) The Balkans as prime glacial refugial territory of European temperate trees. In: Griffiths HI, Kryštufek B, Reed JM (eds) Balkan Biodiversity. Dordrecht, Boston, London, pp 49–68
Wahlberg N, Saccheri I (2007) The effects of Pleistocene glaciations on the phylogeography of Melitaea cinxia (Lepidoptera: Nymphalidae). Eur J Entomol 104:675–684. https://doi.org/10.14411/eje.2007.085
Acknowledgements
The authors are deeply grateful to Mr. Cesc Múrria (University of Barcelona, Spain) for permission to publish data from Múrria et al. (2017); Mr. Arjen Speksnijder, Mr. Oscar Vorst (Naturalis Biodiversity Center, the Netherlands) and Mr. Vincent Dubut (Aix-Marseille Université, France) for permission to publish their data; Mrs. Vlatka Mičetić Stanković (Croatian Natural History Museum, Zagreb, Croatia), Mrs. Branka Bruvo Mađarić (“Ruđer Bošković“ Institute, Zagreb, Croatia) and Ms. Jelena Đuknić (“Siniša Stanković” Institute for Biological Research, Belgrade, Serbia) for suggestions during writing of the manuscript, and Mr. Raymond W. Dooley for linguistic review of the manuscript.
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This study was partly supported by VEGA project 2/0042/20.
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All authors contributed to the study conception and design. Boris Novaković collected some of specimens in the field. Fedor Čiampor worked on barcoding and molecular taxa analyses. Marko Raković worked on population genetic analyses. Boris Novaković and Marko Raković wrote the manuscript. Teodora Teofilova and Ivana Živić reviewed several drafts of the manuscript. The first draft of the manuscript was written by Boris Novaković and Marko Raković and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript. The present study is a part of the PhD research of the riffle beetles from the Balkan Peninsula (Novaković 2020).
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Novaković, B.B., Raković, M.B., Čiampor Jr, F. et al. Genetic variability of the riffle beetle Elmis maugetii Latreille, 1802 (Coleoptera: Elmidae) in Europe and North Africa. Biologia 77, 3173–3183 (2022). https://doi.org/10.1007/s11756-022-01206-4
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DOI: https://doi.org/10.1007/s11756-022-01206-4