Mitochondrial phylogeography of the Mediterranean horseshoe bat on the Balkan Peninsula

Authors

  • Ivana Budinski Department of Genetic Research, Institute for Biological Research “Siniša Stanković” – National Institute of Republic of Serbia,, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0001-8834-4200
  • Vladimir M. Jovanović Department of Genetic Research, Institute for Biological Research “Siniša Stanković” – National Institute of Republic of Serbia,, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0002-8056-5065
  • Branka Pejić Department of Genetic Research, Institute for Biological Research “Siniša Stanković” – National Institute of Republic of Serbia,, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0002-4849-1756
  • Jelena Blagojević Department of Genetic Research, Institute for Biological Research “Siniša Stanković” – National Institute of Republic of Serbia,, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0001-7102-5510
  • Marija Rajičić Department of Genetic Research, Institute for Biological Research “Siniša Stanković” – National Institute of Republic of Serbia,, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0002-2470-9888
  • Milan Paunović Department of Biological Collections, Natural History Museum, Njegoševa 51, 11000 Belgrade http://orcid.org/0000-0002-8414-5674
  • Primož Presetnik Centre for Cartography of Fauna and Flora, Ljubljana Office, Tacenska cesta 20, SI-1210 Ljubljana http://orcid.org/0000-0003-4599-0493
  • Mladen Vujošević Department of Genetic Research, Institute for Biological Research “Siniša Stanković” – National Institute of Republic of Serbia,, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0002-5577-4455

Keywords:

D-loop, mitochondrial DNA, refugium, Rhinolophus euryale

Abstract

Paper description:

  • Large Mediterranean peninsulas (Iberian, Italian, Balkan) are the main glacial refugia for many European bat species.
  • We analysed mitochondrial D-loop sequences of Rhinolophus euryale from the Balkans in order to examine its genetic diversity and demographic history.
  • Our results yielded twenty new haplotypes that belonge to the same monophyletic clade. The star-like topology of haplotype network and shallow genetic differentiation support a scenario of population expansion.
  • New data on the genetic diversity of this species are presented. We propose that the Balkan Peninsula was its glacial refugium during the Pleistocene.


Abstract: The Balkan Peninsula is identified as one of the major glacial refugia in Europe during the Pleistocene, and it has served as a genetic source for post-glacial recolonization for many temperate species. The aim of this study was to investigate the genetic diversity and phylogeographic patterns of the Mediterranean horseshoe bat, Rhinolophus euryale Blasius 1853, on the Balkan Peninsula. We also analyzed its demographic history and tested the hypothesis that this region was a glacial refugium for this species. We collected 82 samples from 20 localities in the Balkans and Italy and sequenced the mitochondrial D-loop region. Our results revealed low nucleotide but high haplotype diversity, with 20 out of 24 haplotypes reported for the first time. All Balkan and Italian samples belonged to a single genetic clade in the phylogenetic reconstruction, where they clustered together with previously published samples from Turkey, southern France and North Africa. The haplotype network had a star-like pattern that is indicative of recent population expansion. Both mismatch distribution and shallow genetic differentiation also supported the scenario of a sudden demographic expansion. We estimated that expansion within this lineage commenced in the Late Pleistocene. We suggest that the Balkan Peninsula was a glacial refugium for R. euryale.

https://doi.org/10.2298/ABS190529059B

Received: May 29, 2019; Revised: August 5, 2019; Accepted: September 9, 2019; Published online: September 13, 2019

How to cite this article: Budinski I, Jovanović VM, Pejić B, Blagojević J, Rajičić M, Paunović M, Presetnik P, Vujošević M. Mitochondrial phylogeography of the Mediterranean horseshoe bat on the Balkan Peninsula. Arch Biol Sci. 2019;71(4):767-74.

Downloads

Download data is not yet available.

References

Hewitt GM. Post-glacial re-colonization of European biota. Biol J Linnean Soc. 1999;68:87-112.

Avise JC. Phylogeography: the history and formation of species. Cambridge, Mass: Harvard University Press; 2000. 464 p.

Taberlet P, Fumagalli L, Wust-Saucy A-G, Cosson J-F. Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol. 1998;7:453-64.

Randi E. Phylogeography of South European mammals. In: Weiss S, Ferrand N, editors. Phylogeography of Southern European Refugia. Dordrecht: Springer Netherlands; 2007. p. 101-26.

Hewitt GM. Mediterranean Peninsulas: The Evolution of Hotspots. In: Zachos FE, Habel JC, editors. Biodiversity Hotspots. Berlin, Heidelberg: Springer Berlin Heidelberg; 2011. p. 123-47.

Rebelo H, Froufe E, Brito JC, Russo D, Cistrone L, Ferrand N, Jones G. Postglacial colonization of Europe by the barbastelle bat: agreement between molecular data and past predictive modelling. Mol Ecol. 2012;21:2761-74.

Bilgin R, Gürün K, Rebelo H, Puechmaille SJ, Maracı Ö, Presetnik P, Benda P, Hulva P, Ibáñez C, Hamidovic D, Fressel N, Horáček I, Karataş A, Karataş A, Allegrini B, Georgiakakis P, Gazaryan S, Nagy ZL, Abi-Said M, Lučan RK, Bartonička T, Nicolaou H, Scaravelli D, Karapandža B, Uhrin M, Paunović M, Juste J. Circum-Mediterranean phylogeography of a bat coupled with past environmental niche modeling: A new paradigm for the recolonization of Europe? Mol Phylogenet Evol. 2016;99:323-36.

Furman A, Öztunç T, Postawa T, Çoraman E. Shallow genetic differentiation in Miniopterus schreibersii (Chiroptera: Vespertilionidae) indicates a relatively recent re-colonization of Europe from a single glacial refugium. Acta Chiropterol. 2010;12:51-9.

Kerth G, Petrov B, Conti A, Anastasov D, Weishaar M, Gazaryan S, Jaquiéry J, König B, Perrin N, Bruyndonckx N. Communally breeding Bechstein’s bats have a stable social system that is independent from the postglacial history and location of the populations. Mol Ecol. 2008;17:2368-81.

Ruedi M, Walter S, Fischer MC, Scaravelli D, Excoffier L, Heckel G. Italy as a major Ice Age refuge area for the bat Myotis myotis (Chiroptera: Vespertilionidae) in Europe. Mol Ecol. 2008;17:1801-14.

Petit E, Excoffier L, Mayer F. No Evidence of bottleneck in the postglacial recolonization of Europe by the Noctule Bat (Nyctalus noctula). Evolution. 1999;53:1247-58.

Boston ESM, Ian Montgomery W, Hynes R, Prodohl PA. New insights on postglacial colonization in western Europe: the phylogeography of the Leisler’s bat (Nyctalus leisleri). Proc R Soc Lond B Biol Sci. 2015;282:20142605.

Razgour O, Juste J, Ibáñez C, Kiefer A, Rebelo H, Puechmaille SJ, Arlettaz R, Burke T, Dawson DA, Beaumont M, Jones G. The shaping of genetic variation in edge-of-range populations under past and future climate change. Ecol Lett. 2013;16:1258-66.

Bilgin R, Furman A, Çoraman E, Karataş A. Phylogeography of the Mediterranean horseshoe bat, Rhinolophus euryale (Chiroptera: Rhinolophidae), in southeastern Europe and Anatolia. Acta Chiropterol. 2008;10:41-9.

Najafi N, Akmali V, Sharifi M. Historical explanation of genetic variation in the Mediterranean horseshoe bat Rhinolophus euryale (Chiroptera: Rhinolophidae) inferred from mitochondrial cytochrome-b and D-loop genes in Iran. Mitochondrial DNA A DNA Mapp Seq Anal. 2019;30(1):135-47.

Bilgin R, Çoraman E, Karataş A, Morales JC. Phylogeography of the Greater horseshoe bat, Rhinolophus ferrumequinum (Chiroptera: Rhinolophidae), in Southeastern Europe and Anatolia, with a specific focus on whether the Sea of Marmara is a barrier to gene flow. Acta Chiropterol. 2009;11:53-60.

Flanders J, Jones G, Benda P, Dietz C, Zhang S, Li G, Sharifi M, Rossiter SJ. Phylogeography of the greater horseshoe bat, Rhinolophus ferrumequinum : contrasting results from mitochondrial and microsatellite data. Mol Ecol. 2009;18:306-18.

Dool SE, Puechmaille SJ, Dietz C, Juste J, Ibáñez C, Hulva P, Roué SG, Petit EJ, Jones G, Russo D, Toffoli R, Viglino A, Martinoli A, Rossiter SJ, Teeling EC. Phylogeography and postglacial recolonization of Europe by Rhinolophus hipposideros : evidence from multiple genetic markers. Mol Ecol. 2013;22:4055-70.

Juste J, Ibáñez C, Muñoz J, Trujillo D, Benda P, Karataş A, Ruedi M. Mitochondrial phylogeography of the long-eared bats (Plecotus) in the Mediterranean Palaearctic and Atlantic Islands. Mol Phylogenet Evol. 2004;31:1114-26.

Benda P, Faizolâhi K, Andreas M, Obuch J, Reiter A, Ševčík M, Uhrin M, Vallo P, Ashrafi S. Bats (Mammalia: Chiroptera) of the Eastern Mediterranean and Middle East. Part 10. Bat fauna of Iran. Acta Soc Zool Bohem. 2012;76:163-582.

Dietz C, Kiefer A. Bats of Britain and Europe. 1st ed. Bloomsbury Publishing; 2016. p. 400.

Juste J, Alcaldé J. Rhinolophus euryale. [cited 2018 Dec 10]. In: The IUCN Red List of Threatened Species. [Internet]. IUCN; 2016 Apr 25. Available from: https://www.iucnredlist.org/species/19516/21971185

Uhrin M, Boldogh S, Bücs S, Paunović M, Mikova E, Juhász M, Juhász M, Csősz I, Estók P, Fulín M, Gombkötő P, Jére4 C, Barti L, Karapandža B, Matis Š, Nagy Z, Szodoray-Parádi F, Benda P. Revision of the occurrence of Rhinolophus euryale in the Carpathian region, Central Europe. Vespertilio. 2012;16:289-328.

Hutterer R, Ivanova T, Meyer-Cords C, Rodrigues L. Bat migrations in Europe: A review of banding data and literature. 1st ed. Bonn: Landwirtschaftsvlg Münster; 2005. p. 180.

Budinski I, Blagojević J, Jovanović VM, Pejić B, Adnađević T, Paunović M, Vujošević M. Population genetic structure of the Mediterranean horseshoe bat Rhinolophus euryale in the central Balkans. PLoS One. 2019;14:e0210321.

Canadian Council on Animal Care, CCAC species-specific recommendations on: BATS [Internet]. Ottawa, Canada: Canadian Council on Animal Care; 2003 [updated 2003 May 10; cited 2018 Dec 10]. Available from: https://www.ccac.ca/Documents/Standards/Guidelines/Add_PDFs/Wildlife_Bats.pdf .

Brunet-Rossinni AK, Wilkinson GS. Methods for age estimation and the study of senescence in bats. In: Kunz TH, Parsons S, editors. Ecological and behavioral methods for the study of bats. 2nd ed. John Hopkins University Press; 2009. p. 315-25.

Racey PA. Reproductive assessment of bats. In: Kunz TH, Parsons S, editors. Ecological and behavioral methods for the study of bats. 2nd ed. The Johns Hopkins University Press; 2009. p. 249-64.

Worthington Wilmer J, Barratt EM. A non-lethal method of tissue sampling for genetic studies of chiropterans. Bat Research News. 1996;37:1-3.

Strauss WM. Preparation of genomic DNA from mammalian tissue. Curr Protoc Mol Biol. 2001;Chapter 2:Unit2.2.

Puechmaille SJ, Gouilh MA, Piyapan P, Yokubol M, Mie KM, Bates PJ, Satasook C, New T, Hla Bu SS, Mackie IJ, Petit EJ, Teeling EC . The evolution of sensory divergence in the context of limited gene flow in the bumblebee bat. Nat Commun. 2011;2:573.

Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:4673-80.

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30:2725-9.

Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol. 2017;34:3299-302.

Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard A, Rambaut A, Drummond AJ. BEAST 2: A software platform for Bayesian evolutionary analysis. PLoS Comput Biol. 2014;10:e1003537.

Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9:772.

Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol. 2018;67:901-4.

Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980;16:111-20.

Bandelt HJ, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999;16:37-48.

Rogers AR, Harpending H. Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol. 1992;9:552-69.

Fu YX. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics. 1997;147:915-25.

Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123:585-95.

Rajaei Sh H, Rödder D, Weigand AM, Dambach J, Raupach MJ, Wägele JW. Quaternary refugia in southwestern Iran: insights from two sympatric moth species (Insecta, Lepidoptera). Org Divers Evol. 2013;13:409-23.

Çoraman E, Furman A, Karataş A, Bilgin R. Phylogeographic analysis of Anatolian bats highlights the importance of the region for preserving the Chiropteran mitochondrial genetic diversity in the Western Palaearctic. Conserv Genet. 2013;14:1205-16.

Shackleton JC, van Andel TH, Runnels CN. Coastal paleogeography of the Central and Western Mediterranean during the last 125.000 years and its archaeological implications. J Field Archaeol. 1984;11:307-14.

Downloads

Published

2019-12-19

How to Cite

1.
Budinski I, Jovanović VM, Pejić B, Blagojević J, Rajičić M, Paunović M, Presetnik P, Vujošević M. Mitochondrial phylogeography of the Mediterranean horseshoe bat on the Balkan Peninsula. Arch Biol Sci [Internet]. 2019Dec.19 [cited 2024Apr.20];71(4):767-74. Available from: https://www.serbiosoc.org.rs/arch/index.php/abs/article/view/4330

Issue

Section

Articles

Most read articles by the same author(s)