A first look at mitochondrial genetic diversity in Miniopterus schreibersii in Serbia
DOI:
https://doi.org/10.2298/ABS240208006BKeywords:
Schreiber’s bat, Chiroptera, HV1, control region, haplotypesAbstract
Paper description:
- Miniopterus schreibersii genetic diversity across its distribution has been explored using mitochondrial and nuclear markers, but without representation from Serbia.
- The mitochondrial hypervariable region 1 (HV1) gene fragment was screened to assess the genetic diversity of Serbian schreibersii and its relatedness to European and Asia Minor samples.
- Nine haplotypes, including 6 new ones, were found, indicating connectivity with Europe and Anatolia. The haplotype network suggested a single refugium origin and sudden population expansion.
- The genetic data for the Balkan region enhance our understanding of schreibersii population structure and support a previous hypothesis about its Anatolian origin.
Abstract: Schreiber’s bent-winged bat Miniopterus schreibersii (Chiroptera) is a widespread, cave-dwelling, regionally migrating species whose genetic diversity was studied throughout its distribution area using mitochondrial and nuclear markers. Previous studies revealed little to no structuring of populations and established Anatolia to be a single refugium during the last glacial maximum. The Balkans were well covered in these studies but usually lacked samples from Serbia. We sequenced the mitochondrial hypervariable region 1 (HV1) gene in M. schreibersii collected at seven sites in Serbia to assess their genetic relatedness to other European and Asia Minor populations and check whether the Balkans exhibit a higher genetic diversity than Western Europe due to its closeness to Anatolia. We recorded nine haplotypes from Serbia, six of which had not been previously reported, with a haplotype diversity of 0.585. The remaining three were shared with individuals from Portugal, Greece, and Turkey. A single most common haplotype was present throughout the species distribution range, pointing to a well-connected population and as indicated by the shape of the haplotype network, a common origin, and a sudden population expansion. Results complement existing data on M. schreibersii having a non-structured population, adding valuable new data from the Balkans supporting the previous hypothesis about its Anatolian origin.
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References
Paunović M, Karapandža B, Budinski I, Stamenković S. Fauna slepih miševa (Mammalia, Chiroptera) Srbije. Odeljenje. Petanović R, editor. Beograd: Srpska akademija nauka i umetnosti, Prirodnjački muzej u Beogradu; 2020. 601 p.
Furman A, Postawa T, Öztunç T, Çoraman E. Cryptic diversity of the bent-wing bat, Miniopterus schreibersii (Chiroptera: Vespertilionidae), in Asia Minor. BMC Evol Biol. 2010;10(1):121. https://doi.org/10.1186/1471-2148-10-121
Bilgin R, Gürün K, Maraci Ö, Furman A, Hulva P, Çoraman E, Lučan RK, Bartonička T, Horáček I. Syntopic occurrence in Turkey supports separate species status for Miniopterus schreibersii schreibersii and M. schreibersii pallidus (Mammalia: Chiroptera). Acta Chiropterologica 2012;14(2):279-89. http://www.bioone.org/doi/abs/10.3161/150811012X661611
Puechmaille SJ, Allegrini B, Benda P, Gürün K, Šrámek J, Ibañez C, Juste J, Bilgin R. A new species of the Miniopterus schreibersii species complex (Chiroptera: Miniopteridae) from the Maghreb region, North Africa. Zootaxa. 2014;3794(1):108-24. https://doi.org/10.11646/zootaxa.3794.1.4
Dietz C, Kiefer A. Bats of Britain and Europe. Bloomsbury Publishing; 2016. 398 p.
Hutterer R, Ivanova T, Mayer-Cords C, Rodrigues L. Bat migrations in Europe: A review of banding data and literature. Bonn : Naturschutz und biologische Vielfalt; 2005.
Ramos Pereira MJ, Salgueiro P, Rodrigues L, Coelho MM, Palmeirim JM. Population structure of a cave-dwelling bat, Miniopterus schreibersii: Does it reflect history and social organization? J Hered 2009;100(5):533-44. https://doi.org/10.1093/jhered/esp032
Rodrigues L, Pereira MJR, Rainho A, Palmeirim JM. Behavioural determinants of gene flow in the bat Miniopterus schreibersii. Behav Ecol Sociobiol. 2010;64(5):835-43. https://doi.org/10.1007/s00265-009-0900-9
Witsenburg F, Clément L, López-Baucells A, Palmeirim J, Pavlinić I, Scaravelli D, Ševčík M, Dutoit L, Salamin N, Goudet J, Christe P. How a haemosporidian parasite of bats gets around: the genetic structure of a parasite, vector and host compared. Mol Ecol 2015;24(4):926-40. https://onlinelibrary.wiley.com/doi/10.1111/mec.13071
Moulistanos A, Chatzoglou G, Karaiskou N, Gkagkavouzis K, Minoudi S, Papoulidis I, Alivizatos C, Panagiotopoulou M, Youlatos D, Tsaktsira M, Triantafyllidis A, Scaltsoyiannes A. Genetic diversity of bat species in the cross-border area of Greece and Bulgaria. J Biol Res. 2023;30:6. https://doi.org/10.26262/jbrt.v30i0.9024
Dufresnes C, Dutoit L, Brelsford A, Goldstein-Witsenburg F, Clément L, López-Baucells A, Palmeirim J, Pavlinić I, Scaravelli D, Ševčík M, Christe P, Goudet J. Inferring genetic structure when there is little: Population genetics versus genomics of the threatened bat Miniopterus schreibersii across Europe. Sci Rep 2023;13(1):1523. https://doi.org/10.1038/s41598-023-27988-4
Borloti I, Dinis H, Vasconcelos R. Bats out of Africa: Disentangling the systematic position and biogeography of bats in Cabo Verde. Genes (Basel). 2020;11(8):877. https://doi.org/10.3390/genes11080877
Gürün K, Furman A, Juste J, Ramos Pereira MJ, Palmeirim JM, Puechmaille SJ, Hulva P, Presetnik P, Hamidovic D, Ibáñez C, Karataş A, Allegrini B, Georgiakakis P, Scaravelli D, Uhrin M, Nicolaou H, Abi-Said MR, Nagy ZL, Gazaryan S, Bilgin R. A continent-scale study of the social structure and phylogeography of the bent-wing bat, Miniopterus schreibersii (Mammalia: Chiroptera), using new microsatellite data. J Mammal 2019;100(6):1865-78.https://doi.org/10.1093/jmammal/gyz153
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 Chiropterologica 2010;12(1):51-9. https://doi.org/10.3161/150811010X504581
Bilgin R, Gürün K, Rebelo H, Puechmaille SJ, Maraci 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. https://doi.org/10.1016/j.ympev.2016.03.024
Hewitt GM. Mediterranean Peninsulas: The Evolution of Hotspots. In: Zachos FE, Habel JC, editors. Biodiversity hotspots distribution and protection of conservation priority areas. Berlin, Heidelberg: Springer Berlin Heidelberg; 2011. p. 123-47. https://doi.org/10.1007/978-3-642-20992-5_7
Çoraman E, Furman A, Karataş A, Bilgin R, Karatas A. 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(6):1205-16. https://doi.org/10.1007/s10592-013-0509-4
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(10):2368-81. https://doi.org/10.1111/j.1365-294X.2008.03768.x
Bilgin R, Karataş A, Çoraman E, Disotell T, Morales J. Regionally and climatically restricted patterns of distribution of genetic diversity in a migratory bat species, Miniopterus schreibersii (Chiroptera: Vespertilionidae). BMC Evol Biol 2008;8(1):209. https://doi.org/10.1186/1471-2148-8-209
Furman A, Öztunç T, Çoraman E. On the phylogeny of Miniopterus schreibersii schreibersii and Miniopterus schreibersii pallidus from Asia Minor in reference to other Miniopterus taxa (Chiroptera: Vespertilionidae). Acta Chiropterologica 2010;12(1):61-72.https://doi.org/10.3161/150811010X504590
Strauss WM. Preparation of genomic DNA from mammalian tissue. Curr Protoc Immunol. 1993;8(1):8-10. https://doi.org/10.1002/0471142735.im1002s08
Wilkinson GS, Chapman AM. Length and sequence variation in evening bat D-loop mtDNA. Genetics. 1991;128(3):607-17. https://doi.org/10.1093/genetics/128.3.607
Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sanchez-Gracia A. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol. 2017;34(12):3299-302. https://doi.org/10.1093/molbev/msx248
Excoffier L, Lischer HEL. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010;10(3):564-7. https://doi.otg/10.1111/j.1755-0998.2010.02847.x
Leigh JW, Bryant D. POPART: Full-feature software for haplotype network construction. Methods Ecol Evol. 2015;6(9):1110-6. https://doi.org/10.1111/2041-210X.12410
Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genet Soc Am. 1989;(123):585-95. 10.1093/genetics/123.3.585
Bilgin R, Karatas A, Çoraman E, Pandurski I, Papadatou E, Morales JC. Molecular taxonomy and phylogeography of Miniopterus schreibersii (Kuhl, 1817) (Chiroptera : Vespertilionidae), in the Eurasian transition. Biol J Linn Soc. 2006;87:577-82. https://doi.org/10.1111/j.1095-8312.2006.00591.x
Furman A, Çoraman E, Bilgin R, Karataş A. Molecular ecology and phylogeography of the bent-wing bat complex (Miniopterus schreibersii) (Chiroptera: Vespertilionidae) in Asia Minor and adjacent regions. Zool Scr. 2009;38(2):129-41. https://doi.org/10.1111/j.1463-6409.2008.00365.x
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30(12):2725-9. https://doi.org/10.1093/molbev/mst197
Tamura K, Nei M, Kumar S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A. 2004;101(30):11030-5. https://doi.org/10.1073/pnas.0404206101
Stanković D, Paunović M, Raković M. Atlas migratornih ptica i slepih miševa Srbije. Beograd: Prirodnjački muzej u Beogradu; 2018. 535 p.
Presetnik P, Budinski I, Hodžić M, Mulaomerović J. Miniopterus schreibersii migration. 7. 5. 2016, Petrovaradin (Serbia) – 19. 2. 2017, Dardagani- Zvornik (Bosnia and Herzegovina). Hypsugo. 2017;2(1):50-1.
Budinski I, Pejić B, Paunović M, Karapandža B, Josipović J. Evropski dugokrilaš, Minipterus schreibersii, Schreiber’s bent-winged bat. In: Stanković D, Paunović M, Raković M, editors. Atlas migratornih ptica i slepih miševa Srbije. Beograd: Ministarstvo zaštite životne sredine Republike Srbije, Ministarstvo kulture i informisanja Republike Srbije, Prirodnjački muzej u Beogradu; 2018. p. 513-22.
Miller-Butterworth CM, Jacobs DS, Harley EH. Strong population substructure is correlated with morphology and ecology in a migratory bat. Nature. 2003;424:187-91. https://doi.org/10.1038/nature01742
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