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Lack of intraspecific variations of the mitochondrial cytochrome b gene in the greater mouse-tailed bat Rhinopoma microphyllum (Chiroptera: Rhinopomatidae) in Iran

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Abstract

Rhinopoma microphyllum is one of the species of bats that lives in arid and semi-arid areas of Iran. The initial suggestion of the presence of two subspecies R. m. microphyllum and R. m. harrisoni based on their morphological characteristics has been questioned on the basis of small differences between the populations. Later, other researchers assigned Iranian populations of this species to one or two subspecies based on their morphological and molecular characteristics. The present study provides a phylogeographical analysis of this species using 687 bp of the mitochondrial cytochrome b in 81 bats in Iran, Jordan, Levant and Ethiopia. Based on mtDNA sequences, we found a low degree of genetic diversity in the Iranian populations of R. microphyllum (π = 0.0025), which shows a close relationship between the haplotypes. The analysis of genetic distance (0.15–1.93%), phylogenetic trees, and statistical parsimony network showed that all Iranian samples were grouped in the same clade, while Levant, Jordan and Ethiopian samples belonged to a different clade. Molecular dating suggested the Iranian R. microphyllum lineage split from the R. microphyllum of the Levant and Jordan clade during the Pliocene 3.18 (2.11–4.32 Ma). Taking these results into consideration, we can conclude that all Iranian specimens belong to the same subspecies as R. m. harrisoni since molecular results indicate that Iranian samples are differ from Levant subspecies (R. m. microphyllum).

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References

  • Agnarsson I, Zambrana-Torrelio CM, Flores-Saldana NP, May-Collado LJ (2011) A time-calibrated species-level phylogeny of bats (Chiroptera, Mammalia). PLoS Curr Tree Life. https://doi.org/10.1371/currents.RRN1212

    Article  Google Scholar 

  • Akmali V, Farazmand A, Darvish J, Sharifi M (2011) Phylogeography and taxonomic status of the greater mouse-tailed bat Rhinopoma microphyllum (Chiroptera: Rhinopomatidae) in Iran. Acta Chiropterol 13:279–290

    Google Scholar 

  • Akmali V, Mehdizadeh R, Chaghamirza K, Moradi M, Sharifi M (2014) Taxonomic evaluation of the bent-winged bat (Miniopterus) populations occurring in Iran inferred from mitochondrial cytochrome- b sequences. Mammalia 79(4):449–455

    Google Scholar 

  • Baker RJ, Bradley RD (2006) Speciation in mammals and the genetic species concept. J Mammal 87:643–662

    PubMed  Google Scholar 

  • Benda P, Andreas M, Kock D, Lucan R, Munclinger P, Nova P, Obuch J, Ochman K, Reiter A, Uhrin M, Weinfurtova D (2006) Bats (Mammalia: Chiroptera) of the Eastern Mediterranean. Part 4. Bat fauna of Syria: distribution, systematics, ecology. Acta Soc Zool Bohem 70:1–329

    Google Scholar 

  • Benda P, Reiter A, Al-Jumaily M, Nasher AK, Hulva P (2009) A new species of mouse-tailed bat (Chiroptera: Rhinopomatidae: Rhinopoma) from Yemen. J Natl Mus (Prague) Nat Hist Ser 177(6):53–68

    Google Scholar 

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

    Google Scholar 

  • Benda P, Kasso M, Nicolas V, Pleurdeau D, Stoetzel E, Workalemahu S, Bekele A, Denys C (2019) New data on bats from dire dawa region, eastern Ethiopia, with the first record of Rhinopoma microphyllum in the country. J Nat His 53:41–42

    Google Scholar 

  • Bilgin R, Karataş A, Çoraman E, Pandurski I, Papadatou E, Morales JC (2006) Molecular taxonomy and phylogeography of Miniopterus schreibersii (Kuhl, 1817) (Chiroptera: Vespertilionidae), in the Eurasian transition. Biol J Linn Soc Lond 87:577–582

    Google Scholar 

  • Bilgin R, Karataş A, Çoraman E, Morales JC (2008) The mitochondrial and nuclear genetic structure of Myotis capaccinii (Chiroptera: Vespertilionidae) in the Eurasian transition, and its taxonomic implications. Zool Scr 37:253–262

    Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    CAS  PubMed  Google Scholar 

  • DeBlase AF (1980) The bats of Iran: systematics, distribution, ecology. Field Zool 4:1–424

    Google Scholar 

  • Dool SE, Puechmaille SJ, Dietz C, Juste J, Ibánez C, Hulva P, Roué SG, Petit E, Jones G, Russo D, Toffoli R (2013) Phylogeography and postglacial recolonization of Europe by Rhinolophus hipposideros: evidence from multiple genetic markers. Mol Ecol 22:4055–4070

    CAS  PubMed  Google Scholar 

  • Drummond AJ, Marc A, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29(8):1969–1973

    CAS  PubMed  PubMed Central  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin: ver.3.1: an integrated software package for population genetics data analysis. Evol Biol 1:47–50

    CAS  Google Scholar 

  • Fernandes CA, Rohling EJ, Siddall M (2006) Absence of post-Miocene red sea land bridges: biogeographic implications. J Biogeogr 33:961–966

    Google Scholar 

  • Flanders JON, Jones G, Benda P, Dietz C, Zhang S, Li G, Sharifi M, Rossiter SJ (2009) Phylogeography of the greater horseshoe bat, Rhinolophus ferrumequinum: contrasting results from mitochondrial and microsatellite data. Mol Ecol 18:306–318

    CAS  PubMed  Google Scholar 

  • Furman A, Öztunç T, Çoraman E (2010) On the phylogeny of Miniopterus Schreibersii Schreibersii and Miniopterus Schreibersii Pallidus from Asia minor in reference to other Miniopterus Taxa (Chiroptera: Vespertilionidae). Acta Chiropterol 12:61–72

    Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704

    PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hill JE (1977) A review of the Rhinopomatidae (Mammalia: Chiroptera). Bull Br Mus Nat Hist Zool Ser 32:29–43

    Google Scholar 

  • Hulva P, Horacek I, Benda P (2007) Molecules, morphometrics and new fossils provide an integrated view of the evolutionary history of Rhinopomatidae (Mammalia: Chiroptera). BMC Evol Biol 7:165

    PubMed  PubMed Central  Google Scholar 

  • Irwin DM, Kocher TD, Wilson AC (1991) Evolution of the cytochrome b gene of mammals. J Mol Evol 32:128–144

    CAS  PubMed  Google Scholar 

  • Kafaei S, Sharifi M, Akmali V (2020) Population genetic structure and phylogeography of the small mouse-tailed bat, Rhinopoma muscatellum Thomas, 1903 (Chiroptera: Rhinopomatidae) in Iran inferred from mitochondrial DNA". Acta Chiroptrol 22(1):29–40. https://doi.org/10.3161/15081109ACC2020.22.1.003

    Article  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    CAS  PubMed  Google Scholar 

  • Kock D (1969) Die Fledermaus-Fauna des Sudan. Abh der Senckenbergischen Naturforschenden Ges 521:1–238

    Google Scholar 

  • Koufos GD, Kostopoulos DS, Vlachou TD (2005) Neogene/quaternary mammalian migrations in Eastern Mediterranean. Belg J Zool 135(2):181–190

    Google Scholar 

  • Koopman KF (1994) Chiroptera: systematics. Handbook of zoology: mammalia, vol 8. Walter de Gruyter, New York, p 217

    Google Scholar 

  • Levin E, yom-tov Y, barnea A, Huchon D (2008) Genetic diversity and phylogeography of the greater mouse-tailed bat Rhinopoma microphyllum (Brünnich, 1782) in the Levant. Acta Chiropterol 10(2):207–212

    Google Scholar 

  • Li G, Jones G, Rossiter SJ, Chen SF, Parsons S, Zhang S (2006) Phylogenetics of small horseshoe bats from East Asia based on mitochondrial DNA sequence variation. J Mammal 87(6):1234–1240

    Google Scholar 

  • Loumassine H-E, Allegrini B, Bounaceur F, Peyre O, Aulagnier S (2018) A new mammal species for Algeria, Rhinopoma microphyllum (Chiroptera: Rhinopomatidae): morphological and acoustic identification. Mammalia 82(1):85–88

    Google Scholar 

  • Memish Z, Mishra N, Olival K, et al (2013) Middle east respiratory syndrome coronavirus in bats, Saudi Arabia. Emerg Infect Dis 19:e131172

  • Miller-Butterworth CM, Jacobs DS, Harley EH (2003) Strong population substructure is correlated with morphology and ecology in a migratory bat. Nature 424:187–191

    CAS  PubMed  Google Scholar 

  • Najafi N, Akmali V, Sharifi M (2018) 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 Part A 25:1–13

    Google Scholar 

  • Najafi N, Sharifi M, Akmali V (2019) First insights into the population genetic structure and the phylogeographic status of the Mehely’s horseshoe bat Rhinolophus mehelyi (Chiroptera: Rhinolophidae) in Iran inferred from mitochondrial genes. Mammal Biol 99:97–108

    Google Scholar 

  • Porter CA, Baker RJ (2004) Systematics of Vampyressa and related genera of phyllostomid bats as determined by cytochrome-b sequences. Mammalia 85:126–132

    Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    CAS  PubMed  Google Scholar 

  • Rambaut A (2012) FigTree v.1. 4.0. University of Oxford, Oxford

    Google Scholar 

  • Rambaut A, Drummond AJ (2009) Tracer v1.5.0. http://beast.bio.ed.ac.uk/Trace. Accessed 23 Apr 2013

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    CAS  PubMed  Google Scholar 

  • Rozas J, Sanchez-de I, Barrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    CAS  PubMed  Google Scholar 

  • Ruedi M, Castella V (2003) Genetic consequences of the ice ages on nurseries of the bat Myotis myotis: a mitochondrial and nuclear survey. Mol Ecol 12:1527–1540

    CAS  PubMed  Google Scholar 

  • Ruedi M, McCracken GF (2009) Genetics and evolution: phylogeographic analysis of bats. In: Kunz TH, Parsons S (eds) Ecological and behavioral methods for the study of bats, 2nd edn. Boston Johns Hopkins University Press, Baltimore, pp 739–756

    Google Scholar 

  • Schlitter DA, Deblase AF (1974) Taxonomy and geographic distribution of Rhinopoma microphyllum (Chiroptera: Rhinopomatidae) in Iran, with the description of a new subspecies. Mammalia 38:657–665

    Google Scholar 

  • Schlitter DA, Qumsiyeh MB (1996) Rhinopoma microphyllum. Mamm Species 542:1–5

    Google Scholar 

  • Shahabi S, Akmali V, Sharifi M (2019) Echolocation call frequency and mitochondrial control region variation in the closely related bat species of the genus Rhinolophus (Chiroptera: Rhinolophidae) occurring in Iran: implications for taxonomy and intraspecific phylogeny. Mammal Res 4:485

    Google Scholar 

  • Shahabi S, Akmali V, Sharifi M (2017) Taxonomic evaluation of the greater horseshoe bat Rhinolophus ferrumequinum (Chiroptera: Rhinolophidae) in Iran inferred from the mitochondrial D-loop gene. Zool Sci 34(4):361–367

    Google Scholar 

  • Simmons NB (2005) Order chiroptera. In: Wilson DE, Reeder DM (eds) Mammal species of the World: a taxonomic and geographic reference, 3rd edn. The Johns Hopkins University Press, Baltimore, p 2142

    Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    CAS  PubMed  PubMed Central  Google Scholar 

  • Van Cakenberghe V, De Vree F (1994) A revision of the Rhinopomatidae Dobson 1872, with the description of a new subspecies (Mammalia: Chiroptera). Senckenb Biol 73:1–24

    Google Scholar 

  • Worthington Wilmer J, Barratt EM (1996) A non-lethal method of tissue sampling for genetic studies of chiropterans. Bat Res News 37:1–3

    Google Scholar 

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Authors and Affiliations

  1. Department of Biology, Faculty of Science, Lorestan University, Lorestan, Iran

    Shiva Bagherfard

  2. Department of Biology, Faculty of Science, Razi University, Kermanshah, Iran

    Nargess Najafi, Ahmad Gharzi & Vahid Akmali

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  1. Shiva Bagherfard
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Correspondence to Vahid Akmali.

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Bagherfard, S., Najafi, N., Gharzi, A. et al. Lack of intraspecific variations of the mitochondrial cytochrome b gene in the greater mouse-tailed bat Rhinopoma microphyllum (Chiroptera: Rhinopomatidae) in Iran. Genetica 149, 37–45 (2021). https://doi.org/10.1007/s10709-020-00109-z

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