Hidden diversity in Senegalese bats and associated findings in the systematics of the family Vespertilionidae

Frontiers in Zoology

Volumn 10, Issue 1, 2013, Pages 1-16

  Koubínová, Darina ^a   Irwin, Nancy ^b   Hulva, Pavel ^a   Koubek, Petr ^c,d   Zima, Jan ^c  

^a CHARLES UNIVERSITY   (Czech Republic)

^b UNIVERSITY OF YORK   (United Kingdom)

^c INSTITUTE OF VERTEBRATE BIOLOGY   (Czech Republic)

^d CZECH UNIVERSITY OF LIFE SCIENCES PRAGUE   (Czech Republic)

Author keywords

DNA; Karyotypes; Phylogenetics; Systematics; Vespertilionidae; Western Africa

Indexed keywords

EPTESICUS; EPTESICUS NASUTUS; GLISCHROPUS TYLOPUS; NYCTICEINOPS SCHLIEFFENI; PIPISTRELLUS; PIPISTRELLUS HESPERIDUS; SCOTOECUS HIRUNDO; VESPERTILIONIDAE;

EID: 84882620318     PISSN: None     EISSN: 17429994     Source Type: Journal    
DOI: 10.1186/1742-9994-10-48     Document Type: Article

References (103)

1. Simmons NB. Order Chiroptera. Mammal species of the world. A taxonomic and geographic reference 2005, 312-529. Baltimore: Johns Hopkins University Press, Wilson DE, Reeder DM, 3.
2. Koopman KF. Chiroptera: systematics. Handbook of zoology. Volume 8, Mammalia (60) 1994, 1-217. Berlin: Walter de Gruyter Press, Niethammer J, Schliemann H, Starck D.
3. Simmons NB, Geisler JH. Phylogenetic relationships of Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx to extant bat lineages, with comments on the evolution of echolocation and foraging strategies in Microchiroptera. Bull Am Mus Nat Hist 1998, 235:1-182.
4. Volleth M, Bronner G, Göpfert MC, Heller K-G, Von Helversen O, Yong H-S. Karyotype comparison and phylogenetic relationships of Pipistrellus-like bats (Vespertilionidae; Chiroptera; Mammalia). Chromosome Res 2001, 9:25-46. 10.1023/A:1026787515840, 11272789.
5. Volleth M, Heller K-G. Phylogenetic relationships of vespertilionid genera (Mammalia: Chiroptera) as revealed by karyological analysis. Z Zool Syst Evolut-forsch 1994, 32:11-34.
6. Zima J, Horáček I. Synopsis of karyotypes of vespertilionid bats (Mammalia: Chiroptera). Acta Univ Carol - Biol 1985, 1981:311-329.
7. Hoofer SR, Van Den Bussche RA. Molecular phylogenetics of the chiropteran family Vespertilionidae. Acta Chiropterol 2003, 5(Suppl):1-63.
8. Lack JB, Roehrs ZP, Stanley CE, Ruedi M, Van Den Bussche RA. Molecular phylogenetics of Myotis indicate familial-level divergence for the genus Cistugo (Chiroptera). J Mammal 2010, 91:976-992.
9. Roehrs ZP, Lack JB, Van Den Bussche RA. A molecular phylogenetic reevaluation of the tribe Nycticeiini (Chiroptera: Vespertilionidae). Acta Chiropterol 2011, 13:17-31.
10. Roehrs ZP, Lack JB, Van Den Bussche RA. Tribal phylogenetic relationships within Vespertilioninae (Chiroptera: Vespertilionidae) based on mitochondrial and nuclear sequence data. J Mammal 2010, 91:1073-1092.
11. Monadjem A, Richards L, Taylor PJ, Stoffberg S. High diversity of pipistrelloid bats (Vespertilionidae: Hypsugo, Neoromicia, and Pipistrellus) in a West African rainforest with the description of a new species. Zool J Linn Soc 2013, 167:191-207.
12. Stadelmann B, Herrera LG, Arroyo-Cabrales J, Flores-Martínez JJ, May BP, Ruedi M. Molecular systematics of the fishing bat Myotis (Pizonyx) vivesi. J Mammal 2004, 85:133-139.
13. Stadelmann B, Jacobs DS, Schoeman C, Ruedi M. Phylogeny of African Myotis bats (Chiroptera, Vespertilionidae) inferred from cytochrome b sequences. Acta Chiropterol 2004, 6:177-192.
14. Stadelmann B, Lin L-K, Kunz TH, Ruedi M. Molecular phylogeny of New World Myotis (Chiroptera, Vespertilionidae) inferred from mitochondrial and nuclear DNA genes. Mol Phylogenet Evol 2007, 43:32-48. 10.1016/j.ympev.2006.06.019, 17049280.
15. Van Cakenberghe V, Seamark ECJ. African Chiroptera Report 2012, 1-5902. Pretoria: AfricanBats, http://www.africanbats.org.
16. Tate GHH. Results of the Archbold expeditions. No. 47. Review of the Vespertilionine bats, with special attention to genera and species of the Archbold collection. Bull Am Mus Nat Hist 1942, 80:221-297.
17. Hill JE, Harrison DL. The baculum in the Vespertilioninae (Chiroptera: Vespertilionidae) with a systematic review, a synopsis of Pipistrellus and Eptesicus, and the descriptions of a new genus and subgenus. Bull Brit Mus Nat Hist Zool 1987, 52:225-305.
18. Kawai K, Nikaido M, Harada M, Matsumura S, Lin L-K, Wu Y, Hasegawa M, Okada N. The status of the Japanese and East Asian bats of the genus Myotis (Vespertilionidae) based on mitochondrial sequences. Mol Phylogenet Evol 2003, 28:297-307. 10.1016/S1055-7903(03)00121-0, 12878466.
19. Frost DR, Timm RM. Phylogeny of plecotine bats (Chiroptera: " 'Vespertilionidae'" ): summary of the evidence and proposal of a logically consistent taxonomy. Am Mus Novit 1992, 3034:1-16.
20. Volleth M, Heller K-G, Fahr J. Phylogenetic relationships of three " Nycticeiini" genera (Vespertilionidae, Chiroptera, Mammalia) as revealed by karyological analysis. Mamm Biol 2006, 71:1-12.
21. Horáček I, Fejfar O, Hulva P. A new genus of vespertilionid bat from Early Miocene of Jebel Zelten, Libya, with comments on Scotophilus, and early history of vespertilionid bats (Chiroptera). Lynx, n.s. 2006, 37:131-150.
22. Hoofer SR, Van Den Bussche RA, Horáček I. Generic status of the American pipistrelles (Vespertilionidae) with description of a new genus. J Mammal 2006, 87:981-992.
23. Von Helversen O, Heller K-G, Mayer F, Nemeth A, Volleth M, Gombkötö P. Cryptic mammalian species: a new species of whiskered bat (Myotis alcathoe n. sp.) in Europe. Naturwissenschaften 2001, 88:217-223. 10.1007/s001140100225, 11482435.
24. Zhang J-S, Han N-J, Jones G, Lin L-K, Zhang J-P, Zhu G-J, Huang D-W, Zhang S-Y. A new species of Barbastella (Chiroptera: Vespertilionidae) from North China. J Mammal 2007, 88:1393-1403.
25. Eger JL, Schlitter DA. A new species of Glauconycteris from West Africa (Chiroptera: Vespertilionidae). Acta Chiropterol 2001, 3:1-10.
26. Goodman SM, Jenkins RKB, Ratrimomanarivo FH. A review of the genus Scotophilus (Mammalia, Chiroptera, Vespertilionidae) on Madagascar, with the description of a new species. Zoosystema 2005, 27:867-882.
27. Kruskop SV, Lavrenchenko LA. A new species of long-eared bat (Plecotus; Vespertilionidae, Mammalia) from Ethiopia. Myotis 2000, 38:5-17.
28. Kouame OML, Jengre N, Kobele M, Knox D, Ahon DB, Gbondo J, Gamys J, Egnankou W, Siaffa D, Okoni-Williams A, Saliou M. Key Biodiversity Areas identification in the Upper Guinea forest biodiversity hotspot. J Threat Taxa 2012, 4:2745-2752.
29. Rosevear DR. The Bats of West Africa 1965, 1-418. United Kingdom: British Museum of Natural History London.
30. Lelant V, Chenaval N. Bilan succinct des espèces de chauves-souris inventoriées au Sénégal lors de la mission de novembre-décembre 2010. Electronic Report 2011, http://storage.canalblog.com/44/45/738905/63677824.pdf.
31. Adam F, Hubert B. Chiroptères nouveaux pour le Sénégal. Mammalia 1972, 36:59-70.
32. Dorst J. A propos de quelques chiroptères du Sénégal, et description d'une forme nouvelle du genre Pipistrellus. Bull Mus Natl Hist Nat 1960, 31:471-474.
33. Verschuren J. XXII. Note sur les cheiroptères du Sénégal, principalement dans les parcs nationaux du Niokolo-Koba et du Delta du Saloum. Mém Inst Fr Afr Noire 1982, 92:307-313.
34. Aellen V. Le Parc National de Niokolo-Koba. II. Chiroptères. Mém Inst Fr Afr Noire 1956, 48A:23-34.
35. Felsenstein J. PHYLIP - Phylogeny Inference Package (Version 3.2). Cladistics 1989, 5:164-166.
36. Baker RJ, Bradley RD. Speciation in mammals and the genetic species concept. J Mammal 2006, 87:643-662. 10.1644/06-MAMM-F-038R2.1, 2771874, 19890476.
37. Mayer F, Dietz C, Kiefer A. Molecular species identification boosts bat diversity. Front Zool 2007, 4:4. 10.1186/1742-9994-4-4, 1802075, 17295921.
38. Kearney TC, Volleth M, Contrafatto G, Taylor PJ. Systematic implications of chromosome GTG-band and bacula morphology for Southern African Eptesicus and Pipistrellus and several other species of Vespertilioninae (Chiroptera: Vespertilionidae). Acta Chiropterol 2002, 4:55-76.
39. Bickham JW, Patton JC, Schlitter DA, Rautenbach IL, Honeycutt RL. Molecular phylogenetics, karyotypic diversity, and partition of the genus Myotis (Chiroptera: Vespertilionidae). Mol Phylogenet Evol 2004, 33:333-338. 10.1016/j.ympev.2004.06.012, 15336668.
40. McBee KM, Schlitter DA, Robbins RL. Systematics of African bats of the genus Eptesicus (Mammalia: Vespertilionidae). 2. Karyotypes of African species and their generic relationships. Ann Carnegie Mus 1987, 56:213-222.
41. Rautenbach IL, Bronner GN, Schlitter DA. Karyotypic data and attendant systematic implications for the bats of southern Africa. Koedoe 1993, 36:87-104.
42. Peterson RL, Nagorsen DW. Chromosomes of fifteen species of bats (Chiroptera) from Kenya and Rhodesia. Roy Ont Mus Life Sci Occ Pap 1975, 27:1-14.
43. Rautenbach IL, Fenton MB. Bats from Mana Pools National Park in Zimbabwe and the first record of Eptesicus rendallii from the country. Z Säugetierk 1992, 57:112-115.
44. Ruedas LA, Lee TE, Bickham JW, Schlitter DA. Chromosomes of five species of vespertilionid bats from Africa. J Mammal 1990, 71:94-100.
45. White TA, Bordewich M, Searle JB. A network approach to study karyotypic evolution: the chromosomal races of the common shrew (Sorex araneus) and house mouse (Mus musculus) as model systems. Syst Biol 2010, 59:262-276. 10.1093/sysbio/syq004, 20525634.
46. Faria R, Navarro A. Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol Evol 2010, 25:660-669. 10.1016/j.tree.2010.07.008, 20817305.
47. Horn A, Basset P, Yannic G, Banaszek A, Borodin PM, Bulatova NS, Jadwiszczak K, Jones RM, Polyakov AV, Ratkiewicz M, Searle JB, Shchipanov NA, Zima J, Hausser J. Chromosomal rearrangements do not seem to affect the gene flow in hybrid zones between karyotypic races of the common shrew (Sorex araneus). Evolution 2012, 66:882-889. 10.1111/j.1558-5646.2011.01478.x, 22380446.
48. Benda P, Hanák V, Andreas M, Reiter A, Uhrin M. Two new species of bats (Chiroptera) for the fauna of Libya: Rhinopoma hardwickii and Pipistrellus rueppellii. Myotis 2004, 41-42:109-124.
49. Veith M, Mucedda M, Kiefer A, Pidinchedda E. On the presence of pipistrelle bats (Pipistrellus and Hypsugo; Chiroptera: Vespertilionidae) in Sardinia. Acta Chiropterol 2011, 13:89-99.
50. Bergsten J. A review of long-branch attraction. Cladistics 2005, 21:163-193.
51. Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755. 10.1093/bioinformatics/17.8.754, 11524383.
52. Roberts A. Descriptions of numerous new subspecies of mammals. Ann Transvaal Mus 1946, 20:303-328.
53. Kearney TC. Systematic revision of southern African species in the genera Eptesicus, Neoromicia, Hypsugo and Pipistrellus (Chiroptera: Vespertilionidae) 2005, 1-580. Durban: PhD thesis. University of Kwa-Zulu-Natal.
54. Roberts A. Preliminary description of fifty-seven new forms of South African mammals. Mainly 38 from Vernay-Lang Kalahari Expedition, 1930. Ann Transvaal Mus 1932, 15:1-19.
55. Kock D. Identity of the African Vespertilio hesperida Temminck 1840 (Mammalia, Chiroptera, Vespertilionidae). Senckenberg Biol 2001, 81:277-283.
56. Porter CA, Primus AW, Hoffmann FG, Baker RJ. Karyology of five species of bats (Vespertilionidae, Hipposideridae, and Nycteridae) from Gabon with comments on the taxonomy of Glauconycteris. Occ Pap Mus Tex Tech Univ 2010, 295:1-7.
57. Lack JB, Van Den Bussche RA. Identifying the confounding factors in resolving phylogenetic relationships in Vespertilionidae. J Mammal 2010, 91:1435-1448.
58. Francis CM, Borisenko AV, Ivanova NV, Eger JL, Lim BK, Guillén-Servent A, Kruskop SV, Mackie I, Hebert PDN. The role of DNA barcodes in understanding and conservation of mammal diversity in Southeast Asia. PLoS ONE 2010, 5:e12575. 10.1371/journal.pone.0012575, 2933245, 20838635.
59. Kingdon J. The Kingdon Field Guide to African Mammals 1997, 478. Princeton: A&C Black Publishers.
60. Csorba G, Son NT, Saveng I, Furey NM. Revealing cryptic bat diversity: three new Murina and redescription of M. tubinaris from Southeast Asia. J Mammal 2011, 92:891-904.
61. Agnarsson I, Zambrana-Torrelio CM, Flores-Saldana NP, May-Collado LJ. A time-calibrated species-level phylogeny of bats (Chiroptera, Mammalia). PLoS Curr 2011, 3. RRN1212.
62. Hanák V, Horáček I. Zur Südgrenze des Areals von Eptesicus nilssoni (Chiroptera: Vespertilionidae). Ann Naturhist Mus Wien 1985, 88:337-388.
63. Clare EL. Cryptic species?. Patterns of maternal and paternal gene flow in eight Neotropical bats. PLoS ONE 2011, 6:e21460.
64. Nesi N, Kadjo B, Pourrut X, Leroy E, Pongombo Shongo C, Cruaud C, Hassanin A. Molecular systematics and phylogeography of the tribe Myonycterini (Mammalia, Pteropodidae) inferred from mitochondrial and nuclear markers. Mol Phylogenet Evol 2013, 66:126-137. 10.1016/j.ympev.2012.09.028, 23063885.
65. DeMenocal PB. African climate change and faunal evolution during the Pliocene-Pleistocene. Earth Planet Sci Lett 2004, 220:3-24.
66. Bonnefille R. Cenozoic vegetation, climate changes and hominid evolution in tropical Africa. Global Planet Change 2010, 72:390-411.
67. Nicolas V, Missoup AD, Denys C, Kerbis Peterhans J, Katuala P, Couloux A, Colyn M. The roles of rivers and Pleistocene refugia in shaping genetic diversity in Praomys misonnei in tropical Africa. J Biogeogr 2011, 38:191-207.
68. Maley J. The African rain forest: main characteristics of changes in vegetation and climate from the Upper Cretaceous to the Quaternary. Proc Roy Soc Edinburgh 1996, 104B:31-73.
69. Lorenzen ED, Masembe C, Arctander P, Siegismund HR. A long-standing Pleistocene refugium in southern Africa and a mosaic of refugia in East Africa: insights from mtDNA and the common eland antelope. J Biogeogr 2010, 37:571-581.
70. Booth AH. The Niger, the Volta and the Dahomey Gap as geographic barriers. Evolution 1958, 12:48-62.
71. Salzmann U, Hoelzmann P. The Dahomey Gap: an abrupt climatically induced rain forest fragmentation in West Africa during the late Holocene. The Holocene 2005, 15:190-199.
72. Booth AH. The Dahomey Gap and the mammalian fauna of the West African Forest. Rev Zool Bot Afr 1954, 50:305-314.
73. Nicolas V, Quérouil S, Verheyen E, Verheyen W, Mboumba JF, Dillen M, Colyn M. Mitochondrial phylogeny of African wood mice, genus Hylomyscus (Rodentia, Muridae): Implications for their taxonomy and biogeography. Mol Phylogenet Evol 2006, 38:779-793. 10.1016/j.ympev.2005.11.024, 16414288.
74. Fuchs J, Crowe TM, Bowie RCK. Phylogeography of the fiscal shrike (Lanius collaris): a novel pattern of genetic structure across the arid zones and savannas of Africa. J Biogeogr 2011, 38:2210-2222.
75. Lorenzen ED, Arctander P, Siegismund HR. Three reciprocally monophyletic mtDNA lineages elucidate the taxonomic status of Grant's gazelles. Conservation Genetics 2008, 9:593-601.
76. Muwanika VB, Nyakaana S, Siegismund HR, Arctander P. Phylogeography and population structure of the common warthog (Phacochoerus africanus) inferred from variation in mitochondrial DNA sequences and microsatellite loci. Heredity 2003, 91:361-372. 10.1038/sj.hdy.6800341, 14512951.
77. Djossa BA, Sinsin BA, Kalko EKV, Fahr J. Inventory of bat species of Niaouli Forest, Bénin, and its bearing on the significance of the Dahomey Gap as a zoogeographic barrier. African Bat Conservation News 2008, 15:4-6.
78. Robbins CB. The Dahomey gap - a reevaluation of its significance as a faunal barrier to West African high forest mammals. Bull Carnegie Mus nat Hist 1978, 6:168-174.
79. Weber N, Kalko EKV, Fahr J. A first assessment of home range and foraging behaviour of the African long-tongued bat Megaloglossus woermanni (Chiroptera: Pteropodidae) in a heterogeneous landscape within the Lama Forest Reserve, Benin. Acta Chiropterol 2009, 11:317-329.
80. Larsen RJ, Knapp MC, Genoways HH, Khan FAA, Larsen PA, Wilson DE, Baker RJ. Genetic Diversity of Neotropical Myotis (Chiroptera: Vespertilionidae) with an Emphasis on South American Species. PLoS ONE 2012, 7:e46578. 10.1371/journal.pone.0046578, 3463536, 23056352.
81. Eaton MJ, Martin A, Thorbjarnarson J, Amato G. Species-level diversification of African dwarf crocodiles (Genus Osteolaemus): A geographic and phylogenetic perspective. Mol Phylogenet Evol 2009, 50:496-506. 10.1016/j.ympev.2008.11.009, 19056500.
82. Hausberger B, Kimpel D, Van Neer A, Korb J. Uncovering cryptic species diversity of a termite community in a West African savanna. Mol Phylogenet Evol 2011, 61:964-969. 10.1016/j.ympev.2011.08.015, 21896335.
83. Vallo P, Benda P, Červený J, Koubek P. Conflicting mitochondrial and nuclear paraphyly in small-sized West African house bats (Vespertilionidae). Zool Scr 2013, 42:1-12.
84. Vallo P, Benda P, Martínková N, Kaňuch P, Kalko EKV, Červený J, Koubek P. Morphologically uniform bats Hipposideros aff. ruber (Hipposideridae) exhibit high mitochondrial genetic diversity in southeastern Senegal. Acta Chiropterol 2011, 13:79-88.
85. Koubínová D, Sreepada KS, Koubek P, Zima J. Karyotypic variation in rhinolophid and hipposiderid bats (Chiroptera: Rhinolophidae, Hipposideridae). Acta Chiropterol 2010, 12:393-400.
86. Barratt EM, Deaville R, Burland TM, Bruford MW, Jones G, Racey PA, Wayne RK. DNA answers the call of pipistrelle bat species. Nature 1997, 387:138-139.
87. Kingston T, Rossiter SJ. Harmonic-hopping in Wallacea's bats. Nature 2004, 429:654-657. 10.1038/nature02487, 15190351.
88. Hulva P, Fornůsková A, Chudárková A, Evin A, Allegrini B, Benda P, Bryja J. Mechanisms of radiation in a bat group from the genus Pipistrellus inferred by phylogeography, demography and population genetics. Mol Ecol 2010, 19:5417-5431. 10.1111/j.1365-294X.2010.04899.x, 21054608.
89. Planiglobe http://www.planiglobe.com.
90. Baker RJ. Karyotypic trends in bats. Biology of Bats. Volume 130 1970, 65-96. New York: Academic Press; 1, Wimsatt WA.
91. Hsu TC, Benirschke K. An Atlas of Mammalian Chromosomes. Volumes 1-10 1967, 1977. Berlin Heidelberg - New York: Springer Verlag.
92. Springer MS, Hollar LJ, Burk A. Compensatory substitutions and the evolution of the mitochondrial 12S rRNA gene in mammals. Mol Biol Evol 1995, 12:1138-1150.
93. Teeling EC, Scally M, Kao DJ, Romagnoli ML, Springer MS, Stanhope MJ. Molecular evidence regarding the origin of echolocation and flight in bats. Nature 2000, 403:188-192. 10.1038/35003188, 10646602.
94. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A. Geneious V5.4 2011, http://www.geneious.com.
95. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002, 30:3059-3066. 10.1093/nar/gkf436, 135756, 12136088.
96. MAFFT version 6 http://mafft.cbrc.jp/alignment/server/.
97. Warnow T. Standard maximum likelihood analyses of alignments with gaps can be statistically inconsistent. PLoS Curr 2012, 4:RRN1308. 3299439,3299439, 22453901.
98. Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 2007, 56:564-577. 10.1080/10635150701472164, 17654362.
99. Nylander JAA. MrModeltest 2.3. Program distributed by the author 2004, Uppsala University: Evolutionary Biology Centre.
100. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690. 10.1093/bioinformatics/btl446, 16928733.
101. Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop: 14 November 2010, 1-8. LA: GCE New Orleans.
102. Pattengale ND, Alipour M, Bininda-Emonds ORP, Moret BME, Stamatakis A. How many bootstrap replicates are necessary?. J Comput Biol 2010, 17:337-354. 10.1089/cmb.2009.0179, 20377449.
103. Degnan JH, Rosenberg NA. Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol Evol 2009, 24:332-340. 10.1016/j.tree.2009.01.009, 19307040.