Skip to main content
Log in

A comparative ZOO-FISH analysis in bats elucidates the phylogenetic relationships between Megachiroptera and five microchiropteran families

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Fluorescence in-situ hybridization with human whole chromosome painting probes (WCPs) was applied to compare the karyotypes of members of five bat families. Twenty-five evolutionarily conserved units (ECUs) were identified by ZOO-FISH analysis. In 10 of these 25 ECUs, thorough GTG-band comparison revealed an identical banding pattern in all families studied. Differences in the remaining ECUs were used as characters to judge the phylogenetic relationships within Chiroptera. Close relations hips were found between Rhinolophidae and Hipposideridae. Also closely related are the representatives of the yangochiropteran families Phyllostomidae (genus studied: Glossophaga, Volleth et al. 1999), Molossidae and Vespertilionidae. All microchiropteran species studied here share four common features not found in the megachiropteran species Eonycteris spelaea. Two of these are considered as derived characters with a high probability of parallel evolution. On the other hand, Eonycteris shares one common, probably derived feature with the rhinolophoid families Rhinolophidae and Hipposideridae and an additional one only with Hipposideridae. At the moment, the relationships between Yangochiroptera, Rhinolophoidea and Megachiroptera must be left in an unsolved trichotomy. Comparison of neighboring segment combinations found in Chiroptera with those found in other mammalian taxa revealed six synapomorphic features for Chiroptera. Therefore, for karyological reasons, monophyly of Chiroptera is strongly supported.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Baker RJ, Bass RA (1979) Evolutionary relationships of the Phyllonycterinae to the glossophagine genera Glossophaga and Monophyllus. J Mammal 60: 364-372.

    Google Scholar 

  • Baker RJ, Honeycutt RL, Bass RA (1988) Genetics. In: Greenhall AM, Schmidt U, eds. Natural History of Vampire Bats. Boca Raton, Florida: CRC Press, pp 31-40.

    Google Scholar 

  • Baker RJ, Hood CS, Honeycutt RL (1989) Phylogenetic relationships and classification of the higher categories of the New World bat family Phyllostomidae. Syst Zool 38: 228-238.

    Article  Google Scholar 

  • Bickham JW (1979) Banded karyotypes of 11 species of American bats (genus Myotis). Cytologia 44: 789-797.

    PubMed  CAS  Google Scholar 

  • Bielec PE, Gallagher DS, Womack JE, Busbee DL (1998) Homologies between human and dolphin chromosomes detected by heterologous chromosome painting. Cytogenet Cell Genet 81: 18-25.

    Article  PubMed  CAS  Google Scholar 

  • Cavagna P, Menotti A, Stanyon R (2000) Genomic homology of the domestic ferret with cats and humans. Mammalian Genome 11: 866-870.

    Article  PubMed  CAS  Google Scholar 

  • Chowdhary BP, Raudsepp T, Frönicke L, Scherthan H (1998) Emerging patterns of comparative genome organization in some mammalian species as revealed by Zoo-FISH. Genome Res 8: 577-589.

    PubMed  CAS  Google Scholar 

  • Dixkens C, Klett C, Bruch J, et al. (1998) ZOO-FISH analysis in insectivores: “Evolution extols the virtue of the status quo”. Cytogenet Cell Genet 80: 61-67.

    Article  PubMed  CAS  Google Scholar 

  • Ellerman JR, Morrison-Scott TCS (1966) Checklist of Palaearctic and Indian Mammals. London: British Museum (Natural History), pp 810.

    Google Scholar 

  • Frönicke L, Scherthan H (1997) Zoo-fluorescence in situ hybridization analysis of human and Indian muntjac karyotypes (Muntiakus muntjak vaginalis) reveals satellite DNA clusters at the margins of conserved syntenic segments. Chromosome Res 5: 254-261.

    Article  PubMed  Google Scholar 

  • Frönicke L, Wienberg J (2001) Comparative chromosome painting defines the high rate of karyotype changes between pigs and bovids. Mammalian Genome 12: 442-449.

    Article  PubMed  CAS  Google Scholar 

  • Frönicke L, Chowdhary BP, Scherthan H, Gustavsson I (1996) A comparative map of the porcine and human genomes demonstrates ZOO-FISH and gene mapping-based chromosomal homologies. Mammalian Genome 7: 285-290.

    Article  PubMed  Google Scholar 

  • Frönicke L, Müller-Navia J, Romanakis K, Scherthan H(1997) Chromosomal homeologies between human, harbor seal (Phoca vitulina) and the putative ancestral carnivore karyotype revealed by Zoo-FISH. Chromosoma 106: 108-113.

    Article  PubMed  Google Scholar 

  • Göbbel L (2000) The external nasal cartilages in Chiroptera: significance for infraordinal relationships. J Mammal Evol 7: 167-201.

    Article  Google Scholar 

  • Goureau A, Yerle M, Schmitz A et al. (1996) Human and porcine correspondence of chromosome segments using bidirectional chromosome painting. Genomics 36: 252-262.

    Article  PubMed  CAS  Google Scholar 

  • Graphodatsky AS, Yang F, Serdukova N, Perelman P, Zhdanova NS, Ferguson-Smith MA (2000) Dog chromosome-specific paints reveal evolutionary inter-and intrachromosomal rearrangements in the American mink and human. Cytogenet Cell Genet 90: 275-278.

    Article  PubMed  CAS  Google Scholar 

  • Gray JE (1821) On the natural arrangement of vertebrose animals. London Med Reposit 15: 296-310.

    Google Scholar 

  • Haiduk MW, Baker RJ, Robbins LW, Schlitter DA (1981) Chromosomal evolution in AfricanMegachiroptera: G-band and C-band assessment of the magnitude of change in similar standard karyotypes. Cytogenet Cell Genet 29: 221-232.

    PubMed  CAS  Google Scholar 

  • Haig D (1999) A brief history of human autosomes. Phil Trans R Soc Lond B 354: 1447-1470.

    Article  CAS  Google Scholar 

  • Hameister H, Klett C, Bruch J, Dixkens C, Vogel W, Christensen K (1997): Zoo-FISH analysis: the American mink (Mustela vison) closely resembles the cat karyotype. Chromosome Res 5: 5-11.

    Article  PubMed  CAS  Google Scholar 

  • Harada M (1982) Karyological study of the Bonin flying fox (Pteropus pselaphon). Conservation Report of the Minami-Iwojima Wilderness Area, Tokyo, Japan. Nature Conservation Bureau, Environment Agency of Japan, pp 243-248.

  • Hayes H (1995) Chromosome painting with human chromosome-specific DNA libraries reveals the extent and distribution of conserved segments in bovine chromosomes. Cytogenet Cell Genet 71: 168-174.

    PubMed  CAS  Google Scholar 

  • Hutcheon JM, Kirsch JAW, Pettigrew JD (1998) Base compositional biases and the bat problem. III. The question of microchiropteran monophyly. Phil Trans R Soc Lond B 353: 607-617.

    Article  CAS  Google Scholar 

  • Koopman KF (1984) Bats. In: S Anderson, JK Jones, eds. Orders and Families of Recent Mammals of the World. New York: Wiley, pp 145-186.

    Google Scholar 

  • Koopman KF (1985) A synopsis of the families of bats, part VII. Bat Res News 25: 25-29.

    Google Scholar 

  • Korstanje R, O'Brien PCM, Yang F et al. (1999) Complete homology maps of the rabbit (Oryctolagus cuniculus) and human by reciprocal chromosome painting. Cytogenet Cell Genet 86: 317-322.

    Article  PubMed  CAS  Google Scholar 

  • Madsen O, Scally M, Douady CJ et al. (2001) Parallel adaptive radiations in two major clades of placental mammals. Nature 409: 610-614.

    Article  PubMed  CAS  Google Scholar 

  • Miller GS (1907) The Families and Genera of Bats. Washington, DC: Smithsonian Institution, 1-282.

    Google Scholar 

  • Mindell DP, Dick CW, Baker RJ (1991) Phylogenetic relationships among megabats, microbats and primates. Proc Natl Acad Sci USA 88: 10322-10326.

    Article  PubMed  CAS  Google Scholar 

  • Müller S, Stanyon R, O'Brien PCM, Ferguson-Smith MA, Plesker R, Wienberg J (1999) Defining the ancestral karyotype of all primates by multidirectional chromosome painting between tree shrews, lemurs and humans. Chromosoma 108: 393-400.

    Article  PubMed  Google Scholar 

  • Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O'Brien SJ (2001) Molecular phylogenetics and the origin of placental mammals. Nature 409: 614-618.

    Article  PubMed  CAS  Google Scholar 

  • Narita Y, Oda SI, Takenaka O, Kageyama T (2001) Phylogenetic position of Eulipotyphla inferred from the cDNA sequences of pepsinogens A and C. Mol Phyl Evol 21: 32-42.

    Article  CAS  Google Scholar 

  • Nash WG, Wienberg J, Ferguson-Smith MA, Menninger JC, O'Brien SJ (1998) Comparative genomics: tracking chromosome evolution in the family Ursidae using reciprocal chromosome painting. Cytogenet Cell Genet 83: 182-192.

    Article  PubMed  CAS  Google Scholar 

  • Nikaido M, Harada M, Cao Y, Hasegawa M, Okada N (2000) Monophyletic origin of the order Chiroptera and its phylogenetic position among Mammalia, as inferred from the complete sequence of the mitochondrial DNA of a Japanese megabat, the Ryukyu flying fox (Pteropus dasymallus). J Mol Evol 51: 318-328.

    PubMed  CAS  Google Scholar 

  • Nikaido M, Kawai K, Cao Y et al. (2001) Maximum likelihood analysis of the complete mitochondrial genomes of eutherians and a reevaluation of the phylogeny of bats and insectivores. J Mol Evol 53: 508-516.

    Article  PubMed  CAS  Google Scholar 

  • Novacek MJ (1992) Mammalian phylogeny: shaking the tree. Nature 356: 121-125.

    Article  PubMed  CAS  Google Scholar 

  • O'Brien SJ, Womack JE, Lyon LA, Moore KJ, Jenkins NA, Copeland NG (1993) Anchored reference loci for comparative genomemapping in mammals. Nature Genet 3: 103-112.

    Article  PubMed  Google Scholar 

  • O'Brien SJ, Menotti-Ramond M, Murphy WJ et al. (1999) The promise of comparative cytogenetics in mammals. Science 286: 458-480.

    Article  PubMed  Google Scholar 

  • Onuma M, Cao Y, Hasegawa M, Kusakabe S (2000) A close relationship of Chiroptera with Eulipotyphla (core Insectivora) suggested by four mitochondrial genes. Zool Sci (Tokyo) 17: 1327-1332.

    CAS  Google Scholar 

  • Patton, JC, Baker RJ (1978) Chromosomal homology and evolution of phyllostomatoid bats. Syst Zool 27: 449-462.

    Article  Google Scholar 

  • Pettigrew JD (1986) Flying primates? Megabats have the advanced pathway from eye to midbrain. Science 231: 1304-1306.

    PubMed  CAS  Google Scholar 

  • Pettigrew JD, Jamieson BGM, Robson SK, Hall LS, Mcanally KI, Cooper HM (1989) Phylogenetic relations between microbats, megabats and primates (Mammalia: Chiroptera and Primates). Phil Trans R Soc Lond B 325: 489-559.

    CAS  Google Scholar 

  • Qumsiyeh MB, Owen RD, Chesser RK (1988) Differential rates of genic and chromosomal evolution in bats of the family Rhinolophidae. Genome 30: 326-335.

    PubMed  CAS  Google Scholar 

  • Raudsepp T, Frönicke L, Scherthan H, Gustavsson I, Chowdhary BP (1996) Zoo-FISH delineates conserved chromosomal segments in horse and man. Chromosome Res 4: 218-225.

    Article  PubMed  CAS  Google Scholar 

  • Rettenberger G, Klett C, Zechner U et al. (1995) ZOO-FISH analysis: cat and human karyotypes closely resemble the putative ancestral mammalian karyotype. Chromosome Res 3: 479-486.

    Article  PubMed  CAS  Google Scholar 

  • Richard F, Lombard M, Dutrillaux B (2000) Phylogenetic origin of human chromosomes 7, 16, and 19 and their homologs in placental mammals. Genome Res 10: 644-651.

    Article  PubMed  CAS  Google Scholar 

  • Richard F, Messaoudi C, Lombard M, Dutrillaux B (2001) Chromosome homologies between man and mountain zebra (Equus zebra hartmannae) and description of a new ancestral synteny involving sequences homologous to human chromosomes 4 and 8. Cytogenet Cell Genet 93: 291-296.

    Article  PubMed  CAS  Google Scholar 

  • Rokas A, Holland PWH (2000) Rare genomic changes as a tool for phylogenetics. Trends Ecol Phylogenet 15: 454-459.

    Google Scholar 

  • Seabright M (1971) A rapid staining technique for human chromosomes. Lancet II: 971-972.

    Article  Google Scholar 

  • Simmons NB (1998) A reappraissal of interfamilial relationships of bats. In: TH Kunz, PA Racey, eds. Bat Biology and Conservation. Washington, London: Smithsonian Inst. Press, pp 3-26.

    Google Scholar 

  • Simmons NB, Geisler JH (1998) 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 235: 1-182.

    Google Scholar 

  • Springer MS, Teeling EC, Madsen O, Stanhope M, de Jong WW(2001a) Integrated fossil and molecular data reconstruct bat echolocation. Proc Natl Acad Sci USA 98: 6241-6246.

    Article  PubMed  CAS  Google Scholar 

  • Springer MS, Teeling E, Stanhope MJ (2001b) External nasal cartilages in bats: evidence for chiropteran monophyly? J Mammal Evol 8: 231-236.

    Article  Google Scholar 

  • Sreepada KS, Naidu KN, Gururaj ME (1993) Trends of karyotypic evolution in the genus Hipposideros (Chiroptera: Mammalia). Cytobios 75: 49-57.

    PubMed  CAS  Google Scholar 

  • Teeling E, Scally M, Kao D, Romagnoli ML, Springer MS, Stanhope MJ (2000) Molecular evidence regarding the origin of echolocation and flight in bats. Nature 403: 188-192.

    Article  PubMed  CAS  Google Scholar 

  • Teeling EC, Madsen O, van den Bussche RA, de Jong WW, Stanhope MJ, Springer MS (2002) Microbat paraphyly and the convergent evolution of a key innovation in Old World rhinolophoid microbats. Proc Natl Acad Sci USA 99: 1431-1436.

    Article  PubMed  CAS  Google Scholar 

  • Van den Bussche RA, Hoofer SR (2001) Evaluating monophyly of Nataloidea (Chiroptera) with mitochondrial DNA sequences. J Mammal 82: 320-327.

    Article  Google Scholar 

  • Volleth M (1987) Differences in the location of nucleolus organizer regions in European vespertilionid bats. Cytogenet Cell Gen 44: 186-197.

    Article  CAS  Google Scholar 

  • Volleth M (1989) Karyotypevolution und Phylogenie der Vespertilionidae (Mammalia: Chiroptera). PhD Dissertation, Erlangen, 1-262.

  • Volleth M, Heller K-G (1994) Phylogenetic relationships of vespertilionid genera (Mammalia: Chiroptera) as revealed by karyological analysis. Zool Syst Evolut-forsch 32: 11-34.

    Article  Google Scholar 

  • Volleth M, Klett C, Kollak A et al. (1999) ZOO-FISH analysis in a species of the order Chiroptera: Glossophaga soricina (Phyllostomidae). Chromosome Res 7: 57-64.

    Article  PubMed  CAS  Google Scholar 

  • Volleth M, Bronner G, Göpfert MC, Heller K-G, von Helversen O, Yong HS (2001) Karyotype comparison and phylogenetic relationships of Pipistrellus-like bats (Vespertilionidae; Chiroptera; Mammalia). Chromosome Res 9: 25-46.

    Article  PubMed  CAS  Google Scholar 

  • Wadell PJ, Cao Y, Hauf J, Hasegawa M (1999) Using novel phylogenetic methods to evaluate mammalian mtDNA, including amino acid-invariant sites-logDet plus site stripping, to detect internal conflicts in the data, with special reference to the position of hedgehog, armadillo, and elephant. Syst Biol 48: 31-53.

    Article  Google Scholar 

  • Wienberg J, Stanyon R, Nash WG et al. (1997) Conservation of human vs. feline genome organization revealed by reciprocal chromosome painting. Cytogenet Cell Genet 77: 211-217.

    PubMed  CAS  Google Scholar 

  • Yang F, O'Brien PCM, Milne BS et al. (1999) A complete chromosome map for the dog, red fox, and human and its integration with canine genetic maps. Genomics 62: 189-202.

    Article  PubMed  CAS  Google Scholar 

  • Yang F, Graphodatsky AS, O'Brien PCM et al. (2000) Reciprocal chromosome painting illuminates the history of genome evolution of the domestic cat, dog and human. Chromosome Res 8: 393-404.

    Article  PubMed  CAS  Google Scholar 

  • Zima J, Volleth M, Horácek I et al. (1992) Comparative karyology of rhinolophid bats. In: I Horácek, V Vorhalik, eds. Prague Studies in Mammalogy. Prague: Charles University Press, pp 229-236.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Volleth, M., Heller, KG., Pfeiffer, R. et al. A comparative ZOO-FISH analysis in bats elucidates the phylogenetic relationships between Megachiroptera and five microchiropteran families. Chromosome Res 10, 477–497 (2002). https://doi.org/10.1023/A:1020992330679

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1020992330679

Navigation