Skip to main content
SpringerLink
Log in

Comparative cytogenetics of bats (Chiroptera): The prevalence of Robertsonian translocations limits the power of chromosomal characters in resolving interfamily phylogenetic relationships

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Although the monophyly of Chiroptera is well supported by many independent studies, higher-level systematics, e.g. the monophyly of microbats, remains disputed by morphological and molecular studies. Chromosomal rearrangements, as one type of rare genomic changes, have become increasingly popular in phylogenetic studies as alternatives to molecular and other morphological characters. Here, the representatives of families Megadermatidae and Emballonuridae are studied by comparative chromosome painting for the first time. The results have been integrated into published comparative maps, providing an opportunity to assess genome-wide chromosomal homologies between the representatives of eight bat families. Our results further substantiate the wide occurrence of Robertsonian translocations in bats, with the possible involvement of whole-arm reciprocal translocations (WARTs). In order to search for valid cytogenetic signature(s) for each family and superfamily, evolutionary chromosomal rearrangements identified by chromosomal painting and/or banding comparison are subjected to two independent analyses: (1) a cladistic analysis using parsimony and (2) the mapping of these chromosomal changes onto the molecularly defined phylogenetic tree available from the literature. Both analyses clearly indicate the prevalence of homoplasic events that reduce the reliability of chromosomal characters for resolving interfamily relationships in bats.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ao L, Gu X, Feng Q et al. (2006) Karyotype relationships of six bat species (Chiroptera, Vespertilionidae) from China revealed by chromosome painting and G-banding comparison. Cytogenet Genome Res 115: 145–153.

    Article  PubMed  CAS  Google Scholar 

  • Ao L, Mao X, Nie W et al. (2007) Karyotypic evolution and phylogenetic relationships in the order Chiroptera as revealed by G-banding comparison and chromosome painting. Chromosome Res 15: 257–267.

    PubMed  CAS  Google Scholar 

  • Baker RJ, Longmire JL, Maltbie M et al. (1997) DNA synapomorphies for a variety of taxonomic levels from a cosmid library from the New World bat Macrotus waterhousii. Syst Biol 46: 579–589.

    Article  PubMed  CAS  Google Scholar 

  • Baker RJ, Bickham JW (1980) Karyotypic evolution in bats: evidence of extensive and conservative chromosomal evolution in closely related taxa. Syst Zool 29: 239–253.

    Article  Google Scholar 

  • Baker RJ, Bickham JW (1986) Speciation by monobrachial centric fusions. Proc Natl Acad Sci USA 83: 8245–8248.

    Article  PubMed  CAS  Google Scholar 

  • Baker RJ, Bickham JW, Arnold ML (1985) Chromosomal evolution in Rhogeessa (Chiroptera: Vespertilionidae): possible speciation by centric fusions. Evolution 39: 233–243.

    Article  Google Scholar 

  • Barghoorn SF (1997) New material of Vespertiliacus Schlosser (Mammalia, Chiroptera) and suggested relationships of emballonurid bats based on cranial morphology. Amer Mus Novitates 2618: 1–29.

    Google Scholar 

  • Bickham JW (1979) Chromosomal variation and evolutionary relationships of vespertilionid bats. J Mamm 60: 350–363.

    Article  Google Scholar 

  • Borowik OA (1995) Coding chromosomal data for phylogenetic analysis: phylogenetic resolution of the Pan-Homo-Gorilla trichotomy. Syst Biol 44: 563–570.

    Article  Google Scholar 

  • Britton-Davidian J, Catalan J, da Graca Ramalhinho M et al. (2005) Chromosomal phylogeny of Robertsonian races of the house mouse on the island of Madeira: testing between alternative mutational process. Genet Res 86: 171–183.

    Article  PubMed  CAS  Google Scholar 

  • Catalan J, Auffray JC, Pellestor D, Britton-Davidian J (2000) Spontaneous occurrence of a Robertsonian fusion involving chromosome 19 by single whole-arm reciprocal translocation (WART) in wild derived house mice. Chromosome Res 8: 593–601.

    Article  PubMed  CAS  Google Scholar 

  • Dobigny G, Ducroz JF, Robinson TJ, Volobouev V (2004) Cytogenetics and cladistics. Syst Biol 53: 470–484.

    Article  PubMed  Google Scholar 

  • Eick GN, Jacobs DS, Matthee CA (2005) A nuclear DNA phylogenetic perspective on the evolution of echolocation and historical biogeography of extant bats (Chiroptera). Mol Biol Evol 22: 1869–1886.

    Article  PubMed  CAS  Google Scholar 

  • Fredga K (1996) The chromosome races of Sorex araneus in Scandinavia. Hereditas 125: 123–135.

    Article  Google Scholar 

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

    Google Scholar 

  • Gunnel GF, Simmons NB (2005) Fossil evidence and the origin of bats. J Mamm Evol 12: 209–246.

    Article  Google Scholar 

  • Haiduk MW, Baker RJ, Robbins LW, Schlitter DA (1981) Chromosomal evolution in African Megachiroptera: 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 

  • Harada M, Minezana M, Takada S, Yenbutra S, Nunpakdee P, Ohtani S (1982) Karyological analysis of 12 species of bats from Thailand. Caryologia 35: 269–278.

    Google Scholar 

  • Hauffe HC, Piálek J (1997) Evolution of the chromosomal races of Mus musculus domesticus in the Rhaetian Alps: the roles of whole-arm reciprocal translocation and zonal raciation. Biol J Linn Soc 62: 255–278.

    Google Scholar 

  • Hood CS, Baker RJ (1986) G- and C-band chromosome studies of bats of the family Emballonuridae. J Mammal 67: 705–711.

    Article  Google Scholar 

  • Hood JS, Schlitter DA, Georgudaki JI, Yenbutra S, Baker RJ (1988) Chromosomal studies of bats (Mammalia:Chiroptera) from Thailand. Ann Carnegie Mus 57: 99–109.

    Google Scholar 

  • Hill JE (1974) A new family, genus, and species of bat (Mammalia: Chiroptera) from Thailand. Bull British Mus (Nat. Hist.) 27: 301–336.

    Google Scholar 

  • Hulva P, Horácek I (2002) Craseonycteris thonglongyai (Chiroptera: Craseonycteridae) is a rhinolophoid: molecular evidence from cytochrome b. Acta Chiropterol 4: 107–120.

    Google Scholar 

  • Hutcheon JM, Kirsch JAW (2004) Camping in a different tree: results of molecular systematic studies of bats using DNA-DNA hybridization. J Mammal Evol 11: 17–47.

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jones G, Teeling EC (2006) The evolution of echolocation in bats. Trends Ecol Evol 21: 149–156.

    Article  PubMed  Google Scholar 

  • Jones KE, Purvis A, MacLarnon A, Bininda-Emonds ORP, Simmons NB (2002) A phylogenetic supertree of the bats (Mammalia: Chiroptera). Biol Rev 77: 223–259.

    Article  PubMed  Google Scholar 

  • Kasahara S, Dutrillaux B (1983) Chromosome banding patterns of four species of bats, with special reference to a case of X-autosome translocation. Ann Genet 26: 197–201.

    PubMed  CAS  Google Scholar 

  • King M (1993) Species Evolution: The Role of Chromosome Change. London: Cambridge University Press.

    Google Scholar 

  • Koopman KF (1994) Chiroptera: Systematics. In: Niethammer J, Schliemann H, Starck D, eds. Handbook of Zoology, vol. 8. Berlin: Walter de Gruyter Press, pp. 1–217.

    Google Scholar 

  • Li T, O’Brien PC, Biltueva L et al. (2004) Evolution of genome organizations of squirrels (Sciuridae) revealed by cross-species chromosome painting. Chromosome Res 12: 317–335.

    Article  PubMed  Google Scholar 

  • Liu FGR, Miyamoto MM (1999) A phylogenetic assessment of molecular and morphological data for eutherian mammals. Syst Biol 48: 54–64.

    Article  PubMed  CAS  Google Scholar 

  • Mao X, Nie W, Wang J et al. (2007a) Karyotype evolution in Rhinolophus bats (Rhinolophidae, Chiroptera) illuminated by cross-species chromosome painting and G-banding comparison. Chromosome Res 15: 835-848.

    Article  CAS  Google Scholar 

  • Mao X, Wang J, Su W et al. (2007b) The G- and C- banded karyotypes of four species of bats from China. Chin J Zool 42: 33-40.

    Google Scholar 

  • Miller GS (1907) The families and genera of bats. US Natl Mus Bull 57: 1–282.

    Google Scholar 

  • Müller S, Hollatz M, Wienberg J (2003) Chromosomal phylogeny and evolution of gibbons (Hylobatidae). Hum Genet 113: 493–501.

    Article  PubMed  Google Scholar 

  • Murphy WJ, Eizirkik E, O’Brien SJ et al. (2001) Resolution of the early placental mammalian radiation using Bayesian phylogenetics. Science 294: 2348–2352.

    Article  PubMed  CAS  Google Scholar 

  • Nachman MW, Boyer SN, Searle JB, Aquadro CF (1994) Mitochondrial DNA variation and the evolution of Robertsonian chromosomal races of house mice, Mus domesticus. Genetics 136: 1105–1120.

    PubMed  CAS  Google Scholar 

  • Neusser M, Stanyon R, Bigoni F, Wienberg J, Müller S (2001) Molecular cytotaxonomy of New World monkeys (Platyrrhini)—comparative analysis of five species by multi-color chromosome painting gives evidence for a classification of Callimico goeldii within the family of Callitrichidae. Cytogenet Cell Genet 94: 206–215.

    Article  PubMed  CAS  Google Scholar 

  • Nie W, Wang J, O’Brien PCM et al. (2002) The genome phylogeny of domestic cat, red panda and five mustelid species revealed by comparative chromosome painting and G-banding. Chromosome Res 10: 209–222.

    Article  PubMed  CAS  Google Scholar 

  • Pieczarka JC, Nagamachi CY, O’Brien PCM et al. (2005) Reciprocal chromosome painting between two South American bats: Carollia brevicauda and Phyllostomus hastatus (Phyllostomidae, Chiroptera). Chromosome Res 13: 339–347.

    Article  PubMed  CAS  Google Scholar 

  • Porter CA, Goodman M, Stanhope MJ (1996) Evidence on mammalian phylogeny from sequences of exon 28 of the von Willebrand factor gene. Mol Phylogent Evol 5: 89–101.

    Article  CAS  Google Scholar 

  • Qumsiyeh MB, Baker RJ (1985) G- and C-banded karyotypes of the Rhinopomatidae (Microchiroptera). J Mammal 66: 541–544.

    Article  Google Scholar 

  • Ray-Chaudhuri SP, Pathak S, Sharma T (1971) Karyotypes of five Indian species of Microchiroptera. Caryologia 24: 239–245.

    Google Scholar 

  • Rokas A, Holland PWH (2000) Rare genomic changes as a tool for the phylogenetic a tool for phylogenetics. Trends Evol 11: 454–459.

    Article  Google Scholar 

  • Scherthan H, Cremer T, Arnason U, Weier HU, Lima-de-Faria A, Fronicke L (1994) Comparative chromosome painting discloses homologous segments in distantly related mammals. Nat Genet 6: 342–347.

    Article  PubMed  CAS  Google Scholar 

  • Seabright M (1971) A rapid staining technique for human chromosomes. Lancet 2: 971–972.

    Article  PubMed  CAS  Google Scholar 

  • Searle JB (1993) Chromosomal hybrid zones in eutherian mammals. In: Harrison RG, ed. Hybrid Zones and the Evolutionary Process. Oxford: Oxford University Press, pp. 309–353.

    Google Scholar 

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

    Google Scholar 

  • Simmons NB (2000) Bat phylogeny: an evolutionary context for comparative studies. In: Adams RA, Pedersen CS, eds. Ontogeny, Functional Ecology, and Evolution of Bats. Cambridge: Cambridge University Press, pp. 9–58.

    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, vol. 1. Baltimore, MD: Johns Hopkins University Press, pp. 312–529.

    Google Scholar 

  • Simmons NB, Geisler JH (1998) Phylogenetic relationships of Icaronycteris, Archaconycteris, Hassianycteris and Palaeochiroptera to extant bat lineages, with comments on the evolution of echolocation and foraging strategies in Michrochiroptera. Bull Am Mus Nat Hist 235: 1–182.

    Google Scholar 

  • Smith JD (1972) Systematics of the Chiroptera family Mormoopidae. Miscellaneous Publication, University of Kansas, Museum of Natural History 56: 1–132.

  • Smith JD (1976) Chiropteran evolution. In: Baker RJ, Jones JK, Carter DC, eds. Biology of the Bats of the New World Family Phyllostomatidae, vol. I. pp. 46–69. [Special Publications, Museum of Texas Tech University 10: 1–218].

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

    Article  Google Scholar 

  • Swofford DL (1998) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Sunderland, MA: Sinauer Associates.

    Google Scholar 

  • Teeling EC, Scally M, Kao D, Romagnoli ML, Springer MS, Tanhope 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 

  • Teeling, EC, Madsen O, Murphy WJ, Springer MS, O’Brien SJ (2003) Nuclear gene sequences confirm an ancient link between New Zealand’s short-tailed bat and South American noctilionoid bats. Mol Phylogenet Evol 28: 308–319.

    Article  PubMed  CAS  Google Scholar 

  • Teeling EC, Springer MS, Madsen O, Bates P, O’Brien SJ, Murphy WJ (2005) A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307: 580–584.

    Article  PubMed  CAS  Google Scholar 

  • Telenius H, Pelmear AH, Tunnacliffe A et al. (1992) Cytogenetic analysis by chromosome painting using DOP-PCR amplified flow-sorted chromosomes. Genes Chromosomes Cancer 4: 257–263.

    Article  PubMed  CAS  Google Scholar 

  • Van Den Bussche RA, Hoofer SR (2004) Phylogenetic relationships among recent chiropteran families and the importance of choosing appropriate out-group taxa. J Mammal 85: 321–330.

    Article  Google Scholar 

  • Van Valen L (1979) The evolution of bats. Evol Theory 4: 104–121.

    Google Scholar 

  • Veyrunes F, Watson J, Robinson TJ, Britton-Davidian J (2007) Accumulation of rare sex chromosome rearrangements in the African pygmy mouse, Mus (Nannomys) minutoides: a whole-arm reciprocal translocation (WART) involving an X-autosome fusion. Chromosome Res 15: 223–230.

    Article  PubMed  CAS  Google Scholar 

  • Volleth M, Heller KG (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, Heller KG, Pfeiffer RA, Hameister H (2002) A comparative ZOO-FISH analysis in bats elucidates the phylogenetic relationships between Megachiroptera and five microchiroptera families. Chromosome Res 10: 477–497.

    Article  PubMed  CAS  Google Scholar 

  • Warner JW, Patton JL, Gradner AL, Baker RJ (1974) Karyotypic analysis of twenty-one species of molossid bats (Molossidae: Chiroptera). Can J Genet Cytol 16: 165–174.

    PubMed  CAS  Google Scholar 

  • Winking (1986) Some aspects of Robertsonian variation in European wild mice. Curr Top Microbiol Immunol 127: 68–74.

    PubMed  CAS  Google Scholar 

  • Yang F, Carter NP, Shi L, Ferguson-Smith MA (1995) A comparative study of karyotypes of muntjacs by chromosome painting. Chromosoma 103: 642–652.

    Article  PubMed  CAS  Google Scholar 

  • Yang F, Müller S, Just R, Ferguson-Smith MA, Wienberg J (1997) Comparative chromosome painting in mammals: human and the Indian muntjac (Muntiacus muntjak vaginalis). Genomics 39: 396–401.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yang F, Fu B, O’Brien PCM, Nie W, Ryder OA, Ferguson-Smith MA (2004) Refined genome-wide comparative map of the domestic horse, donkey and human based on cross-species chromosome painting: insight into the occasional fertility of mules. Chromosome Res 12: 65–76.

    Article  PubMed  CAS  Google Scholar 

  • Yang F, Graphodatsky AS, Li T et al. (2006) Comparative genome maps of the pangolin, hedgehog, sloth, anteater and human revealed by cross-species chromosome painting: further insight into the ancestral karyotype and genome evolution of eutherian mammals. Chromosome Res 14: 283–296.

    Article  PubMed  CAS  Google Scholar 

  • Yong HS (1984) Robertsonian translocation, pericentric inversion and heterochromatin block in the evolution of the Tailless Fruit Bat. Experientia 40: 875–876.

    Article  Google Scholar 

  • Zhang W (1985) A study on the karyotypes in four species of bat (Rhinolophus). Acta Theriol Sin 5: 95–101.

    Google Scholar 

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

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Kunming, Yunnan, PR China

    Xiuguang Mao, Wenhui Nie, Jinhuan Wang, Weiting Su, Qing Feng & Yingxiang Wang

  2. The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, CB10 1SA, UK

    Fengtang Yang

  3. Institut de Recherche pour le Développement, Centre de Biologie pour la Gestion des Populations, Campus de Baillarguet, CS3016, 34988, Montferrier-sur-Lez, France

    Gauthier Dobigny

  4. The Graduate School of the Chinese Academy of Sciences, Beijing, PR China

    Xiuguang Mao

Authors
  1. Xiuguang Mao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wenhui Nie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jinhuan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Weiting Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qing Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yingxiang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gauthier Dobigny
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Fengtang Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Gauthier Dobigny or Fengtang Yang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mao, X., Nie, W., Wang, J. et al. Comparative cytogenetics of bats (Chiroptera): The prevalence of Robertsonian translocations limits the power of chromosomal characters in resolving interfamily phylogenetic relationships. Chromosome Res 16, 155–170 (2008). https://doi.org/10.1007/s10577-007-1206-2

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-007-1206-2

Key words

Search

Navigation