Advertisement

Chromosome Research

, Volume 18, Issue 6, pp 635–653 | Cite as

Cross-species chromosome painting in bats from Madagascar: the contribution of Myzopodidae to revealing ancestral syntenies in Chiroptera

  • Leigh R. Richards
  • Ramugondo V. Rambau
  • Jennifer M. Lamb
  • Peter J. Taylor
  • Fengtang Yang
  • M. Corrie Schoeman
  • Steven M. Goodman
Article

Abstract

The chiropteran fauna of Madagascar comprises eight of the 19 recognized families of bats, including the endemic Myzopodidae. While recent systematic studies of Malagasy bats have contributed to our understanding of the morphological and genetic diversity of the island’s fauna, little is known about their cytosystematics. Here we investigate karyotypic relationships among four species, representing four families of Chiroptera endemic to the Malagasy region using cross-species chromosome painting with painting probes of Myotis myotis: Myzopodidae (Myzopoda aurita, 2n = 26), Molossidae (Mormopterus jugularis, 2n = 48), Miniopteridae (Miniopterus griveaudi, 2n = 46), and Vespertilionidae (Myotis goudoti, 2n = 44). This study represents the first time a member of the family Myzopodidae has been investigated using chromosome painting. Painting probes of M. myotis were used to delimit 29, 24, 23, and 22 homologous chromosomal segments in the genomes of M. aurita, M. jugularis, M. griveaudi, and M. goudoti, respectively. Comparison of GTG-banded homologous chromosomes/chromosomal segments among the four species revealed the genome of M. aurita has been structured through 14 fusions of chromosomes and chromosomal segments of M. myotis chromosomes leading to a karyotype consisting solely of bi-armed chromosomes. In addition, chromosome painting revealed a novel X-autosome translocation in M. aurita. Comparison of our results with published chromosome maps provided further evidence for karyotypic conservatism within the genera Mormopterus, Miniopterus, and Myotis. Mapping of chromosomal rearrangements onto a molecular consensus phylogeny revealed ancestral syntenies shared between Myzopoda and other bat species of the infraorders Pteropodiformes and Vespertilioniformes. Our study provides further evidence for the involvement of Robertsonian (Rb) translocations and fusions/fissions in chromosomal evolution within Chiroptera.

Keywords

Chiroptera Madagascar Myzopoda chromosome painting karyotypic evolution 

Abbreviations

CBG-banding

C-banding by treatment with barium hydroxide

GTG-banding

G-banding by trypsin digestion

IHB

Intercalary heterochromatic block

MAU

Myzopoda aurita

MGO

Myotis goudoti

MGR

Miniopterus griveaudi

MJU

Mormopterus jugularis

MMY

Myotis myotis

Rb

Robertsonian

X-A

X-autosome translocation

Zoo-FISH

Zoo-fluorescence in situ hybridization

Notes

Acknowledgments

This study was supported by grants awarded by the John D. and Catherine T. MacArthur Foundation (to SMG), Volkswagen Foundation (to SMG, PJT and JML), South African National Research Foundation (to RVR, LRR), and the South African Biosystematics Initiative (to JML). FY is supported by the Wellcome Trust. We thank F. Ratrimomanarivo, C. Maminirina, and B. Ramasindrazana for their assistance with fieldwork and specimen collection.

References

  1. 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 115:145–153CrossRefPubMedGoogle Scholar
  2. 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 15:257–267PubMedGoogle Scholar
  3. Baker RJ, Jordan RG (1970) Chromosomal studies of some neotropical bats of the families Emballonuridae, Noctilionidae, Natalidae and Vespertilionidae. Caryologia 23:595–604Google Scholar
  4. Baker JW, Patton JL (1967) Karyotypes and karyotypic variation of North American vespertilionid bats. J Mammal 48:270–286CrossRefGoogle Scholar
  5. Baker RJ, Bass RA (1979) Evolutionary relationships of the Brachyphylllinae to the Glossophagine genera Glossophaga and Monophyllus. J Mammal 60:364–372CrossRefGoogle Scholar
  6. Baker RJ, Bickham JW (1980) Karyotypic evolution in bats: evidence of extensive and conservative chromosomal evolution in closely related taxa. Syst Zool 29:239–253CrossRefGoogle Scholar
  7. Baker RJ, Qumsiyeh MB (1988) Methods in chiropteran mitotic studies. In: Kunz TH (ed) Ecological and behavioral methods for the study of bats. Smithsonian Press, Washington, DC, pp 425–435Google Scholar
  8. Baker RJ, Genoways HH, Seyfarth PA (1981) Results of the Alcoa Foundation-Suriname expeditions. VI. Additional chromosomal data for bats (Mammalia: Chiroptera) from Suriname. Ann Carnegie Mus 50:333–344Google Scholar
  9. Bickham JW (1979a) Banded karyotypes of 11 species of American bats (genus Myotis). Cytologia 44:789–797PubMedGoogle Scholar
  10. Bickham JW (1979b) Chromosomal variation and evolutionary relationships of vespertilionid bats. J Mammal 60:350–363CrossRefGoogle Scholar
  11. Bickham JW, Daniel MJ, Haiduk MW (1980) Karyotype of Mystacina tuberculata (Chiroptera: Mystacinidae). J Mammal 61:322–324CrossRefGoogle Scholar
  12. Bickham JW, McBee K, Schlitter DA (1986) Chromosomal variation among seven species of Myotis (Chiroptera: Vespertilionidae). J Mammal 67:746–750CrossRefGoogle Scholar
  13. Dobigny G, Ozouf-Costaz C, Bonilla C, Volobouev V (2004) Viability of X-autosome translocations in mammals: an epigenomic hypothesis from a rodent case-study. Chromosoma 113:34–41CrossRefPubMedGoogle Scholar
  14. Eger JL, Mitchell L (1996) Biogeography of the bats of Madagascar. Biogéographie de Madagascar 1996:321–328Google Scholar
  15. Eger JL, Mitchell L (2003) Chiroptera, bats. In: Goodman SM, Benstead JP (eds) The Natural History of Madagascar. University of Chicago Press, Chicago, Illinois, pp 1287–1298Google Scholar
  16. 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 22:1869–1886CrossRefPubMedGoogle Scholar
  17. Ferguson-Smith MA, Trifonov V (2007) Mammalian karyotype evolution. Nat Rev Genet 8:950–962CrossRefPubMedGoogle Scholar
  18. Gannon WL, Sikes RS, Animal Care and Use Committee of the American Society of Mammalogists (2007) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 88:809–823CrossRefGoogle Scholar
  19. Gardner JL (1977) Chromosomal variation in Vampyressa and a review of chromosomal evolution in the Phyllostomidae (Chiroptera). Syst Zool 26:300–318CrossRefGoogle Scholar
  20. Goodman SM, Maminirina CP, Weyeneth N et al (2009a) The use of molecular and morphological characters to resolve the taxonomic identity of cryptic species: the case of Miniopterus manavi (Chiroptera: Miniopteridae). Zool Scr 38:339–363CrossRefGoogle Scholar
  21. Goodman SM, Maminirina CP, Bradman HM et al (2009b) The use of molecular phylogenetic and morphological tools to indentify cryptic and paraphyletic species: examples from the diminutive long-fingered bats (Chiroptera: Miniopteridae: Miniopterus) on Madagascar. Am Mus Novit 3669:1–34CrossRefGoogle Scholar
  22. Hood CS, Baker RJ (1986) G- and C-band chromosome studies of bats of the family Emballonuridae. J Mammal 67:705–711CrossRefGoogle Scholar
  23. Hood CS, Schlitter DA, Georgudaki JI, Yenbutra S, Baker RJ (1988) Chromosomal studies of bats (Mammalia: Chiroptera) from Thailand. Ann Carnegie Mus 57:99–109Google Scholar
  24. Hoofer SR, Reeder SA, Hansen EW, Van Den Bussche RA (2003) Molecular phylogenetics and taxonomic review of noctilionoid and vespertilionoid bats (Chiroptera: Yangochiroptera). J Mammal 84:809–821CrossRefGoogle Scholar
  25. Hsu TC, Baker RJ, Utakoji T (1968) The multiple sex chromosome system of American leaf-nosed bats (Chiroptera, Phyllostomidae). Cytogenetics 7:27–38CrossRefPubMedGoogle Scholar
  26. Kerridge DC, Baker RJ (1978) Natalus micropus. Mamm Species 114:1–3CrossRefGoogle Scholar
  27. Koopman KF (1994) Chiroptera: systematics. In: Niethammer J, Schliemann H, Starck D (eds) Handbook of Zoology, vol 8. Walter de Gruyter Press, Berlin, pp 1–217Google Scholar
  28. Lamb JM, Ralph TMC, Goodman SM et al (2008) Phylogeography and predicted distribution of African-Arabian and Malagasy populations of giant mastiff bats, Otomops spp. Acta Chiropt 10:21–40CrossRefGoogle Scholar
  29. Lyon MF (1968) Chromosomal and subchromosomal inactivation. Annu Rev Genet 2:31–52CrossRefGoogle Scholar
  30. Mao X, Wang J, Su W et al (2007) Karyotype evolution in Rhinolophus bats (Rhinolophidae, Chiroptera) illuminated by cross-species chromosome painting and G-banding comparison. Chromosome Res 15:835–848CrossRefPubMedGoogle Scholar
  31. Mao X, Nie W, Wang J et al (2008) Comparative cytogenetics of bats (Chiroptera): the prevalence of Robertsonian translocations limits the power of chromosomal characters in resolving interfamily phylogenetic relationships. Chromosome Res 16:155–170CrossRefPubMedGoogle Scholar
  32. Miller-Butterworth CM, Murphy WJ, O’Brien SJ, Jacobs DS, Springer MS, Teeling EC (2007) A family matter: conclusive resolution of the taxonomic position of the long-fingered bats, Miniopterus. Mol Biol Evol 24:1553–1561CrossRefPubMedGoogle Scholar
  33. O’Brien J, Mariani C, Olson L et al (2009) Multiple colonisations of the western Indian Ocean by Pteropus fruit bats (Megachiroptera: Pteropodidae): the furthest islands were colonised first. Mol Phylogenet Evol 51:294–303CrossRefPubMedGoogle Scholar
  34. Parish DA, Vise P, Wichman HA, Bull JJ, Baker RJ (2002) Distribution of LINES and other repetitive elements in the karyotype of the bat Carollia: implications for X-chromosome inactivation. Cytogenet Genome Res 96:191–197CrossRefPubMedGoogle Scholar
  35. Patton JC, Baker RJ (1978) Chromosomal homology and evolution of Phyllostomoid bats. Syst Zool 27:449–462CrossRefGoogle Scholar
  36. Peterson RL, Eger JL, Mitchell L (1995) Chiroptêres. Vol 84. Fauna de Madagascar. Museum National d’Histoire Naturelle, Paris, pp 1–204Google Scholar
  37. Pieczarka JC, Nagamachi CY, O’Brien PCM et al (2005) Reciprocal chromosome painting between two South American bats: Carollia brevicuda and Phyllostomus hastatus (Phyllostomidae, Chiroptera). Chromosome Res 13:339–347CrossRefPubMedGoogle Scholar
  38. Ratrimomanarivo FH, Vivian J, Goodman SM (2007) Morphological and molecular assessment of the specific status of Mops midas (Chiroptera: Molossidae) from Madagascar and Africa. Afr Zool 42:237–253CrossRefGoogle Scholar
  39. Ratrimomanarivo FH, Goodman SM, Hoosen N, Taylor PJ, Lamb J (2008) Morphological and molecular variation in Mops leucostigma (Chiroptera: Molossidae) of Madagascar and the Comoros: phylogeny, phylogeography, and geographic variation. Mitt Hamb Zool Mus Inst 105:57–101Google Scholar
  40. Russell AL, Goodman SM, Cox MP (2008) Coalescent analyses support multiple mainland-to-island dispersals in the evolution of Malagasy Triaenops bats (Chiroptera: Hipposideridae). J Biogeogr 35:995–1003CrossRefGoogle Scholar
  41. Seabright M (1971) A rapid staining technique for human chromosomes. Lancet 2:971–972CrossRefPubMedGoogle Scholar
  42. Sharp AJ, Spotswood HT, Robinson DO, Turner BM, Jacobs PA (2002) Molecular and cytogenetic analysis of the spreading of X-inactivation in X;autosome translocations. Hum Mol Genet 11:3145–3156CrossRefPubMedGoogle Scholar
  43. Simmons NB (1998) A reappraisal of interfamilial relationships of bats. In: Kunz TH, Racey PA (eds) Bat Biology and Conservation. Smithsonian Institution Press, Washington DC, pp 3–26Google Scholar
  44. Simmons NB (2005) Order Chiroptera. In: Wilson DE, Reeder DM (eds) Mammal Species of the World: a Taxonomic and Geographic Reference, vol 1, 3rd edn. Johns Hopkins University Press, Baltimore, MD, pp 312–529Google Scholar
  45. Simmons NB, Geisler JH (1998) Phylogenetic relationships of Icaronycteris, Archanycteris, Hassianycteris and Palaeochiroptera to extant bat lineages, with comments on the evolution of echolocation and foraging strategies in Microchiroptera. Bull Am Mus Nat Hist 235:1–182Google Scholar
  46. Smith JD (1976) Chiropteran evolution. In: Baker RJ, Jones JK, Carter DC (eds) Biology of the bats of the new world family Phyllostomidae, vol. I. [Special Publications, Museum of Texas Tech University 10: 1–218], pp 46–69Google Scholar
  47. Sreepada KS, Koubínová D, Konečny A et al (2008) Karyotypes of three species of molossid bats (Molossidae, Chiroptera) from India and western Africa. Folia Zool 57:347–357Google Scholar
  48. Stadelmann B, Jacobs DS, Schoeman MC, Ruedi M (2004) Phylogeny of Myotis bats (Chiroptera, Vespertilionidae) inferred from cytochrome b sequences. Acta Chiropt 6:177–192Google Scholar
  49. Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306CrossRefPubMedGoogle Scholar
  50. Teeling EC, Springer MS, Madsen O, Bates P, O’Brien SJ, Murphy MJ (2005) A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307:580–584CrossRefPubMedGoogle Scholar
  51. Telenius H, Pelmear AH, Tunnacliffe A et al (1992) Cytogenetic analysis by chromosome painting using DOP-PCR amplified flow-sorted chromosomes. Gene Chromosome Canc 4:257–263CrossRefGoogle Scholar
  52. Tucker PK, Bickham JW (1989) Heterochromatin and sex-chromosome variation in bats of the genus Carollia (Chiroptera: Phyllostomidae). J Mammal 70:174–179CrossRefGoogle Scholar
  53. Van Den Bussche RA, Hoofer SR (2001) Evaluating monophyly of Nataloidea (Chiroptera) with mitochondrial DNA sequences. J Mammal 82:320–327CrossRefGoogle Scholar
  54. Van Den Bussche RA, Reeder SA, Hansen EW, Hoofer SR (2003) Utility of the dentin matrix protein 1 (DMP1) gene for resolving mammalian intraordinal phylogenetic relationships. Mol Phylogenet Evol 26:89–101CrossRefGoogle Scholar
  55. Volleth M, Yong HS (1987) Glischropus tylophus, the first known old-world bat with an X-autosome translocation. Cell Mol Life Sci 43:922–924CrossRefGoogle Scholar
  56. Volleth M, Heller KG (2007) Chromosome number reduction accompanied by extensive heterochromatin addition in the bat Glauconycteris beatrix (Mammalia; Chiroptera, Vespertilionidae). Cytogenet Genome Res 119:245–247CrossRefPubMedGoogle Scholar
  57. Volleth M, Klett C, Kollak A et al (1999) ZOO-FISH analysis in a species of the order Chiroptera: Glossophaga soricina (Phyllostomidae). Chromosome Res 7:57–64CrossRefPubMedGoogle Scholar
  58. Volleth M, Heller KG, Pfeiffer R, Hameister H (2002) A comparative ZOO-FISH analysis in bats elucidates the phylogenetic relationships between Megachiroptera and five microchiropteran families. Chromosome Res 10:477–497CrossRefPubMedGoogle Scholar
  59. Weyeneth N, Goodman SM, Stanley WT, Ruedi M (2008) The biogeography of Miniopterus bats Chiroptera: Miniopteridae) from the Comoro Archipelago inferred from mitochondrial DNA. Mol Ecol 17:5205–5219CrossRefPubMedGoogle Scholar
  60. Wienberg J, Stanyon R (1997) Comparative painting of mammalian chromosomes. Curr Opin Genet Dev 7:784–791CrossRefPubMedGoogle Scholar
  61. Yong HS, Dhaliwal SS (1976) Chromosomes of the fruit-bat subfamily Macroglossinae from peninsular Malaysia. Cytologia 41:85–89Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Leigh R. Richards
    • 1
  • Ramugondo V. Rambau
    • 2
  • Jennifer M. Lamb
    • 1
  • Peter J. Taylor
    • 3
    • 4
  • Fengtang Yang
    • 5
  • M. Corrie Schoeman
    • 1
  • Steven M. Goodman
    • 6
    • 7
  1. 1.School of Biological and Conservation SciencesUniversity of KwaZulu-NatalDurbanSouth Africa
  2. 2.DST-NRF Center of Excellence for Invasion Biology and Evolutionary Genomics Group, Department of Botany and ZoologyUniversity of StellenboschStellenboschSouth Africa
  3. 3.Durban Natural Science MuseumDurbanSouth Africa
  4. 4.School of Environmental SciencesUniversity of VendaThohoyandouSouth Africa
  5. 5.The Wellcome Trust Sanger InstituteWellcome Trust Genome CampusHinxtonUK
  6. 6.Department of ZoologyField Museum of Natural HistoryChicagoUSA
  7. 7.AntananarivoMadagascar

Personalised recommendations