Chromosome Research

, Volume 15, Issue 8, pp 1075–1091 | Cite as

Chromosomal evolution in tenrecs (Microgale and Oryzorictes, Tenrecidae) from the Central Highlands of Madagascar

  • C. Gilbert
  • S. M. Goodman
  • V. Soarimalala
  • L. E. Olson
  • P. C. M. O’Brien
  • F. F. B. Elder
  • F. Yang
  • M. A. Ferguson-Smith
  • T. J. Robinson
Article

Abstract

Tenrecs (Tenrecidae) are a widely diversified assemblage of small eutherian mammals that occur in Madagascar and Western and Central Africa. With the exception of a few early karyotypic descriptions based on conventional staining, nothing is known about the chromosomal evolution of this family. We present a detailed analysis of G-banded and molecularly defined chromosomes based on fluorescence in situ hybridization (FISH) that allows a comprehensive comparison between the karyotypes of 11 species of two closely related Malagasy genera, Microgale (10 species) and Oryzorictes (one species), of the subfamily Oryzorictinae. The karyotypes of Microgale taiva and M. parvula (2n = 32) were found to be identical to that of O.hova (2n = 32) most likely reflecting the ancestral karyotypes of both genera, as well as that of the Oryzorictinae. Parsimony analysis of chromosomal rearrangements that could have arisen following Whole Arm Reciprocal Translocations (WARTs) showed, however, that these are more likely to be the result of Robertsonian translocations. A single most parsimonious tree was obtained that provides strong support for three species associations within Microgale, all of which are consistent with previous molecular and morphological investigations. By expanding on a recently published molecular clock for the Tenrecidae we were able to place our findings in a temporal framework that shows strong chromosomal rate heterogeneity within the Oryzorictinae. We use these data to critically examine the possible role of chromosomal rearrangements in speciation within Microgale.

Key words

Afrotheria cytogenetics evolution speciation Tenrecidae 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Asher RJ (2001) Cranial anatomy in tenrecid insectivorans: character evolution across competing phylogenies. Am Mus Novit 3352: 1–4.CrossRefGoogle Scholar
  2. Asher RJ, Hofreiter M (2006) Tenrec phylogeny and the noninvasive extraction of nuclear DNA. Syst Biol 55: 181–94.CrossRefPubMedGoogle Scholar
  3. Baker RJ, Bickham JW (1980) Karyotypic evolution in bats: evidence of extensive and conservative chromosomal evolution in closely related taxa. Syst Zool 29: 239–53.CrossRefGoogle Scholar
  4. Baker RJ, Bickham JW (1986) Speciation by monobrachial centric fusion. Proc Natl Acad Sci USA 83: 8245–248.CrossRefPubMedGoogle Scholar
  5. Bedford JM (2004) Enigmas of mammalian gamete form and function. Biol Rev Camb Philos Soc 79: 429–60.CrossRefPubMedGoogle Scholar
  6. Bedford JM, Mock OB, Goodman SM (2004) Novelties of conception in insectivorous mammals (Lipotyphla), particularly shrews. Biol Rev Camb Philos Soc 79: 1–9.CrossRefGoogle Scholar
  7. Bernischke K (1969) Comparative mammalian cytogenetics: an international conference at Darmouth medical school, Hanover, New Hampshire. New-York: Springer-Verlag.Google Scholar
  8. Borgaonkar DS (1967) Additions to the list of chromosome numbers in the insectivores and primates. J Heredity 58: 211–13.Google Scholar
  9. Borgaonkar DS, Gould E (1965) Chromosome complement of tenrecs, Centetes ecaudatus (Order Insectivora, Class Mammalia). Experientia 21(11): 631–32.CrossRefPubMedGoogle Scholar
  10. Borgaonkar DS, Gould E (1968) Homozygous reciprocal translocation as a mode of speciation in Microgale Thomas 1883 (Tenrecidae, Insectivora). Experientia 24: 506–09.CrossRefPubMedGoogle Scholar
  11. Borgaonkar DS, Gould E (1969) Karyotype of Microgale cowani and its phylogenetic significance. Mammalian Chromosomes Newsletter 10: 31.Google Scholar
  12. Britton-Davidian J, Catalan J, da Graça Ramalhinho M et al. (2000) Rapid chromosomal evolution in island mice. Nature 403: 158.CrossRefPubMedGoogle Scholar
  13. Britton-Davidian J, Catalan J, da Graça Ramalhinho M et al. (2005) Chromosomal phylogeny of Robertsonian races of the house mouse on the island of Madeira: testing between alternative mutational processes. Genet Res 86: 171–83.CrossRefPubMedGoogle Scholar
  14. Capanna E, Castiglia R (2004) Chromosomes and speciation in Mus musculus domesticus. Cytogenet Genome Res 105: 375–84.CrossRefGoogle Scholar
  15. Dobigny G, Ducroz JF, Robinson TJ, Volobouev V (2004) Cytogenetics and cladistic. Syst Biol 53: 470–84.CrossRefPubMedGoogle Scholar
  16. Dobigny G, Aniskin V, Granjon L, Cornette R, Volobouev V (2005) Recent radiation in West African Taterillus (Rodentia, Gerbillinae): the concerted role of chromosome and climatic changes. Heredity 95: 358–68.CrossRefPubMedGoogle Scholar
  17. Eichenlaub-Ritter U, Winking H (1990) Nondisjunction, disturbance in spindle structure, and characteristics of chromosome alignment in maturing oocytes of mice heterozygous for Robertsonian translocations. Cytogenet Cell Genet 54: 47–4.CrossRefPubMedGoogle Scholar
  18. Enders AC, Blankenship TN, Goodman SM, Soarimalala V, Carter AM (2006) Placental diversity in Malagasy tenrecs: placentation in shrew tenrecs (Microgale spp.), the mole-like rice tenrecs (Oryzorictes hova) and the web-footed tenrec (Limnogale mergulus). Placenta 28: 748–59.CrossRefPubMedGoogle Scholar
  19. Endo H, Yonezawa T, Rakotondraparany F, Sasaki M, Hasegawa M (2006) The adaptational strategies of the hindlimb muscles in the Tenrecidae species including the aquatic web-footed tenrec (Limnogale mergulus). Ann Anat 188: 383–90.CrossRefPubMedGoogle Scholar
  20. Garagna S, Redi CA, Zuccotti M, Britton–Davidian J, Winking H (1990) Kinetics of oogenesis in mice heterogeneous for Robertsonian translocations. Differentiation 42: 167–71.CrossRefPubMedGoogle Scholar
  21. Garagna S, Broccoli D, Redi CA, Searle JB, Cooke HJ, Capanna E (1995) Robertsonian metacentrics of the house mouse lose telomeric sequences but retain some minor satellite DNA in the pericentromeric area. Chromosoma 103: 685–92.CrossRefPubMedGoogle Scholar
  22. Gilbert C, O’Brien PC, Bronner GN et al. (2006) Chromosome painting and molecular dating indicate a low rate of chromosomal evolution in golden moles (Chrysochloridae, Mammalia). Chromosome Res 14: 793–03.CrossRefPubMedGoogle Scholar
  23. Goodman SM, Rakotondravony D (2000) The effects of forest fragmentation and isolation on insectivorous small mammals (Lipotyphla) on the Central High Plateau of Madagascar. J Zool 250: 193–00.CrossRefGoogle Scholar
  24. Goodman SM, Soarimalala V (2004) A new species of Microgale (Lipotyphla: Tenrecidae: Oryzorictinae) from the Forêt des Mikea of southwestern Madagascar. Proc Biol Soc Washington 117: 251–265.Google Scholar
  25. Goodman SM, Raxworthy CJ, Maminirina CP, Olson LE (2006) A new species of shrew tenrec (Microgale jobihely) from northern Madagascar. J Zool 270: 384–98.CrossRefGoogle Scholar
  26. Hauffe HC, Pialek 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 Lond 62: 255–78.Google Scholar
  27. Hauffe HC, Searle JB (1998) Chromosomal heterozygosity and fertility in house mice (Mus musculus domesticus) from Northern Italy. Genetics 150: 1143–154.PubMedGoogle Scholar
  28. Jenkins PD (1993) A new species of Microgale (Insectivora: Tenrecidae) from Eastern Madagascar with an unusual dentition. Am Mus Novit 3067: 1–1.Google Scholar
  29. Jenkins PD (2003) Microgale, shrew Tenrecs. In: Goodman SM, Benstead JP, eds. The natural history of Madagascar. The University of Chicago Press, pp 1273–279.Google Scholar
  30. Jenkins PD, Goodman SM (1999) A new species of Microgale (Lipotyphla, Tenrecidae) from isolated forest in southwestern Madagascar. Bull Nat His Mus Lond (Zoology) 65: 155–64.Google Scholar
  31. Jenkins PD, Raxworthy CJ, Nussbaum RA (1997) A new species of Microgale (Insectivora, Tenrecidae), with comments on the status of four other taxa of shrew tenrecs. Bull Nat His Mus. Lond (Zoology) 63: 1–2.Google Scholar
  32. King M (1993) Species Evolution: The Role of Chromosomal Change. Cambridge: Cambridge University Press.Google Scholar
  33. MacPhee RDE (1987) The shrew tenrecs of Madagascar: systematic revision and Holocene distribution of Microgale (Tenrecidae, Insectivora). Am Mus Novit 2889: 1–5.Google Scholar
  34. Martin RD (1972) Adaptive radiation and behaviour of the Malagasy lemurs. Philo Trans Roy Soc Lond B 264: 295–52.CrossRefGoogle Scholar
  35. Martin RD (1995) Prosimians: from obscurity to extinction? In: Alterman L, Doyle GA, Izard MK, eds. Creatures of the Dark: The Nocturnal Prosimians. New York: Plenum Press, pp 535–563.Google Scholar
  36. Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O’Brien SJ (2001) Molecular phylogenetics and the origins of placental mammals. Nature 409: 614–18.CrossRefPubMedGoogle Scholar
  37. Nachman MW, Searle JB (1995) Why is the house mouse karyotype so variable? Trends Ecol Evol 10: 397–02.CrossRefGoogle Scholar
  38. Nanda I, Schneider-Rasp S, Winking H, Schmid M (1995) Loss of telomeric sites in the chromosomes of Mus musculus domesticus (Rodentia: Muridae) during Robertsonian rearrangements. Chromosome Res 3: 399–09.CrossRefPubMedGoogle Scholar
  39. Nevo E, Filippucci MG, Redi C, Korol A, Beiles A (1994) Chromosomal speciation and adaptive radiation of mole rats in Asia Minor correlated with increased ecological stress. Proc Natl Acad Sci USA 91: 8160–164.CrossRefPubMedGoogle Scholar
  40. Olivieri G, Zimmermann E, Randrianambinina B et al. (2007) The ever-increasing diversity in mouse lemurs: Three new species in north and northwestern Madagascar. Mol Phylogenet Evol 43: 309–27.CrossRefPubMedGoogle Scholar
  41. Olson LE, Goodman SM (2003) Phylogeny and biogeography of tenrecs. In: Goodman SM, Benstead JP, eds. The natural history of Madagascar. The University of Chicago Press, pp 1235–242.Google Scholar
  42. Olson LE, Goodman SM, Yoder AD (2004) Illumination of cryptic species boundaries in long-tailed shrew tenrecs (Mammalia: Tenrecidae; Microgale), with new insights into geographic variation and distributional constraints. Biol J Linn Soc Lond 83: 1–2.CrossRefGoogle Scholar
  43. Pardini AT, O’Brien PCM, Fu B et al. (2007) Chromosome painting among Proboscidea, Hyracoidea and Sirenia: support for Paenungulata (Afrotheria, Mammalia) but not Tethytheria. Proc R Soc B 274: 1333–340.CrossRefPubMedGoogle Scholar
  44. Pialek J, Hauffe HC, Searle JB (2005) Chromosomal variation in the house mouse. Biol J Linn Soc Lond 84: 535–63.CrossRefGoogle Scholar
  45. Poux C, Madsen O, Marquard E, Vietes DR, de Jong WW, Vences M (2005) Asynchronous colonization of Madagascar by the four endemic clades of primates, tenrecs, carnivores, and rodents as inferred from nuclear genes. Syst Biol 54: 719–30.CrossRefPubMedGoogle Scholar
  46. Redi CA, Capanna E (1978) DNA-content variation in mouse spermatozoa arising from irregular meiotic segregation. Boll Zool 45: 315–22.Google Scholar
  47. Rieseberg LH (2001) Chromosomal rearrangements and speciation. Trends Ecol Evol 16: 351–58.CrossRefPubMedGoogle Scholar
  48. Robinson TJ, Seiffert ER (2004) Afrotherian origin and interrelationships: new views and future prospects. Cur Top Dev Biol 63: 37–9.CrossRefGoogle Scholar
  49. Saïd K, Saad A, Auffray J-C, Britton-Davidian J (1993) Fertility estimates in the Tunisian all acrocentric and Robertsonian populations of the house mouse and their chromosomal hybrids. Heredity 71: 532–38.CrossRefPubMedGoogle Scholar
  50. Seabright M (1971) A rapid banding technique for human chromosome. Lancet 2: 971–72.CrossRefPubMedGoogle Scholar
  51. Searle JB (1993) Chromosomal hybrid zones in eutherian mammals. In: Harrison RG, ed. Hybrid zones and the evolutionary process. Oxford University Press, pp 309–53.Google Scholar
  52. Searle JB, Hübner R, Wallace BMN, Garagna S (1990) Robertsonian variation in wild mice and shrews. Chrom Today 10: 253–63.Google Scholar
  53. Springer MS, Cleven GC, Madsen O, et al. (1997) Endemic African mammals shake the phylogenetic tree. Nature 388: 61–4.CrossRefPubMedGoogle Scholar
  54. Stephenson PJ, Racey PA (1995) Resting metabolic rate and reproduction in the Insectivora. Comp Biochem Physio 112A: 215–23.CrossRefGoogle Scholar
  55. Swofford DL (2002) PAUP* 4.0. Phylogenetic Analysis Using Parsimony (*and Other methods). Sinauer Associates, Sunderland, Massachusetts.Google Scholar
  56. Telenius H, Carter NP, Bebb CE, Nordenskjöld M, Ponder BAJ, Tunnacliffe A (1992) Degenerate oligunucleotid-primed PCR: general amplification of target DNA by a single degenerate primer. Genomics 13: 718–25.CrossRefPubMedGoogle Scholar
  57. Thomas O (1882) Description of a new genus and two new species of Insectivora from Madagascar. J Linn Soc Zool 16: 319–22.Google Scholar
  58. Thorne JL, Kishino H (2002) Divergence time and evolutionary rate estimation with multilocus data. Syst Biol 51: 689–02.CrossRefPubMedGoogle Scholar
  59. Viroux M-C, Bauchau V (1992) Segregation and fertility in Mus musculus domesticus (wild mice) heterozygous for the Rb(4.12) translocation. Heredity 68: 131–34.CrossRefPubMedGoogle Scholar
  60. Wallace BMN, Searle JB, Everett CA (1992) Male meiosis and gametogenesis in wild house mice, Mus musculus: Survey of present knowledge and new observations. Z Saugetierkd 53: 148–61.Google Scholar
  61. Wang W, Lan H (2000) Rapid parallel chromosomal number reductions in muntjac deer inferred from mitochondrial DNA phylogeny. Mol Biol Evol 17: 1326–333.PubMedGoogle Scholar
  62. White MJD (1968) Models of speciation. Science 159: 1065–070.CrossRefPubMedGoogle Scholar
  63. Wilmé L, Goodman SM, Ganzhorn JU (2006) Biogeographic evolution of Madagascar micro-endemic biota. Science 312: 1063–064.CrossRefPubMedGoogle Scholar
  64. Winking H, Dulic B, Bulfield G (1988) Robertsonian karyotype variation in the European house mouse (Mus musculus domesticus) from a chromosomal hybrid zone; a comparison between ‘simple’ Robertsonian heterozygotes and homozygotes. Cytogenet Cell Genet 61: 211–20.Google Scholar
  65. Winking H (1986) Some aspects of Robertsonian karyotype variation in European wild mice. Curr Top Microbiol Immunol 127: 68–4.PubMedGoogle Scholar
  66. Yoder A, Yang Z (2004) Divergence dates for Malagasy lemurs estimated from multiple gene loci: geological and evolutionary context. Mol Ecol 13: 757–73.CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • C. Gilbert
    • 1
  • S. M. Goodman
    • 2
    • 3
  • V. Soarimalala
    • 3
    • 4
  • L. E. Olson
    • 5
  • P. C. M. O’Brien
    • 6
  • F. F. B. Elder
    • 7
  • F. Yang
    • 8
  • M. A. Ferguson-Smith
    • 6
  • T. J. Robinson
    • 1
  1. 1.Evolutionary Genomics Group, Department of Botany and ZoologyUniversity of StellenboschStellenboschSouth Africa
  2. 2.Department of ZoologyField Museum of Natural HistoryChicagoUSA
  3. 3.VahatraAntananarivo (101)Madagascar
  4. 4.Département de Biologie AnimaleUniversité d’AntananarivoAntananarivo (101)Madagascar
  5. 5.University of Alaska Museum, University of Alaska FairbanksFairbanksUSA
  6. 6.Centre for Veterinary ScienceUniversity of CambridgeCambridgeUK
  7. 7.Department of Pathology, Cytogenetics LaboratoryUT Southwestern Medical CenterDallasUSA
  8. 8.The Wellcome Trust Sanger InstituteWellcome Trust Genome CampusCambridgeUK

Personalised recommendations