Skip to main content
SpringerLink
Log in

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

  • Published:
Chromosome Research Aims and scope Submit manuscript

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.

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

  • Asher RJ (2001) Cranial anatomy in tenrecid insectivorans: character evolution across competing phylogenies. Am Mus Novit 3352: 1–4.

    Article  Google Scholar 

  • Asher RJ, Hofreiter M (2006) Tenrec phylogeny and the noninvasive extraction of nuclear DNA. Syst Biol 55: 181–94.

    Article  PubMed  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: 239–53.

    Article  Google Scholar 

  • Baker RJ, Bickham JW (1986) Speciation by monobrachial centric fusion. Proc Natl Acad Sci USA 83: 8245–248.

    Article  PubMed  CAS  Google Scholar 

  • Bedford JM (2004) Enigmas of mammalian gamete form and function. Biol Rev Camb Philos Soc 79: 429–60.

    Article  PubMed  Google Scholar 

  • Bedford JM, Mock OB, Goodman SM (2004) Novelties of conception in insectivorous mammals (Lipotyphla), particularly shrews. Biol Rev Camb Philos Soc 79: 1–9.

    Article  Google Scholar 

  • Bernischke K (1969) Comparative mammalian cytogenetics: an international conference at Darmouth medical school, Hanover, New Hampshire. New-York: Springer-Verlag.

    Google Scholar 

  • Borgaonkar DS (1967) Additions to the list of chromosome numbers in the insectivores and primates. J Heredity 58: 211–13.

    Google Scholar 

  • Borgaonkar DS, Gould E (1965) Chromosome complement of tenrecs, Centetes ecaudatus (Order Insectivora, Class Mammalia). Experientia 21(11): 631–32.

    Article  CAS  PubMed  Google Scholar 

  • Borgaonkar DS, Gould E (1968) Homozygous reciprocal translocation as a mode of speciation in Microgale Thomas 1883 (Tenrecidae, Insectivora). Experientia 24: 506–09.

    Article  CAS  PubMed  Google Scholar 

  • Borgaonkar DS, Gould E (1969) Karyotype of Microgale cowani and its phylogenetic significance. Mammalian Chromosomes Newsletter 10: 31.

    Google Scholar 

  • Britton-Davidian J, Catalan J, da Graça Ramalhinho M et al. (2000) Rapid chromosomal evolution in island mice. Nature 403: 158.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Capanna E, Castiglia R (2004) Chromosomes and speciation in Mus musculus domesticus. Cytogenet Genome Res 105: 375–84.

    Article  CAS  Google Scholar 

  • Dobigny G, Ducroz JF, Robinson TJ, Volobouev V (2004) Cytogenetics and cladistic. Syst Biol 53: 470–84.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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 

  • Hauffe HC, Searle JB (1998) Chromosomal heterozygosity and fertility in house mice (Mus musculus domesticus) from Northern Italy. Genetics 150: 1143–154.

    CAS  PubMed  Google Scholar 

  • 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 

  • 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.

  • 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 

  • 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 

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

    Google Scholar 

  • 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 

  • Martin RD (1972) Adaptive radiation and behaviour of the Malagasy lemurs. Philo Trans Roy Soc Lond B 264: 295–52.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Nachman MW, Searle JB (1995) Why is the house mouse karyotype so variable? Trends Ecol Evol 10: 397–02.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Pialek J, Hauffe HC, Searle JB (2005) Chromosomal variation in the house mouse. Biol J Linn Soc Lond 84: 535–63.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Redi CA, Capanna E (1978) DNA-content variation in mouse spermatozoa arising from irregular meiotic segregation. Boll Zool 45: 315–22.

    Google Scholar 

  • Rieseberg LH (2001) Chromosomal rearrangements and speciation. Trends Ecol Evol 16: 351–58.

    Article  PubMed  Google Scholar 

  • Robinson TJ, Seiffert ER (2004) Afrotherian origin and interrelationships: new views and future prospects. Cur Top Dev Biol 63: 37–9.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Seabright M (1971) A rapid banding technique for human chromosome. Lancet 2: 971–72.

    Article  CAS  PubMed  Google Scholar 

  • 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.

  • Searle JB, Hübner R, Wallace BMN, Garagna S (1990) Robertsonian variation in wild mice and shrews. Chrom Today 10: 253–63.

    Google Scholar 

  • Springer MS, Cleven GC, Madsen O, et al. (1997) Endemic African mammals shake the phylogenetic tree. Nature 388: 61–4.

    Article  CAS  PubMed  Google Scholar 

  • Stephenson PJ, Racey PA (1995) Resting metabolic rate and reproduction in the Insectivora. Comp Biochem Physio 112A: 215–23.

    Article  CAS  Google Scholar 

  • Swofford DL (2002) PAUP* 4.0. Phylogenetic Analysis Using Parsimony (*and Other methods). Sinauer Associates, Sunderland, Massachusetts.

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Thorne JL, Kishino H (2002) Divergence time and evolutionary rate estimation with multilocus data. Syst Biol 51: 689–02.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • Wang W, Lan H (2000) Rapid parallel chromosomal number reductions in muntjac deer inferred from mitochondrial DNA phylogeny. Mol Biol Evol 17: 1326–333.

    CAS  PubMed  Google Scholar 

  • White MJD (1968) Models of speciation. Science 159: 1065–070.

    Article  CAS  PubMed  Google Scholar 

  • Wilmé L, Goodman SM, Ganzhorn JU (2006) Biogeographic evolution of Madagascar micro-endemic biota. Science 312: 1063–064.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Winking H (1986) Some aspects of Robertsonian karyotype variation in European wild mice. Curr Top Microbiol Immunol 127: 68–4.

    CAS  PubMed  Google Scholar 

  • Yoder A, Yang Z (2004) Divergence dates for Malagasy lemurs estimated from multiple gene loci: geological and evolutionary context. Mol Ecol 13: 757–73.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Evolutionary Genomics Group, Department of Botany and Zoology, University of Stellenbosch, Stellenbosch, South Africa

    C. Gilbert & T. J. Robinson

  2. Department of Zoology, Field Museum of Natural History, Lake Shore Drive, Chicago, IL, USA

    S. M. Goodman

  3. Vahatra, BP 738, Antananarivo (101), Madagascar

    S. M. Goodman & V. Soarimalala

  4. Département de Biologie Animale, Université d’Antananarivo, BP 906, Antananarivo (101), Madagascar

    V. Soarimalala

  5. University of Alaska Museum, University of Alaska Fairbanks, Fairbanks, AK, USA

    L. E. Olson

  6. Centre for Veterinary Science, University of Cambridge, Cambridge, UK

    P. C. M. O’Brien & M. A. Ferguson-Smith

  7. Department of Pathology, Cytogenetics Laboratory, UT Southwestern Medical Center, Dallas, TX, USA

    F. F. B. Elder

  8. The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, UK

    F. Yang

Authors
  1. C. Gilbert
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. M. Goodman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. Soarimalala
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. L. E. Olson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P. C. M. O’Brien
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. F. F. B. Elder
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. F. Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. M. A. Ferguson-Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. T. J. Robinson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T. J. Robinson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gilbert, C., Goodman, S.M., Soarimalala, V. et al. Chromosomal evolution in tenrecs (Microgale and Oryzorictes, Tenrecidae) from the Central Highlands of Madagascar. Chromosome Res 15, 1075–1091 (2007). https://doi.org/10.1007/s10577-007-1182-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-007-1182-6

Key words

Search

Navigation