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Cross-species chromosome painting unveils cytogenetic signatures for the Eulipotyphla and evidence for the polyphyly of Insectivora

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Abstract

Insectivore-like animals are traditionally believed among the first eutherian mammals that have appeared on the earth. The modern insectivores are thus crucial for understanding the systematics and phylogeny of eutherian mammals as a whole. Here cross-species chromosome painting, with probes derived from flow-sorted chromosomes of human, was used to delimit the homologous chromosomal segments in two Soricidae species, the common shrew (Sorex araneus, 2n = 20/21), and Asiatic short-tailed shrew (Blarinella griselda, 2n = 44), and one Erinaceidae species, the shrew-hedgehog (Neotetracus sinensis, 2n = 32), and human. We report herewith the first comparative maps for the Asiatic short-tailed shrew and the shrew-hedgehog, in addition to a refined comparative map for the common shrew. In total, the 22 human autosomal paints detected 40, 51 and 58 evolutionarily conserved segments in the genomes of common shrew, Asiatic short-tailed shrew, and shrew-hedgehog, respectively, demonstrating that the common shrew has retained a conserved genome organization while the Asiatic short-tailed shrew and shrew-hedgehog have relatively rearranged genomes. In addition to confirming the existence of such ancestral human segmental combinations as HSA 3/21, 12/22, 14/15 and 7/16 that are shared by most eutherian mammals, our study reveals a shared human segmental combination, HSA 4/20, that could phylogenetically unite the Eulipotyphlan (i.e., the core insectivores) species. Our results provide cytogenetic evidence for the polyphyly of the order Insectivora and additional data for the eventual reconstruction of the ancestral eutherian karyotype.

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References

  • Arnason U, Adegoke JA, Bodin K et al. (2002) Mammalian mitogenomic relationships and the root of the eutherian tree. Proc Natl Acad Sci USA 99: 8151–8156.

    Article  CAS  PubMed  Google Scholar 

  • Bigoni F, Stanyon R, Wimmer R, Schempp W (2003) Chromosome painting shows that the proboscis monkey (Nasalis larvatus) has a derived karyotype and is phylogenetically nested with in Asian colobines. Am J Primatol 60: 85–93.

    Article  CAS  PubMed  Google Scholar 

  • Butler PM (1972) The problem of insectivore classification. In: Joysey KA, Kemp TS, eds. Studies in Vertebrate Evolution. Edinburgh: Oliver and Boyd, pp. 53–265.

    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  CAS  PubMed  Google Scholar 

  • Douady CJ, Chatelier PI, Madsen O et al. (2002) Molecular phylogenetic evidence confirming the Eulipotyphla concept and in support of hedgehogs as the sister group to shrews. Mol Phylogenet Evol 25: 200–209.

    CAS  PubMed  Google Scholar 

  • Emerson GL, Kilpatrick CW, McNiff BE, Ottenwalder J, Allard MW (1999) Phylogenetic relationships of the order Insectivora based on complete 12S rRNA sequences from mitochondria. Cladistics 15: 221–230.

    Article  Google Scholar 

  • Frönicke L, Wienberg J, Stone G, Adams L, Stanyon R (2003) Towards the delineation of the ancestral eutherian genome organization: comparative genome maps of the human and the African elephant (Loxodonta africana) generated by chromosome painting. Proc R Soc Lond B 270: 1331–1340.

    Google Scholar 

  • Haeckel E (1866) Systematische Einleitung in die allgemeine Entwicklungsgeschichte. Generelle morphologic der orgnismen. Berlin: Georg Reimer.

    Google Scholar 

  • Krettek A, Gullberg A, Arnason U (1995) Sequence analysis of the complete mitochondrial DNA molecule of the hedgehog, Erinaceus europhaeus, and the phylogenetic position of the lipotyphla. J Mol Evol 41: 952–957.

    Article  CAS  PubMed  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.

    PubMed  Google Scholar 

  • MacPhee RDE, Novacek MJ (1993) Definition and relationships of Lipotyphla. In: Szalay FS, Novacek MJ, Mckenna MC, eds. Mammal Phylogeny, Vol 2: Placentals. New York: Springer-Verlag, pp. 13–31.

    Google Scholar 

  • Madsen O, Scally M, Douady CJ et al. (2001) Parallel adaptive radiations in two major clades of placental mammals. Nature 406: 610–614.

    Google Scholar 

  • Malia MJ, Adkins RM, Allard MW (2002) Molecular support for Afrotheria and the polyphyly of Liotyphla based on analyses of the grown hormone receptor gene. Mol Phylogenet Evol 24: 91–101.

    CAS  PubMed  Google Scholar 

  • McKenna MC (1975) Toward a phylogenetic classification of the Mammalia. In: Luckett WP, Szalay FS, eds. Phylogeny of the Primates: A Multidisciplinary Approach. New York: Plenum Press, pp. 21–46.

    Google Scholar 

  • Mouchaty SK, Gullberg A, Janke A, Arnason U (2000) The phylogenetic position of the Talpidae within Eutheria based on analysis of complete mitochondrial sequences. Mol Biol Evol 17: 60–67.

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Murphy WJ, Stanyon R, O'Brien SJ (2001b) Evolution of mammalian genome organization inferred from comparative gene mapping. Genome Biol 2: 1568–1572.

    Article  Google Scholar 

  • Murphy WJ, Eizirik E, O'Brien SJ et al. (2001c) Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294: 2348–2351.

    Article  CAS  PubMed  Google Scholar 

  • Murphy WJ, Pevzner PA, O'Brien SJ (2004) Mammalian phylogenomics comes of age. Trends Genet 20: 631–639.

    Article  CAS  PubMed  Google Scholar 

  • Nikaido M, Cao Y, Harada M, Okada N, Hasegawa M (2003) Mitochondrial phylogeny of hedgehogs and monophyly of Eulipotyphla. Mol Phylogenet Evol 28: 276–284.

    CAS  PubMed  Google Scholar 

  • Nie W, Liu R, Chen Y, Wang J, Yang F (1998) Mapping chromosomal homologies between humans and two langurs (Semnopithecus francoisi and S. phayrei) by chromosome painting. Chromosome Res 6: 447–453.

    Article  CAS  PubMed  Google Scholar 

  • Nie W, Rens W, Wang J, Yang F (2001) Conserved chromosome segments in Hylobates hoolock revealed by human and H. leucogenys paint probes. Cytogenet Cell Genet 92: 248–253.

    Article  CAS  PubMed  Google Scholar 

  • Nie W, Wang J, O'Brien PC 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  CAS  PubMed  Google Scholar 

  • Nie W, O'Brien PCM, Fu B et al. (2006) Chromosome painting between human and lorisiform prosimians: evidence for the HSA 7/16 synteny in the primate ancestral karyotype. Am J Phys Anthropol 129: 250–259.

    Google Scholar 

  • Nowak RM (1999) Walker's Mammals of the World, 6th edn., Vol 1, Baltimore and London: Johns Hopkins University Press, pp. 169–243.

    Google Scholar 

  • Perelman PL, Graphodatsky AS, Serdukova NA et al. (2005) Karyotypic conservatism in the suborder Feliformia (Order Carnivora). Cytogenet Genome Res 108: 348–354.

    Article  CAS  PubMed  Google Scholar 

  • Richard F, Lombard M, Dutrillaux B (2003a) Reconstruction of the ancestral karyotype of eutherian mammals. Chromosome Res 11: 605–618.

    CAS  PubMed  Google Scholar 

  • Richard F, Messaoudi C, Bonnet-Garnier A, Lombard M, Dutrillaux B (2003b) Highly conserved chromosomes in an Asian squirrel (Menetes berdmorei, Rodentia: Sciuridae) as demonstrated by ZOO-FISH with human probes. Chromosome Res 11: 597–603.

    CAS  PubMed  Google Scholar 

  • Robinson TJ, Fu B, Ferguson-Smith MA, Yang F (2004) Cross-species chromosome painting in the golden mole and elephant shrew: support for the mammalian clades Afrotheria and Afroinsectiphilla but not Afroinsectivora. Proc R Soc Lond B 271: 1477–1484.

    Article  CAS  Google Scholar 

  • Seabright M (1972) The use of proteolytic enzymes for the mapping of structural rearrangements in the chromosomes of man. Chromosoma 36: 204–210.

    Article  CAS  PubMed  Google Scholar 

  • Springer MS, Cleven GC, Madsen O et al. (1997) Endemic African mammals shake the phylogenetic tree. Nature 388: 61–64.

    Article  CAS  PubMed  Google Scholar 

  • Stanhope MJ, Waddell VG, Madsen O et al. (1998) Molecular evidence for multiple origins of Insectivora and for a new order of endemic African insectivore mammals. Proc Natl Acad Sci USA 95: 9967–9972.

    Article  CAS  PubMed  Google Scholar 

  • Stanyon R, Koehler U, Consigliere S (2002) Chromosome painting reveals that galagos have highly derived karyotypes. Am J Phys Anthropol 117: 319–326.

    Article  PubMed  Google Scholar 

  • Stanyon R, Stone G, Garcia M, Fröenicke L (2003) Reciprocal chromosome painting shows that squirrels, unlike murid rodents, have a highly conserved genome organization. Genomics 82: 245–249.

    Article  CAS  PubMed  Google Scholar 

  • Svartman M, Stone G, Page JE, Stanyon R (2004) A chromosome painting test of the basal eutherian karyotype. Chromosome Res 12: 15–53.

    Article  Google Scholar 

  • Telenius H, Pelmear AH, Tunnacliffe A et al. (1992) Cytogeneticanalysis by chromosome painting using DOP-PCR amplified flow-sorted chromosome. Gene Chromosome Cancer 4: 257–263.

    CAS  Google Scholar 

  • Waddell PJ, Shelley S (2003) Evaluating placental interordinal phylogenies with novel sequences including RAG1, γ-fibrinogen, ND6 and mt-tRNA, plus MCMC-driven nucleotide, amino acid, and codon models. Mol Phylogenet Evol 28: 197–224.

    CAS  PubMed  Google Scholar 

  • Waddell PJ, Okada N, Hasegawa M (1999) Towards resolving the interordinal relationships of placental mammals. Syst Biol 48: 1–5.

    CAS  PubMed  Google Scholar 

  • Waddell PJ, Kishino H, Ota R (2001) A phylogenetic foundation for comparative mammalian genomics. Genome Informatics 12: 141–154.

    CAS  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.

    CAS  PubMed  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.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Yang F, Milne BS, Schelling C et al. (2000) Chromosome identification and assignment of DNA clones in the dog using a red fox and dog comparative map. Chromosome Res 8: 93–100.

    CAS  PubMed  Google Scholar 

  • Yang F, Alkalaeva EZ, Perelman PL et al. (2003) Reciprocal chromosome painting among human, aardvark, and elephant (superorder Afrotheria) reveals the likely eutherian ancestral karyotype. Proc Natl Acad Sci USA 100: 1062–1066.

    CAS  PubMed  Google Scholar 

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Correspondence to Fengtang Yang.

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Ye, J., Biltueva, L., Huang, L. et al. Cross-species chromosome painting unveils cytogenetic signatures for the Eulipotyphla and evidence for the polyphyly of Insectivora. Chromosome Res 14, 151–159 (2006). https://doi.org/10.1007/s10577-006-1032-y

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  • DOI: https://doi.org/10.1007/s10577-006-1032-y

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