Chromosome painting in the manatee supports Afrotheria and Paenungulata

BackgroundSirenia (manatees, dugongs and Stellar's sea cow) have no evolutionary relationship with other marine mammals, despite similarities in adaptations and body shape. Recent phylogenomic results place Sirenia in Afrotheria and with elephants and rock hyraxes in Paenungulata. Sirenia and Hyracoidea are the two afrotherian orders as yet unstudied by comparative molecular cytogenetics. Here we report on the chromosome painting of the Florida manatee.ResultsThe human autosomal and X chromosome paints delimited a total of 44 homologous segments in the manatee genome. The synteny of nine of the 22 human autosomal chromosomes (4, 5, 6, 9, 11, 14, 17, 18 and 20) and the X chromosome were found intact in the manatee. The syntenies of other human chromosomes were disrupted in the manatee genome into two to five segments. The hybridization pattern revealed that 20 (15 unique) associations of human chromosome segments are found in the manatee genome: 1/15, 1/19, 2/3 (twice), 3/7 (twice), 3/13, 3/21, 5/21, 7/16, 8/22, 10/12 (twice), 11/20, 12/22 (three times), 14/15, 16/19 and 18/19.ConclusionThere are five derived chromosome traits that strongly link elephants with manatees in Tethytheria and give implicit support to Paenungulata: the associations 2/3, 3/13, 8/22, 18/19 and the loss of the ancestral eutherian 4/8 association. It would be useful to test these conclusions with chromosome painting in hyraxes. The manatee chromosome painting data confirm that the associations 1/19 and 5/21 phylogenetically link afrotherian species and show that Afrotheria is a natural clade. The association 10/12/22 is also ubiquitous in Afrotheria (clade I), present in Laurasiatheria (clade IV), only partially present in Xenarthra (10/12, clade II) and absent in Euarchontoglires (clade III). If Afrotheria is basal to eutherians, this association could be part of the ancestral eutherian karyotype. If afrotherians are not at the root of the eutherian tree, then the 10/12/22 association could be one of a suite of derived associations linking afrotherian taxa.

[1]  Fengtang Yang,et al.  Cross-species chromosome painting unveils cytogenetic signatures for the Eulipotyphla and evidence for the polyphyly of Insectivora , 2006, Chromosome Research.

[2]  Fengtang Yang,et al.  The genome phylogeny of domestic cat, red panda and five mustelid species revealed by comparative chromosome painting and G-banding , 2004, Chromosome Research.

[3]  T. J. Robinson,et al.  Cross-species chromosome painting in the golden mole and elephant-shrew: support for the mammalian clades Afrotheria and Afroinsectiphillia but not Afroinsectivora , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[4]  Klaus-Peter Koepfli,et al.  A new phylogenetic marker, apolipoprotein B, provides compelling evidence for eutherian relationships. , 2003, Molecular phylogenetics and evolution.

[5]  M. Miyamoto,et al.  Phylogenetic assessment of molecular and morphological data for eutherian mammals. , 1999, Systematic biology.

[6]  M. Stanhope,et al.  Additional support for Afrotheria and Paenungulata, the performance of mitochondrial versus nuclear genes, and the impact of data partitions with heterogeneous base composition. , 1999, Systematic biology.

[7]  J. Thewissen,et al.  A retroposon analysis of Afrotherian phylogeny. , 2005, Molecular biology and evolution.

[8]  M. Stanhope,et al.  Molecules consolidate the placental mammal tree. , 2004, Trends in ecology & evolution.

[9]  Fengtang Yang,et al.  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 , 2006, Chromosome Research.

[10]  Gary Stone,et al.  The Ancestral Eutherian Karyotype Is Present in Xenarthra , 2006, PLoS genetics.

[11]  T. J. Robinson,et al.  Comparative molecular cytogenetic studies in the order Carnivora: mapping chromosomal rearrangements onto the phylogenetic tree , 2002, Cytogenetic and Genome Research.

[12]  M A Ferguson-Smith,et al.  Reciprocal chromosome painting among human, aardvark, and elephant (superorder Afrotheria) reveals the likely eutherian ancestral karyotype , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[13]  E. Harley,et al.  Housekeeping genes for phylogenetic analysis of eutherian relationships. , 2006, Molecular biology and evolution.

[14]  H. P. Whidden.  Extrinsic Snout Musculature in Afrotheria and Lipotyphla , 2002, Journal of Mammalian Evolution.

[15]  W. Loughman,et al.  The chromosomes of a male manatee , 1970 .

[16]  J. R. White,et al.  Some studies on blood of the Florida manatee, Trichechus manatus latirostris. , 1976, Comparative biochemistry and physiology. A, Comparative physiology.

[17]  Diana J. Kao,et al.  Molecular evidence for the monophyly of tenrecidae (mammalia) and the timing of the colonization of Madagascar by Malagasy Tenrecs. , 2002, Molecular phylogenetics and evolution.

[18]  Michael M. Miyamoto,et al.  Molecular and Morphological Supertrees for Eutherian (Placental) Mammals , 2001, Science.

[19]  M. Kiefmann,et al.  Retroposed Elements as Archives for the Evolutionary History of Placental Mammals , 2006, PLoS biology.

[20]  M. Stanhope,et al.  Highly congruent molecular support for a diverse superordinal clade of endemic African mammals. , 1998, Molecular phylogenetics and evolution.

[21]  F. Delsuc,et al.  Influence of Tertiary paleoenvironmental changes on the diversification of South American mammals: a relaxed molecular clock study within xenarthrans , 2004, BMC Evolutionary Biology.

[22]  Gary Stone,et al.  Towards the delineation of the ancestral eutherian genome organization: comparative genome maps of human and the African elephant (Loxodonta africana) generated by chromosome painting , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[23]  M. Stanhope,et al.  Molecular phylogenetic evidence confirming the Eulipotyphla concept and in support of hedgehogs as the sister group to shrews. , 2002, Molecular phylogenetics and evolution.

[24]  S. O’Brien,et al.  Molecular phylogenetics and the origins of placental mammals , 2001, Nature.

[25]  W. Murphy,et al.  Resolution of the Early Placental Mammal Radiation Using Bayesian Phylogenetics , 2001, Science.

[26]  Gary Stone,et al.  A chromosome painting test of the basal Eutherian karyotype , 2004, Chromosome Research.

[27]  R. Zori,et al.  A first generation cytogenetic ideogram for the Florida manatee (Trichechus manatus latirostris) based on multiple chromosome banding techniques , 2002 .

[28]  J. Wienberg,et al.  Reciprocal chromosome painting shows that genomic rearrangement between rat and mouse proceeds ten times faster than between humans and cats , 1999, Cytogenetic and Genome Research.

[29]  M. Mckenna.  Toward a Phylogenetic Classification of the Mammalia , 1975 .

[30]  P. Vogel,et al.  The fetal membranes of the otter shrews and a synapomorphy for afrotheria. , 2006, Placenta.

[31]  H. Künzle,et al.  Placentation in species of phylogenetic importance: the Afrotheria. , 2004, Animal reproduction science.

[32]  S. O’Brien,et al.  Molecular dating and biogeography of the early placental mammal radiation. , 2001, The Journal of heredity.

[33]  Fengtang Yang,et al.  Are molecular cytogenetics and bioinformatics suggesting diverging models of ancestral mammalian genomes? , 2006, Genome research.

[34]  P. Waddell,et al.  Evaluating placental inter-ordinal phylogenies with novel sequences including RAG1, gamma-fibrinogen, ND6, and mt-tRNA, plus MCMC-driven nucleotide, amino acid, and codon models. , 2003, Molecular phylogenetics and evolution.

[35]  M. Hasegawa,et al.  Afrotherian phylogeny as inferred from complete mitochondrial genomes. , 2003, Molecular phylogenetics and evolution.

[36]  K. Benirschke,et al.  Trichechus manatus latirostris (Manatee) , 1977 .

[37]  N. Carter,et al.  Degenerate oligonucleotide-primed PCR: general amplification of target DNA by a single degenerate primer. , 1992, Genomics.

[38]  F. Szalay,et al.  Phylogeny of the Primates , 1975, Springer US.

[39]  Pavel A Pevzner,et al.  Mammalian phylogenomics comes of age. , 2004, Trends in genetics : TIG.

[40]  S. O’Brien,et al.  Placental mammal diversification and the Cretaceous–Tertiary boundary , 2003, Proceedings of the National Academy of Sciences of the United States of America.