Analysis of Complete Mitochondrial Genomes from Extinct and Extant Rhinoceroses Reveals Lack of Phylogenetic Resolution

Overview

Journal BMC Evol Biol

Publisher Biomed Central

Specialty Biology

Date 2009 May 13

PMID 19432984

Citations 33

Authors

Eske Willerslev

M Thomas P Gilbert

Jonas Binladen

Simon Y W Ho

Paula F Campos

Aakrosh Ratan

Lynn P Tomsho

Rute R da Fonseca

Andrei Sher

Tatanya V Kuznetsova

Malgosia Nowak-Kemp

Terri L Roth

Webb Miller

Stephan C Schuster

Affiliations

Soon will be listed here.

Abstract

Background: The scientific literature contains many examples where DNA sequence analyses have been used to provide definitive answers to phylogenetic problems that traditional (non-DNA based) approaches alone have failed to resolve. One notable example concerns the rhinoceroses, a group for which several contradictory phylogenies were proposed on the basis of morphology, then apparently resolved using mitochondrial DNA fragments.

Results: In this study we report the first complete mitochondrial genome sequences of the extinct ice-age woolly rhinoceros (Coelodonta antiquitatis), and the threatened Javan (Rhinoceros sondaicus), Sumatran (Dicerorhinus sumatrensis), and black (Diceros bicornis) rhinoceroses. In combination with the previously published mitochondrial genomes of the white (Ceratotherium simum) and Indian (Rhinoceros unicornis) rhinoceroses, this data set putatively enables reconstruction of the rhinoceros phylogeny. While the six species cluster into three strongly supported sister-pairings: (i) The black/white, (ii) the woolly/Sumatran, and (iii) the Javan/Indian, resolution of the higher-level relationships has no statistical support. The phylogenetic signal from individual genes is highly diffuse, with mixed topological support from different genes. Furthermore, the choice of outgroup (horse vs tapir) has considerable effect on reconstruction of the phylogeny. The lack of resolution is suggestive of a hard polytomy at the base of crown-group Rhinocerotidae, and this is supported by an investigation of the relative branch lengths.

Conclusion: Satisfactory resolution of the rhinoceros phylogeny may not be achievable without additional analyses of substantial amounts of nuclear DNA. This study provides a compelling demonstration that, in spite of substantial sequence length, there are significant limitations with single-locus phylogenetics. We expect further examples of this to appear as next-generation, large-scale sequencing of complete mitochondrial genomes becomes commonplace in evolutionary studies. "The human factor in classification is nowhere more evident than in dealing with this superfamily (Rhinocerotoidea)." G. G. Simpson (1945).

Citing Articles

The mitochondrial genome of the mountain wooly tapir, Tapirus pinchaque and a formal test of the effect of altitude on the adaptive evolution of mitochondrial protein coding genes in odd-toed ungulates.

Gutierrez E, Ortega J, Savoie A, Baeza J BMC Genomics. 2023; 24(1):527.

PMID: 37674108 PMC: 10481570. DOI: 10.1186/s12864-023-09596-8.

Consideration of genetic variation and evolutionary history in future conservation of Indian one-horned rhinoceros (Rhinoceros unicornis).

Ghosh T, Kumar S, Sharma K, Kakati P, Sharma A, Mondol S BMC Ecol Evol. 2022; 22(1):92.

PMID: 35858827 PMC: 9301832. DOI: 10.1186/s12862-022-02045-2.

First genomic resource for an endangered neotropical mega-herbivore: the complete mitochondrial genome of the forest-dweller (Baird's) tapir ().

Ennis C, Ortega J, Baeza J PeerJ. 2022; 10:e13440.

PMID: 35669959 PMC: 9166683. DOI: 10.7717/peerj.13440.

Sesamoid bones also show functional adaptation in their microanatomy-The example of the patella in Perissodactyla.

Houssaye A, de Perthuis A, Houee G J Anat. 2021; 240(1):50-65.

PMID: 34402049 PMC: 8655183. DOI: 10.1111/joa.13530.

A first glimpse at the influence of body mass in the morphological integration of the limb long bones: an investigation in modern rhinoceroses.

Mallet C, Billet G, Houssaye A, Cornette R J Anat. 2020; 237(4):704-726.

PMID: 32519813 PMC: 7495277. DOI: 10.1111/joa.13232.

References

Gilbert M, Tomsho L, Rendulic S, Packard M, Drautz D, Sher A . Whole-genome shotgun sequencing of mitochondria from ancient hair shafts. Science. 2007; 317(5846):1927-30. DOI: 10.1126/science.1146971. View

Krause J, Dear P, Pollack J, Slatkin M, Spriggs H, Barnes I . Multiplex amplification of the mammoth mitochondrial genome and the evolution of Elephantidae. Nature. 2005; 439(7077):724-7. DOI: 10.1038/nature04432. View

Dalziel A, Moyes C, Fredriksson E, Lougheed S . Molecular evolution of cytochrome c oxidase in high-performance fish (teleostei: Scombroidei). J Mol Evol. 2006; 62(3):319-31. DOI: 10.1007/s00239-005-0110-7. View

Gilbert M, Kivisild T, Gronnow B, Andersen P, Metspalu E, Reidla M . Paleo-Eskimo mtDNA genome reveals matrilineal discontinuity in Greenland. Science. 2008; 320(5884):1787-9. DOI: 10.1126/science.1159750. View

Benton M, Donoghue P . Paleontological evidence to date the tree of life. Mol Biol Evol. 2006; 24(1):26-53. DOI: 10.1093/molbev/msl150. View

Kishino H, Hasegawa M . Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J Mol Evol. 1989; 29(2):170-9. DOI: 10.1007/BF02100115. View

Haddrath O, Baker A . Complete mitochondrial DNA genome sequences of extinct birds: ratite phylogenetics and the vicariance biogeography hypothesis. Proc Biol Sci. 2001; 268(1470):939-45. PMC: 1088691. DOI: 10.1098/rspb.2001.1587. View

Bandelt H, Dress A . Split decomposition: a new and useful approach to phylogenetic analysis of distance data. Mol Phylogenet Evol. 1992; 1(3):242-52. DOI: 10.1016/1055-7903(92)90021-8. View

Wuyts J, Perriere G, Van de Peer Y . The European ribosomal RNA database. Nucleic Acids Res. 2003; 32(Database issue):D101-3. PMC: 308799. DOI: 10.1093/nar/gkh065. View

10.

Thomas M, Hagelberg E, Jone H, Yang Z, Lister A . Molecular and morphological evidence on the phylogeny of the Elephantidae. Proc Biol Sci. 2001; 267(1461):2493-500. PMC: 1690853. DOI: 10.1098/rspb.2000.1310. View

11.

Gilbert M, Drautz D, Lesk A, Ho S, Qi J, Ratan A . Intraspecific phylogenetic analysis of Siberian woolly mammoths using complete mitochondrial genomes. Proc Natl Acad Sci U S A. 2008; 105(24):8327-32. PMC: 2423413. DOI: 10.1073/pnas.0802315105. View

12.

Ozawa T, Hayashi S, Mikhelson V . Phylogenetic position of mammoth and Steller's sea cow within Tethytheria demonstrated by mitochondrial DNA sequences. J Mol Evol. 1997; 44(4):406-13. DOI: 10.1007/pl00006160. View

13.

Tougard C, Delefosse T, Hanni C, Montgelard C . Phylogenetic relationships of the five extant Rhinoceros species (Rhinocerotidae, Perissodactyla) based on mitochondrial cytochrome b and 12S rRNA genes. Mol Phylogenet Evol. 2001; 19(1):34-44. DOI: 10.1006/mpev.2000.0903. View

14.

Shimodaira H, Hasegawa M . CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics. 2001; 17(12):1246-7. DOI: 10.1093/bioinformatics/17.12.1246. View

15.

Miller W, Drautz D, Ratan A, Pusey B, Qi J, Lesk A . Sequencing the nuclear genome of the extinct woolly mammoth. Nature. 2008; 456(7220):387-90. DOI: 10.1038/nature07446. View

16.

Xu X, Janke A, Arnason U . The complete mitochondrial DNA sequence of the greater Indian rhinoceros, Rhinoceros unicornis, and the Phylogenetic relationship among Carnivora, Perissodactyla, and Artiodactyla (+ Cetacea). Mol Biol Evol. 1996; 13(9):1167-73. DOI: 10.1093/oxfordjournals.molbev.a025681. View

17.

Drummond A, Ho S, Phillips M, Rambaut A . Relaxed phylogenetics and dating with confidence. PLoS Biol. 2006; 4(5):e88. PMC: 1395354. DOI: 10.1371/journal.pbio.0040088. View

18.

Huson D, Bryant D . Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2005; 23(2):254-67. DOI: 10.1093/molbev/msj030. View

19.

Cummings M, Otto S, Wakeley J . Sampling properties of DNA sequence data in phylogenetic analysis. Mol Biol Evol. 1995; 12(5):814-22. DOI: 10.1093/oxfordjournals.molbev.a040258. View

20.

Shepherd L, Holland B, Perrie L . Conflict amongst chloroplast DNA sequences obscures the phylogeny of a group of Asplenium ferns. Mol Phylogenet Evol. 2008; 48(1):176-87. DOI: 10.1016/j.ympev.2008.02.023. View