The new framework for understanding placental mammal evolution

BioEssays

Volumn 31, Issue 8, 2009, Pages 853-864

  Asher, Robert J ^a   Bennett, Nigel ^b   Lehmann, Thomas ^c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF PRETORIA   (South Africa)

^c SENCKENBERG RESEARCH INSTITUTE   (Germany)

Author keywords

Afrotheria; Dental eruption; Dentition; Development; Eutheria; Phylogeny; Skeleton; Vertebrae

Indexed keywords

AFROTHERIA; CANCER RISK; DEVELOPMENTAL STAGE; EDENTATA; EUARCHONTOLOGLIRES; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; LAURASIATHERIA; MAMMAL; NONHUMAN; PHENOTYPE; PHYLOGENY; PLACENTAL MAMMALS; REVIEW; SPECIES DIFFERENCE; TAXONOMIC RANK; TOOTH DEVELOPMENT; TOOTH SIZE;

ANIMALS; DENTITION; EVOLUTION; FEMALE; MAMMALS; PHYLOGENY; PLACENTA; PREGNANCY; SPINE;

AFROTHERIA; DERMOPTERA; ELEPHANTIDAE; EQUIDAE; EUARCHONTOGLIRES; EUTHERIA; MYRMECOPHAGIDAE; ORYCTEROPODIDAE; RODENTIA; SLOTHS; SORICIDAE;

EID: 70349973873     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.200900053     Document Type: Review

References (115)

1. Sarich, V. M., Mammalian systematics: twenty-five years among their albumins and transferrins. In: Szalay, F. S., Novacek, M. J. and McKenna, M. C. editors. Mammal Phylogeny: Placentals. New York, Springer, 1993. pp. 103-114.
2. Prothero, D. R. and Buell, C. D., Evolution: what the fossils say and why it matters. New York, Columbia University Press, 2007. p. 381
3. Butler, P. M., Phylogeny of the insectivores. In: Benton, M. J. editor. The Phylogeny and Classification of the Tetrapods, Vol 2. Oxford, Clarendon Press, 1988. pp. 117-141.
4. Fischer, M. S., Hyracoids, the sister-group of perissodactyls. In: Prothero, D. R. and Schoch, R. M. editors. The Evolution of Perissodactyls. New York, Oxford, 1989. pp. 37-56.
5. Pettigrew, J. D., Maseko, B. C. and Manger, P. R., Primate-like retinotectal decussation in an echolocating megabat, Rousettus aegyptiacus. Neuroscience 2008. 153: 226-231.
6. Hallstrom, B. M., Kullberg, M., Nilsson, M. A. and Janke, A., Phylogenomic data analyses provide evidence that Xenarthra and Afrotheria are sister groups. Mol Biol Evol 2007. 24: 2059-2068.
7. Murphy, W. J., Pringle, T. H., Crider, T. A., Springer, M. S. and Miller, W., Using genomic data to unravel the root of the placental mammal phylogeny. Genome Res 2007. 17: 413-421.
8. Nikolaev, S., Montoya-Burgos, J. I., Margulies, E. H., Program, N. C. S., Rougemont, J., et al. Early history of mammals is elucidated with the ENCODE multiple species sequencing data. PLoS Genet 2007. 3: e2.
9. Wildman, D. E., Uddin, M., Opazo, J. C., Liu, G., Lefort, V., et al. Genomics, biogeography, and the diversification of placental mammals. Proc Natl Acad Sci USA 2007. 104: 14395-14400.
10. Gatesy, J., Baker, R. H. and Hayashi, C., Inconsistencies in arguments for the supertree approach: Supermatrices versus supertrees of Crocodylia. Syst Biol 2004. 53: 342-355.
11. Bininda-Emonds, O. R., Cardillo, M., Jones, K. E., MacPhee, R. D., Beck, R. M., et al. The delayed rise of present-day mammals. Nature 2007. 446: 501-512.
12. Novacek, M. J. and AToL Mammal Morphology Team. A team-based approach yields a new matrix of 4500 morphological characters for mammalian phylogeny. J Vert Paleo 2008. 28: 121A.
13. Cannarozzi, G., Schneider, A. and Gonnet, G., A phylogenomic study of human, dog, and mouse. PLoS Comput Biol 2007. 3: e2.
14. Huttley, G. A., Wakefield, M. J. and Easteal, S., Rates of genome evolution and branching order from whole genome analysis. Mol Biol Evol 2007. 24: 1722-1730.
15. Prasad, A. B. Allard, M. W., NISC Comparative Sequencing Program and Green, E. D., Confirming the phylogeny of mammals by use of large comparative sequence data sets. Mol Biol Evol 2008. 25: 1795-1808.
16. Churakov, G., Kriegs, J. O., Baertsch, R., Zemann, A., Brosius, J. and Schmitz, J., Mosaic Retroposon Insertion Patterns in Placental Mammals. Genome Res 2009.
17. Kjer, K. M. and Honeycutt, R. L., Site specific rates of mitochondrial genomes and the phylogeny of eutheria. BMC Evol Biol 2007. 7: 8.
18. Arnason, U., Adegoke, J. A., Gullberg, A., Harley, E. H., Janke, A. and Kullberg, M., Mitogenomic relationships of placental mammals and molecular estimates of their divergences. Gene 2008. 421: 37-51.
19. Ruiz-Herrera, A. and Robinson, T. C., Chromosomal instability in Afrotheria: fragile sites, evolutionary breakpoints and phylogenetic inference from genome sequence assemblies. BMC Evol Biol 2007. 7: 199.
20. Waddell, P. J., Okada, N. and Hasegawa, M., Towards resolving the interordinal relationships of placental mammals. Syst Biol 1999. 48: 1-5.
21. Murphy, W. J., Eizirik, E., Johnson, W. E., Zhang, Y. P., Ryder, O. A. and O'Brien, S. J., Molecular phylogenetics and the origins of placental mammals. Nature 2001. 409: 614-618.
22. Murphy, W. J., Eizirik, E., O'Brien, S. J., Madsen, O., Scally, M., et al. Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 2001. 294: 2348-2351.
23. Madsen, O., Scally, M., Douady, C. J., Kao, D. J., DeBry, R. W., et al. Parallel adaptive radiations in two major clades of placental mammals. Nature 2001. 409: 610-614.
24. Gregory, W. K., The Orders of Mammals. Bull Am Mus Nat Hist 1910. 27: 1-524.
25. Simpson, G. G., The principles of classification and a classification of mammals. Bull Am Mus Nat Hist 1945. 85: 1-350.
26. McKenna, M. C., Toward a phylogeny and classification of the Mammalia. In: Luckett, W. P. and Szalay, F. S. editors. Phylogeny of the Primates: A Multidisciplinary Approach. New York, Plenum, 1975. pp. 21-46.
27. Novacek, M. J., Mammalian phylogeny: Shaking the tree. Nature 1992. 356: 121-125.
28. Archibald, J. D., Timing and biogeography of the eutherian radiation: Fossils and molecules compared. Mol Phylogenet Evol 2003. 28: 350-359.
29. Hallstrom, B. M. and Janke, A., Resolution among major placental mammal interordinal relationships with genome data imply that speciation influenced their earliest radiations. BMC Evol Biol 2008. 8: 162.
30. Nishihara, H., Maruyama, S. and Okada, N., Retroposon analysis and recent geological data suggest near-simultaneous divergence of the three superorders of mammals. Proc Natl Acad Sci USA 2009.
31. Kriegs, J. O., Churakov, G., Kiefmann, M., Jordan, U., Brosius, J. and Schmitz, J., Retroposed elements as archives for the evolutionary history of placental mammals. PLoS Biol 2006. 4: e91.
32. Roca, A. L., Bar-Gal, G. K., Eizirik, E., Helgen, K. M., Maria, R., et al. Mesozoic origin for West Indian insectivores. Nature 2004. 429: 649-651.
33. Asher, R. J., A web-database of mammalian morphology and a reanalysis of placental phylogeny. BMC Evol Biol 2007. 7: 108.
34. Arnason, U., Adegoke, J. A., Bodin, K., Born, E. W., Esa, Y. B., et al. Mammalian mitogenomic relationships and the root of the eutherian tree. Proc Natl Acad Sci USA 2002. 99: 8151-8156.
35. Asher, R. J., Novacek, M. J. and Geisler, J., Relationships of Endemic African Mammals and their Fossil Relatives based on Morphological and Molecular Evidence. J Mammal Evol 2003. 10: 131-194.
36. Kullberg, M., Nilsson, M. A., Arnason, U., Harley, E. H. and Janke, A., Housekeeping genes for phylogenetic analysis of eutherian relationships. Mol Biol Evol 2006. 23: 1493-1503.
37. Amrine-Madsen, H., Koepfli, K. P., Wayne, R. K. and Springer, M. S., A new phylogenetic marker, apolipoprotein B, provides compelling evidence for eutherian relationships. Mol Phylogenet Evol 2003. 28: 225-240.
38. Nishihara, H., Hasegawa, M. and Okada, N., Pegasoferae, an unexpected mammalian clade revealed by tracking ancient retroposon insertions. Proc Natl Acad Sci USA 2006. 103: 9929-9934.
39. Beard, K. C., Phylogenetic systematics of the Primatomorpha, with special reference to Dermoptera. In: Szalay, F. S., Novacek, M. J. and McKenna, M. C. editors. Mammal Phylogeny: Placentals, New York, Springer, 1993. pp. 129-150.
40. Waddell, P. J. and Shelley, S., 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. Mol Phylogenet Evol 2003. 28: 197-224.
41. Janecka, J. E., Miller, W., Pringle, T. H., Wiens, F., Zitzmann, A., et al. Molecular and genomic data identify the closest living relative of primates. Science 318: 792-794.
42. Schmitz, J., Ohme, M. and Zischler, H., SINE insertions in cladistic analyses and the phylogenetic affiliations of Tarsius bancanus to other primates. Genetics 2001. 157: 777-784.
43. Schmitz, J., Roos, C. and Zischler, H., Primate phylogeny: molecular evidence from retroposons. Cytogenet Genome Res 2005. 108: 26-37.
44. Ni, X., Wang, Y., Hu, Y. and Li, C., A euprimate skull from the early Eocene of China. Nature 2004. 427: 65-68.
45. Bloch, J. I., Silcox, M. T., Boyer, D. M. and Sargis, E. J., New Paleocene skeletons and the relationship of plesiadapiforms to crown-clade primates. Proc Natl Acad Sci USA 2007. 104: 1159-1164.
46. Nie, W., Fu, B., O'Brien, P. C., Wang, J., Su, W., et al. Flying lemurs - the 'flying tree shrews'? Molecular cytogenetic evidence for a Scandentia-Dermoptera sister clade. BMC Biology 2008. 6: 18.
47. Olson, L. E., Sargis, E. J. and Martin, R. D., Intraordinal phylogenetics of treeshrews (Mammalia: Scandentia) based on evidence from the mitochondrial 12S rRNA gene. Mol Phylogenet Evol 2005. 35: 656-673.
48. Tabuce, R., Asher, R. and Lehmann, T., Afrotherian mammals: A review of current data. Mammalia 2008. 72: 2-14.
49. Robinson, T. J., Ruiz-Herrera, A. and Avise, J. C., Hemiplasy and homoplasy in the karyotypic phylogenies of mammals. Proc Natl Acad Sci USA 2008. 105: 14477-14481.
50. Seiffert, E., A new estimate of afrotherian phylogeny based on simultaneous analysis of genomic, morphological, and fossil evidence. BMC Evol Biol 2007. 7: 13.
51. Gill, T., On the relations of the orders of mammals. Science 1870. 267-270.
52. Fischer, M. S. and Tassy, P., The interrelation between Proboscidea, Sirenia, Hyracoidea, and Mesaxonia: the morphological evidence. In: Szalay, F. S., Novacek, M. J. and McKenna, M. C. editors. Mammal Phylogeny: Placentals. New York, Springer, 1993. pp. 217-234.
53. Linnaeus Cv. 1758., Systema naturae: Regnum animale. a photographic facsimile of the first volume of the tenth edition. London, British Museum, 1956.
54. Andrews, C. W., A Descriptive Catalogue of the Tertiary Vertebrata of the Fayum, Egypt. London, British Museum (Natural History), 1906.
55. Nikaido, M., Cao, Y., Harada, M., Okada, N. and Hasegawa, M., Mitochondrial phylogeny of hedgehogs and monophyly of Eulipotyphla. Mol Phylogenet Evol 2003. 28: 276-284.
56. Gaeth, A. P., Short, R. V. and Renfree, M. B., The developing renal, reproductive, and respiratory systems of the African elephant suggest an aquatic ancestry. Proc Natl Acad Sci USA 1999. 96: 5555-5558.
57. Liu, A. G., Seiffert, E. R. and Simons, E. L., Stable isotope evidence for an amphibious phase in early proboscidean evolution. Proc Natl Acad Sci USA 2008. 105: 5786-5791.
58. Asher, R. J. and Seiffert, E. R., Systematics of Endemic African Mammals. In: Werdelin, L. and Sanders, W. editors. Cenozoic Mammals of Africa. Berkeley, University of California Press, In Press.
59. Domning, D. P., The earliest known fully quadrupedal sirenian. Nature 2001. 413: 625-627.
60. Gheerbrant, E., Sudre, J., Cappetta, H., Iarochene, M., Amaghzaz, M. and Bouya, B., A new large mammal from the Ypresian of Morocco: Evidence of surprising diversity of early proboscideans. Acta Palaeontol Pol 2002. 47: 493-506.
61. Gheerbrant, E., Peigne, S. and Thomas, H., First description of the skeleton of a paleogene hyracoid: Saghatherium antiquum from the early Oligocene of Jebel al Hasawnah, Libya. Palaeontographica Abteilung a- Palaozoologie-Stratigraphie 2007. 279: 93-145.
62. Cote, S., Werdelin, L., Seiffert, E. R. and Barry, J. C., Additional material of the enigmatic Early Miocene mammal Kelba and its relationship to the order Ptolemaiida. Proc Natl Acad Sci USA 2007. 104: 5510-5515.
63. Seiffert, E. R., Simons, E. L., Ryan, T. M., Bown, T. M. and Attia, Y., New remains of Eocene and Oligocene Afrosoricida (Afrotheria) from Egypt, with implications for the origin(s) of afrosoricid zalambdodonty. J Vert Paleontol 2007. 27: 963-972.
64. Tabuce, R., Marivaux, L., Adaci,M., Bensalah,M., Hartenberger, J. L., et al. Early tertiary mammals from north Africa reinforce the molecular afrotheria clade. Proc Royal Soc B-Biol Sci 2007. 274: 1159-1166.
65. Lehmann, T., Phylogeny and systematics of the Orycteropodidae (Mammalia, Tubulidentata). Zool J Linn Soc 2009. 155: 649-702.
66. Asher, R. J. and Lehmann, T., Dental eruption in afrotherian mammals. BMC Biol 2008. 6: 14.
67. Asher, R. J. and Olbricht, G., Dental ontogeny in Macroscelides proboscideus (Afrotheria) and Erinaceus europaeus (Lipotyphla). J Mammalian Evol 2009. 16: 99-115.
68. Sanchez-Villagra, M. R., Narita, Y. and Kuratani, S., Thoracolumbar vertebral number: the first skeletal synapomorphy for afrotherian mammals. Syst Biodivers 2007. 5: 1-17.
69. Buchholtz, E. A. and Stepien, C. C., Anatomical transformation in mammals: developmental origin of aberrant cervical anatomy in tree sloths. Evol Dev 2009. 11: 69-79.
70. Werdelin, L. and Nilsonne, A., The evolution of the scrotum and testicular descent in mammals: a phylogenetic view. J The Biol 1999. 196: 61-72.
71. Mess, A. and Carter, A. M., Evolutionary transformations of fetal membrane characters in Eutheria with special reference to Afrotheria. J Exp Zool B Mol Dev Evol 2006. 306: 140-163.
72. Shigehara, N., Epiphyseal union, tooth eruption, and sexual maturation in the common tree shrew, with reference to its systematic problem. Primates 1980. 21: 1-19.
73. Smith, B. H., "Schultz's Rule" and the evolution of tooth replacement patterns in primates and ungulates. In: Teaford, M., Smith, M. and Ferguson, M. editors. Development, Function and Evolution of Teeth. Cambridge: Cambridge University Press. 2000. pp. 212-227.
74. Kellas, L., Observations on the reproductive activity measurement and growth-rate of the dik-dik. Proc Zool Soc Lond 1955. 124: 751-784.
75. Laws, R., Age criteria for the African elephant Loxodonta africana. East Afr Wildl J 1966. 4: 1-37.
76. Van Nievelt, A. F. and Smith, K. K., To replace or not to replace: the significance of reduced tooth replacement in marsupial and placental mammals. Paleobiology 2005. 31: 324-346.
77. Roche, J., Denture et age des Damans de rochers (genre Procavia). Mammalia 1978. 42: 97-103.
78. Domning, D. P. and Hayek, L., Horizontal tooth replacement in the Amazonian Manatee (Trichechus inunguis). Mammalia 1984. 48: 105-127.
79. Leche, W., Zur Entwicklungsgeschichte des Zahnsystems der Säugetiere, zugleich ein Beitrag zur Stammesgeschichte dieser Tiergruppe, Teil 2. Zoologica (Stuttgart) 1907. 49: 1-157.
80. Reeve, N., Hedgehogs. Cambridge, UK: Cambridge University Press. 1994. p. 313.
81. Martin, B. E., Tooth development in Dasypus novemcinctus. J Morphology 1916. 27: 647-691.
82. Hensel, R., Beiträge zur Kenntniss der Säugethiere Süd-Brasiliens. Berlin, Abhandl. König. Akad. Wiss, pp. 1-130. 1872.
83. Beatty, B., Craniodental ontogeny in the Desmostylia. J Vert Paleontol 2008. 283: 49A.
84. Holroyd, P., New data on dental eruption patterns in condylarths and afrotheres. J Vert Paleontol 2008. 283: 93A.
85. Simpson, G. G., The beginning of the age of mammals in South America, part 2. Bull Am Mus Nat Hist 1967. 137: 1-260.
86. Laws, R., Dentition and ageing in the hippopotamus. East Afr Wildl J 1968. 6: 19-52.
87. Robinette, W., Jones, D., Rogers, G. and Gashwiler, J., Notes of tooth development and wear for Rocky Mountain mule deer. J Wildlife Management 1957. 21: 134-153.
88. Kellas, L., Observations on the reproductive activity, measurement and growth-rate of the dik-dik. Proc Zool Soc Lond 1955. 124:751-784.
89. Narita, Y. and Kuratani, S., Evolution of the vertebral formulae in mammals: A perspective on developmental constraints. J Exp Zool B Mol Dev Evol 2005. 304: 91-106.
90. Sánchez-Villagra, M. R., Narita, Y. and Kuratani, S., Thoracolumbar vertebral number: the first skeletal synapomorphy for afrotherian mammals. Syst Biodiver 2007. 5: 1-7.
91. Galis, F., Why do almost all mammals have seven cervical vertebrae? Developmental constraints, Hox genes and Cancer. J Exp Zool 1999. 285: 19-26.
92. Galis, F., Van Dooren, T. J., Feuth, J. D., Metz, J. A., Witkam, A., et al. Extreme selection in humans against homeotic transformations of cervical vertebrae. Evolution 2006. 60: 2643-2654.
93. Buchholtz, E. A., Booth, A. C. and Webbink, K. E., Vertebral anatomy in the Florida manatee, Trichechus manatus latirostris: a developmental and evolutionary analysis. Anat Rec (Hoboken) 2007. 290: 624-637.
94. Burke, A. C. and Nowicki, J. L., A new view of patterning domains in the vertebrate mesoderm. Dev Cell 2003. 4: 159-165.
95. Durland, J. L., Sferlazzo, M., Logan, M. and Burke, A. C., Visualizing the lateral somitic frontier in the Prx1Cre transgenic mouse. J Anat 2008. 212: 590-602.
96. Shearman, R. M. and Burke, A. C., The lateral somitic frontier in ontogeny and phylogeny. J Exp Zoolog B Mol Dev Evol 2008.
97. Owen, R., Descriptive catalogue of the osteological series contained in the museum of the Royal College of Surgeons of England. London, Royal College of Surgeons. 1853.
98. Bornstein, P. E. and Peterson, R. R., Numerical variation of the presacral vertebral column in three population groups in North America. Am J Phys Anthropol 1966. 25: 139-146.
99. Mundlos, S., Cleidocranial dysplasia: clinical and molecular genetics. J Med Genet 1999. 36: 177-182.
100. Otto, F., Kanegane, H. and Mundlos, S., Mutations in the RUNX2 gene in patients with cleidocranial dysplasia. Hum Mutat 2002. 19: 209-216.
101. Aberg, T., Wang, X. P., Kim, J. H., Yamashiro, T., Bei, M., et al. Runx2 mediates FGF signaling from epithelium to mesenchyme during tooth morphogenesis. Dev Biol 2004. 270: 76-93.
102. Wang, X. P., Aberg, T., James, M. J., Levanon, D., Groner, Y. and Thesleff, I., Runx2 (Cbfa1) inhibits Shh signaling in the lower but not upper molars of mouse embryos and prevents the budding of putative successional teeth. J Dent Res 2005. 84: 138-143.
103. Fondon, J. W., 3rd and Garner, H. R., Molecular origins of rapid and continuous morphological evolution. Proc Natl Acad Sci USA 2004. 101: 18058-18063.
104. Sears, K. E., Goswami, A., Flynn, J. J. and Niswander, L. A., The correlated evolution of Runx2 tandem repeats, transcriptional activity, and facial length in carnivora. Evol Dev 2007. 9: 555-565.
105. Huxley, T. H., On the application of the laws of evolution to the arrangement of the Vertebrata and more particularly to the Mammalia. Proc Zool Soc London 1880. 1880: 649-662.
106. Bonaparte, C. L., A new systematic arrangement of the vertebrated animals. Trans Linn Soc 1837. 18: 247-304.
107. Asher, R. J., Insectivoran grade placental mammals: character evolution and fossil history. In: Rose, K. D. and Archibald, D. editors. The Rise of Placental Mammals: Origin and Relationships of the Major Clades. Johns Hopkins University Press, 2005. pp. 50-70.
108. Stanhope, M. J., Waddell, V. G., Madsen, O., de Jong, W., Hedges, S. B., et al. Molecular evidence for multiple origins of Insectivora and for a new order of endemic African insectivore mammals. Proc Natl Acad Sci USA 1998. 95: 9967-9972.
109. Waddell, P. J., Kishino, H. and Ota, R., A phylogenetic foundation for comparative mammalian genomics. Genome Inform 2001. 12: 141-154.
110. Springer, M. S., Murphy, W. J., Eizirik, E., Madsen, O., Scally, M., et al. A molecular classification for the living orders of placental mammals of the phylogenetic placement of primates. In: Ravosa, M. J. and Dagosto, M. editors. Primate Origins: Adaptations and Evolution. New York: Springer, 2007. pp. 1-28.
111. McDowell, S. B., The Greater Antillean insectivores. Bull Am Mus Nat Hist 1958. 115: 115-213.
112. McKenna, M. C. and Bell, S. K., Classification of Mammals Above the Species Level. New York, Columbia University Press, 1997. p. 631
113. Owen, R., Report on the archetype and homologies of the vertebrate skeleton. Rep Brit Assoc Adv Sci 1847. 1846: 169-340.
114. Montgelard, C., Catzeflis, F. and Douzery, E., Phylogenetic relationships of artiodactyls and cetaceans as deduced from the comparison of cytochrome b and 12S rRNA mitochondrial sequences. Mol Biol Evol 1997. 14: 550-559.
115. Haeckel, E., Generelle Morphologie der Organismen; Allgemeine Grundzuege der organischen Formen-Wissenschaft, mechanisch begruendet durch die von Charles Darwin reformierte Descendenz-Theorie. Berlin, Georg Reimer, 1866.