Journal of Mammalian Evolution

, Volume 11, Issue 2, pp 73–104 | Cite as

The Tarsal Complex of Afro-Malagasy Tenrecoidea: A Search for Phylogenetically Meaningful Characters

  • Justine A. Salton
  • Frederick S. Szalay


Morphological characters should be assessed in an ecological and evolutionary framework before their use in phylogenetic analyses. We have attempted such an assessment for the tarsal complex of the Tenrecoidea. The 30+/− extant species of these small mammals live in a diverse range of microhabitats. They exhibit markedly different positional behaviors, encompassing four basic locomotor repertoires: terrestrial running and walking, scansorial climbing, digging, and swimming. Articular surfaces from the upper, middle, and lower ankle joints in 10 Malagasy tenrecid, 1 potamogalid, 1 solenodontid, and 1 macroscelidid species were compared. The results were tested against published data on the correlation between function and morphology in other therian locomotor specialists. Descriptive accounts, supported by quantitative analyses, demonstrate significant differences in many aspects of tarsal morphology that may be explained by function-based hypotheses within the context of the tenrecoid heritage. Three closely related tenrecines (Hemicentetes, Setifer, and Echinops) show divergences in form that are consistent with their respective semifossorial, terrestrial, and scansorial/arboreal modes of locomotion. In addition to functional–adaptive considerations, we propose several synapomorphies for the tenrecine and oryzorictine clades that appear to corroborate their monophyly. There are apparent convergences between the habitual diggers from different subfamilies (Hemicentetes and Oryzorictes), and there are adaptive differences within subfamilies (e.g. arboreal Echinops vs. terrestrial Setifer). The few likenesses between Potamogale and Limnogale cannot be supported as homologies, and the proposal of a recent phylogenetic affiliation between them is therefore rejected here. Manifest differences in tarsal form between Geogale and the oryzorictines support recognition of the subfamily Geogalinae. As expected, the tarsal complex of Solenodon is fundamentally unlike that of the tenrecoids. Finally, the similarities in detail between Macroscelididae and Potamogalidae reflect the stabilization of UAJ during plantarflexion, and therefore such attributes are rejected as synapomorphies. Traits with clear species-specific adaptations are a potential interference in cladistic analyses and cannot be meaningfully used without ecology-based character assessment. While this practice may ultimately reduce the size of a database, it will nonetheless result in taxonomic properties with lasting value against which phylogenetic hypotheses may be tested with confidence.

Afrotheria ecomorphology evolutionary morphology Insectivora tenrecs tarsals 


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  1. Allen, G. M. (1910). Solenodon paradoxus. Mem. Mus. Comp. Zool. 62133–148.Google Scholar
  2. Argot, C. (2002). Functional–adaptive analysis of the hindlimb anatomy of extant marsupials and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus. J. Morphol. 253:76–108.Google Scholar
  3. Asher, R. J. (1999). A morphological basis for assessing the phylogeny of the “Tenrecoidea” (Mammalia, Lipo-typhla). Cladistics 15:231–252.Google Scholar
  4. Asher, R. J. (2000). Phylogenetic History of Tenrecs and Other Insectivoran Mammals, PhD Dissertation, State University of New York, Stony Brook.Google Scholar
  5. Barnett, C. H. (1970). Talocalcaneal movements in mammals. J. Zool. 160:1–7.Google Scholar
  6. Benstead, J. P., Barnes, K. H., and Pringle, C. M. (2001). Diet, activity patterns, foraging movement and responses to deforestation of the aquatic tenrec, Limnogale mergulus (Lipotyphla: Tenrecidae) in eastern Madagascar. J. Zool. 254:119–129.Google Scholar
  7. Bock, W. J. (1981). Functional–adaptive analysis in evolutionary classification. Am. Zool. 21:5–20.Google Scholar
  8. Butler, P. M. (1969). Insectivores and bats from the Miocene of East Africa: New material. In: Fossil Vertebrates from Africa, L. S. B. Leakey, ed., pp. 1–37, Academic Press, London.Google Scholar
  9. Cabrera, A. (1925). Genera mammalium: Insectivora, Galaeopitheca. Museo Nacional de Ciencias Naturales, Madrid.Google Scholar
  10. Carrano, M. T. (1997). Morphological indicators of foot posture in mammals: A statistical and biomechanical analysis. Zool. J. Linn. Soc. 121:77–104.Google Scholar
  11. Conroy, G. C., and Rose, M. D., (1993). The evolution of the primate foot from the earliest primates to the Miocene hominoids. Foot Ankle 3:342–364.Google Scholar
  12. Cifelli, R. L. (1983). Eutherian tarsals from the late Paleocene of Brazil. Am. Mus. Novit. 2761:1–31.Google Scholar
  13. Dagosto, M. (1985). The distal tibia of primates with special to the Omomyidae. Int. J. Primatol. 6:45–75.Google Scholar
  14. Dagosto, M. (1986). The Joints of the Tarsus in the Strepsirhine Primates, PhD Dissertation, City University of New York.Google Scholar
  15. Dagosto, M. (1988). Implications of postcranial evidence for the origin of euprimates. J. Hum. Evol. 17:35–56.Google Scholar
  16. Davis, L. C. (1996). Functional and phylogenetic implications of ankle morphology in Goeldi's monkey (Callimico goeldii). In: Adaptive Radiations of Neotropical Primates, M. A. Norconk, A. L. Rosenberger, and P. A. Garber, eds., pp. 133–156, Plenum Press, New York.Google Scholar
  17. Decker, R. L., and Szalay, F. S. (1974). Origin and function of the pes in the Eocene adapids. In: Primate Locomotion, F. A. Jenkins Jr., ed., pp. 261–291, Academic Press, New York.Google Scholar
  18. Dobson, G. E. (1882). A Monograph of the Insectivora, Systematic and Anatomical, J. Van Voorst, London.Google Scholar
  19. Douady, C. J., Catzeflis, F., Kao, D. J., Springer, M. S., and Stanhope, M. J. (2002). Molecular evidence for the monophyly of Tenrecidae (Mammalia) and the timing of the colonization of Madagascar by Malagasy tenrecs. Mol. Phylogenet. Evol. 22:357–363.Google Scholar
  20. Eisenberg, J. F., and Gould, E. (1966). The behavior of Solenodon paradoxus in captivity with comments of the behavior of other insectivora. Zool. N.Y. 51:49–58.Google Scholar
  21. Eisenberg, J. F., and Gould, E. (1970). The Tenrecs: A Study in Mammalian Behavior and Evolution, Smithsonian Institution Press, Washington, DC.Google Scholar
  22. Emerson, G. L., Kilpatrick, C. W., McNiff, B. E., Ottenwalder, J., and Allard, M. W. (1999). Phylogenetic relationships of the order Insectivora based on complete 12SrRNA sequences from mitochondria. Cladistics 15:221–230.Google Scholar
  23. Fleagle, J. G. (1988). Primate Adaptation and Evolution, 2nd edn., Academic Press, San Diego, CA.Google Scholar
  24. Gebo, D. L. (1993). Functional morphology of the foot in primates. In: Postcranial Adaptation in Non-Human Primates, D. L. Gebo, ed., pp. 121–149, Northern Illinois University Press, DeKalb.Google Scholar
  25. Gebo, D. L., and Dagosto, M. (1988). Foot anatomy, climbing, and the origin of the Indriidae. J. Hum. Evol. 17:135–154.Google Scholar
  26. Gebo, D. L., Dagosto, M., Beard, K. C., and Qi, T. (2001). Middle Eocene primate tarsals from China: Implications for haplorhine evolution. Am. J. Phys. Anthropol. 116:83–107.Google Scholar
  27. Godinot, M., and Dagosto, M. (1983). The astragalus of Necrolemur (Primates, Microchoerinae). J. Paleontol. 57:1321–1324.Google Scholar
  28. Hildebrand, M. (1995). Analysis of Vertebrate Structure, 5th ed., Wiley, New York.Google Scholar
  29. Honegger, R. E., and Noth, W. (1965). Beobachtungen bei der Aufzucht von Igeltanreks Echinops telfairi. Zoologische Beiträge 13:191–218.Google Scholar
  30. Hooker, J. J. (2001). Tarsals of extinct family Nyctitheriidae (Mammalia): Evidence for archontan relationships. Zool. J. Linn. Soc. 132:501–529.Google Scholar
  31. Jenkins, P. D., Goodman, S. M., and Raxworthy, C. J. (1996). The shrew tenrecs (Microgale) (Insectivora: Tenrecidae) of the Reserve Naturelle Integrale d'Andingitra, Madagascar. Fieldiana Zool. 85:191–217.Google Scholar
  32. Jenkins, F. A., and McClearn, D. (1984). Mechanisms of hind foot reversal in climbing mammals. J. Morphol. 182:197–219.Google Scholar
  33. Kemp, T. S. (1982). Mammal-Like Reptiles and the Origin of Mammals, Academic Press, London.Google Scholar
  34. Lewis, O. J. (1962). The homologies of the mammalian tarsal bones. J. Anat. 98:195–208.Google Scholar
  35. Lewis, O. J. (1989). Functional Morphology of the Evolving Hand and Foot, Oxford University Press, New York.Google Scholar
  36. MacPhee, R. D. E. (1987). The shrew tenrecs of Madagascar: Systematic revision and Holocene distribution of Microgale (Tenrecidae, Insectivora). Am. Mus. Novit. 2889:1–45.Google Scholar
  37. Martinez, J.-N., and Sudre, J. (1995). The astragalus of Paleogene artiodactyls: Comparative morphology, vari-ability and prediction of body mass. Lethaia 28:197–209.Google Scholar
  38. McDowell, S. B. (1958). The Greater Antillean insectivores. Bull. Am. Mus. Nat. Hist. 115:113–214.Google Scholar
  39. McKenna, M. C., and Bell, S. K. (1997). Classification of Mammals Above the Species Level, Columbia University Press, New York.Google Scholar
  40. de Muizon, C., Cifelli, R. L., and Bergqvist, L. P. (1998). Eutherian tarsals from the early Paleocene of Bolivia. J. Vertebr. Paleontol. 18:655–663.Google Scholar
  41. Neveu, P., and Gasc, J.-P. (2002). Lipotyphla limb myology comparison. J. Morphol. 252:183–201.Google Scholar
  42. Nowak, R. M. (1999). Walker's Mammals of the World, 6th edn., The Johns Hopkins University Press, Baltimore.Google Scholar
  43. Olson, L. E., and Goodman, S. M. (2004). Phylogeny of Madagascar's tenrecs (Lipotyphla, Tenrecidae). In: The Natural History of Madagascar, S. M. Goodman, J. P. Benstead, and H. Schutz, eds., pp. 1235–1242, University of Chicago Press, Chicago.Google Scholar
  44. Prasad, G. V. R., and Godinot, M. (1994). Eutherian tarsal bones from the late Cretaceous of India. J. Paleontol. 68:892–902.Google Scholar
  45. Rose, K. D. (1999). Postcranial skeleton of Eocene Leptictidae (Mammalia), and its implications for behavior and relationships. J. Vertebr. Paleontol. 19:355–372.Google Scholar
  46. Romankowowa, A. (1963). Comparative study of the structure of the os calcaneus in insectivores and rodents. Acta Theriol. 7:91–126.Google Scholar
  47. Sargis, E. J. (2002). Functional morphology of the hindlimb of tupaiids (Mammalia, Scandentia) and its phyloge-netic implications. J. Morphol. 254:149–185.Google Scholar
  48. Seiffert, E. R., and Simons, E. L. (2001). Astragalar morphology of the late Eocene anthropoids from the Fayum Depression (Egypt) and the origin of catarrhine primates. J. Hum. Evol. 41:577–606.Google Scholar
  49. Simpson, G. G. (1945). The principles of classification and a classification of mammals. Bull. Am. Mus. Nat. Hist. 59:1–350.Google Scholar
  50. Solomon, E. P., Schmidt, R. R., and Adragnsa, P. J. (1990). Human Anatomy and Physiology, Harcourt Brace Jovanovich, Orlando.Google Scholar
  51. Stains, H. (1973). Comparative study of the calcanea of members of the Ursidae and Procyonidae. Bull. South. Calif. Acad. Sci. 72:137–147.Google Scholar
  52. Stains, H. (1975). Calcanea of members of the Canidae. Bull. South. Calif. Acad. Sci. 74:143–155.Google Scholar
  53. Stein, B. (2000). Morphology of subterranean rodents. In: Life Underground: The Biology of Subterranean Rodents, E. A. Lacey, J. L. Patton, and G. N. Cameron, eds., pp. 19–61, University of Chicago Press, Chicago.Google Scholar
  54. Springer, M. S., Cleven, G. C., Madsen, O., de Jong, W. W., Waddell, V. G., Amrine, H. M., and Stanhope, M. J. (1997). Endemic African mammals shake the phylogenetic tree. Nature 388:61–64.Google Scholar
  55. Stephenson, P. J. (1995). Taxonomy of shrew tenrecs (Microgale spp.) from eastern and central Madagascar. J. Zool. Lond. 235:339–350.Google Scholar
  56. Stanhope, M. J., Waddell, V. G., Madsen, O., de Jong, W., Hedges, S. B., Cleven, G. C., Kao, D., and Springer, M. S. (1998). Molecular evidence for multiple origins of Insectivora and for a new order of endemic African insectivore mammals. Proc. Natl. Acad. Sci. U.S.A. 95:9967–9972.Google Scholar
  57. Strasser, E. (1988). Pedal evidence for the origin and diversification of cecopithecid clades. J. Hum. Evol. 17:225–245.Google Scholar
  58. Szalay, F. S. (1966). The tarsus if the Paleocene leptictid Prodiacodon (Insectivora, Mammalia). Am. Mus. Novit. 2267:1–13.Google Scholar
  59. Szalay, F. S. (1977). Phylogenetic relationships and a classification of the eutherian Mammalla. In: Major Patterns in Vertebrate Evolution, M. K, Hecht, P. C. Goody, and B. M. Hecht, eds., pp. 315–374, Plenum Press, New York.Google Scholar
  60. Szalay, F. S. (1984). Arboreality: Is it homologous in metatherian and eutherian mammals? Evol. Biol. 18:215–258.Google Scholar
  61. Szalay, F. S. (1985). Rodent and lagomorph morphotype adaptations, origins, and relationships: Some postcranial attributes analyzed. In: Evolutionary Relationships Among Rodents: A Multidisciplinary Analysis, W.P. Luckett and J.-L. Hartenberger, eds., pp. 83–157, Plenum Press, New York.Google Scholar
  62. Szalay, F. S. (1994). Form-function, and ecological and behavioral morphology in Metatheria. In: Evolutionary History of the Marsupials and an Analysis of Osteological Characters, pp. 85–110, Cambridge University Press, New York.Google Scholar
  63. Szalay, F. S., and Bock, W. J. (1991). Evolutionary theory and systematics: Relationships between process and patterns. Z. Zool. Syst. Evol. 29:1–39.Google Scholar
  64. Szalay, F. S., and Decker, R. L. (1974). Origins, evolution, and function of the tarsus in late Cretaceous Eutheria and Paleocene primates. In: Primate Locomotion, F. A. Jenkins Jr., ed., pp. 223–259, Academic Press, New York.Google Scholar
  65. Szalay, F. S., and Drawhorn, G. (1980). Evolution and diversification of the Archonta in an arboreal milieu. In: Comparative Biology and Evolutionary Relationships of Tree Shrews, W. P. Luckett, ed., pp. 133–169, Plenum Press, New York.Google Scholar
  66. Szalay, F. S., and Langdon, J. H. (1986). The foot of Oreopithecus: An evolutionary assessment. J. Hum. Evol. 15:585–621.Google Scholar
  67. Szalay, F. S., and Lucas, S. G. (1996). The postcranial morphology of Paleocene Chiracus and Mixodectes and the phylogenetic relationships of archontan mammals. Bull. N. Mex. Mus. Nat. Hist. Sci. 7:1–47.Google Scholar
  68. Szalay, F. S., and Sargis, E. J. (2001). Model-based analysis of postcranial osteology of marsupials from the Palaeocence of Itabori (Brazil) and the phylogenetics and biogeography of metatheria. Geodiversitas 23:139–302.Google Scholar
  69. Van Valen, L. (1967). New Paleocene insectivores and insectivore classification. Bull. Am. Mus. Nat. Hist. 135:221–284Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2004

Authors and Affiliations

  • Justine A. Salton
    • 1
  • Frederick S. Szalay
    • 1
  1. 1.Department of BiologyCity University of New YorkNew YorkUSA

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