Evolution and Homology of the Astragalus in Early
Amniotes: New Fossils, New Perspectives
F. Robin O’Keefe,
1
* Christian A. Sidor,
1
Hans C.E. Larsson,
2
Abdoudaye Maga,
3
and
Oumarou Ide
3
1
Department of Anatomy, New York College of Osteopathic Medicine, Old Westbury, New York 11568
2
Redpath Museum, McGill University, Montreal, Quebec H3A 2K6, Canada
3
Institut de Recherches en Sciences Humaines, Niamey, Niger Republic
ABSTRACT The reorganization of the ankle in basal
amniotes has long been considered a key innovation al-
lowing the evolution of more terrestrial and cursorial be-
havior. Understanding how this key innovation arose is a
complex problem that largely concerns the homologizing
of the amniote astragalus with the various ossifications in
the anamniote tarsus. Over the last century, several hy-
potheses have been advanced homologizing the amniote
astragalus with the many ossifications in the ankle of
amphibian-grade tetrapods. There is an emerging consen-
sus that the amniote astragalus is a complex structure
emerging via the co-ossification of several originally sep-
arate elements, but the identities of these elements re-
main unclear. Here we present new fossil evidence bear-
ing on this contentious question. A poorly ossified, juvenile
astragalus of the large captorhinid Moradisaurus grandis
shows clear evidence of four ossification centers, rather
than of three centers or one center as posited in previous
models of astragalus homology. Comparative material of
the captorhinid Captorhinikos chozaensis is also inter-
pretable as demonstrating four ossification centers. A
new, four-center model for the homology of the amniote
astragalus is advanced, and is discussed in the context of
the phylogeny of the Captorhinidae in an attempt to iden-
tify the developmental transitions responsible for the ob-
served pattern of ossification within this clade. Lastly, the
broader implications for amniote phylogeny are discussed,
concluding that the neomorphic pattern of astragalus os-
sification seen in all extant reptiles (including turtles)
arose within the clade Diapsida. J. Morphol. 267:415– 425,
2006. © 2006 Wiley-Liss, Inc.
KEY WORDS: amniote; ankle; astragalus; captorhinid;
homology
The tarsus in amniotes differs radically from that
of anamniote tetrapods. Relative to amphibian-
grade taxa, amniotes have fewer bony elements in
the ankle, and the elements play an increased, more
active role in locomotion by stiffening and stabiliz-
ing the pes (Sumida, 1997). This repatterning of the
tarsus has long been considered a key innovation in
the transition between amphibian-grade and
reptilian-grade tetrapods (Romer, 1956; Gauthier et
al., 1988), allowing increased terrestriality and loco-
motor efficiency. Unfortunately, this transition is
not well understood; the homologies of the various
tarsal elements are unclear, rendering the study of
specific joint articulations difficult (Sumida, 1997, p.
387). New data and new insights on the developmen-
tal and evolutionary repatterning of the amniote
ankle are therefore of prime importance, for they
bear on one of the key transitions in tetrapod his-
tory: the attainment of full terrestriality after the
long transition from fin to limb (Clack, 2002).
Perhaps the most important novelty within the
amniote tarsus is the astragalus, a large, complex
bone comprising the primary area of articulation for
the distal tibia. The definitive astragalus first ap-
pears at the origin of the clade Amniota (Fig. 1A);
amphibian-grade tetrapod taxa below this node,
such as seymouriamorphs and anthracosaurs (re-
gardless of the current debate over their relation-
ships to each other and to Amniota; Clack, 2002),
generally maintain the pattern of tarsal bones char-
acteristic of most anamniote tetrapods, while synap-
sids and reptiles possess a true astragalus (relation-
ships from Coates, 1996; Sumida, 1997). This obvious
correlation between amniote origins and the appear-
ance of the astragalus has lead to a long discussion
of the homologies of this bone (Gegenbauer, 1864;
Zittel, 1932; Romer, 1956; Rieppel, 1993; Kissel et
al., 2002; Berman and Henrici, 2003). However, a
lack of definitive evidence has precluded a satisfac-
tory resolution. Here we present new fossil evidence
that may help to resolve this debate.
Contract grant sponsor: National Geographic Society; Contract
grant number: 7258-02 (to C.A.S.); Contract grant sponsor: New York
College of Osteopathic Medicine (research funds to C.A.S. and F.R.O.);
Contract grant sponsor: National Sciences and Engineering Research
Council, Canada Research Chairs; Contract grant sponsor: Fonds
Que ´be ´cois de la Recherche sur la Nature et les Technologies (to
H.C.E.L.).
*Correspondence to: F.R. O’Keefe, Assistant Professor, Dept. of
Anatomy, New York College of Osteopathic Medicine, NYCOM II Rm.
326, Old Westbury, NY 11568-8000. E-mail: frokeefe@nyit.edu
Published online 18 January 2006 in
Wiley InterScience (www.interscience.wiley.com)
DOI: 10.1002/jmor.10413
JOURNAL OF MORPHOLOGY 267:415– 425 (2006)
© 2006 WILEY-LISS, INC.