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Developmental Basis of Limb Homology in Lizards.

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THE ANATOMICAL RECORD 290:900–912 (2007)
Developmental Basis of Limb Homology
in Lizards
Instituto de Bio y Geociencias-Museo de Ciencias Naturales,
Universidad Nacional de Salta, Salta, Argentina
Instituto de Herpetologı́a-Fundación Miguel Lillo, San Miguel de Tucumán, Argentina
Shubin and Alberch (Evol Biol 1986;20:319–387) proposed a scheme
of tetrapod limb development based on cartilage morphogenesis that provides the arguments to interpret the homologies of skeletal elements and
sets the basis to explain limb specialization through later developmental
modification. Morphogenetic evidence emerged from the study of some
reptiles, but the availability of data for lizards is limited. Here, the study
of adult skeletal variation in 41 lizard taxa and ontogeny in species of
Liolaemus and Tupinambis attempts to fill in this gap and provides supporting evidence for the Shubin-Alberch scheme. Six questions are
explored. Is there an intermedium in the carpus? Are there two centralia
in the carpus? Is there homology among proximal tarsalia of reptiles?
Does digit V belong to the digital arch? Is the pisiform an element of the
autopodium plan? And should the ossification processes be similar to cartilage morphogenesis? We found the following answers. Some taxa exhibit
an ossified element that could represent an intermedium. There is one
centrale in the carpus. Development of proximal tarsalia seems to be
equivalent with that observed among reptiles. Digit V could arise from
the digital arch. Pisiform does not arise as part of the limb plan. And different patterns of ossification occur following a single and conservative
cartilaginous configuration. Lizard limb development shows an early pattern common to other reptiles with clear primary axis and digital arch.
The pattern then becomes lizard-specific with specialization involving
some reduction in prechondrogenic elements. Anat Rec 290:900–912,
2007. Ó 2007 Wiley-Liss, Inc.
Key words: limb; morphogenesis; lizards; homology
Shubin and Alberch (1986) reviewed the literature on
the development and evolution of the tetrapod limb and
proposed a formalism to describe limb skeleton based on
the spatial connectivities among cartilaginous condensations during earlier stages of limb morphogenesis (Fig. 1).
This proposal allowed comparisons among tetrapod taxa
and provided a conceptual basis to interpret the homologies of the skeletal components of the tetrapod limbs.
From this approach, several paleontological, embryological, and developmental genetic studies have contributed
with important data to explain the evolution and diversification of vertebrate locomotor appendages and have
established the homologies of their components.
The interspecific variation of limb skeleton in lizards
has been explored by different authors with different
emphasis (e.g., Wellborn, 1933; Gasc, 1963; RenousÓ 2007 WILEY-LISS, INC.
Lécuru, 1973; Mathur and Goel, 1976; Rieppel, 1992a,
1992b, 1992c, 1993a; Maisano, 2001, 2002a, 2002b).
Nevertheless, data on early limb development in lizards
Grant sponsor: Agencia Nacional de Promoción Cientı́fica y
Tecnológica; Grant number: PICT/2002 12418; Grant sponsor:
Consejo Nacional de Investigaciones Cientı́ficas y Técnicas;
Grant number: PIP 2829.
*Correspondence to: Marissa Fabrezi, Instituto de Bio y Geociencias-Museo de Ciencias Naturales, Universidad Nacional de
Salta, Mendoza 2, 4400-Salta, Argentina. Fax: 54-387-4255455.
Received 24 May 2006; Accepted 23 February 2007
DOI 10.1002/ar.20522
Published online 5 April 2007 in Wiley InterScience (www.
Fig. 1. Pattern of cartilages morphogenesis in tetrapod limbs
modified from Shubin and Alberch (1986: Fig. 20). Limb development
is characterized by differentiation of de novo condensation (humerus/
femur), which bifurcates to give rise to the ulna/fibula and radius/tibia
cartilages. Bold lines depict connectivities and gray figures denote the
postaxial side of limb where most differentiation events take place.
Condensation, bifurcation, and segmentation of the ulna/fibula produce the formation of cartilages of the primary axis in a proximodistal
sequence (black bold line), the digital arch in a posteroanterior
sequence (black medium bold line), and the intermedium and centralia
in proximomedial direction (gray bold line). Differentiation of the primary axis involves the origin of digit IV, from which the digital arch
arises. Digit V could represent a de novo condensation in this model.
The intermedium is segmented from the end of ulna/fibula and bifurcates in centrale series. Radiale/tibiale originates from the distal end
of radius/tibia in the preaxial side of the limb (black thin line). cd1–5/
td1–5, distal carpalia 1–5/distal tarsalia 1–5; crd/ctd, centrale radiale
distale/centrale tibiale distale; crp/ctp, centrale radiale proximale/centrale tibiale proximale; cud/cfd, centrale ulnare distale/centrale fibulare
distale; cup/cfp, centrale ulnare proximale/centrale fibulare proximale;
I, intermedium; I–V, metarcarpalia I–V/metatarsalia I–V; r/t, radiale/
tibiale; Ra/Ti, radius/tibia; u/f, ulnare/fibulare; Ul/Fi, ulna/fibula (Shubin
and Alberch, 1986).
are scarce and limited to Agama (Holmgren, 1933), Calotes (Mathur and Goel, 1976), Chamaleo (Rieppel, 1993a),
Hemiergis (Shapiro, 2002), and Tarentola and Chalcides
(Goldschmidt, 1943).
At present, lizards are the only tetrapod group in
which the interpretation of limb morphology does not
have an embryological basis (for urodeles, see Blanco
and Alberch, 1992; Vorobyeva and Hinchliffe, 1996; Hinchliffe and Vorobyeva, 1999; for anurans, see Fabrezi
and Alberch, 1996; Fabrezi and Barg, 2001; for turtles,
see Burke and Alberch, 1985; Sheil, 2003, 2005; for crocodiles, see Müller and Alberch, 1990; for birds, see Hinchliffe and Hecht, 1984; Burke and Feduccia, 1997;
Feduccia et al., 2005; for mammals, see Prochel et al.,
2003, 2004; Sanchez-Villagra and Döttling, 2003). This
problem arises from the difficulty to get complete embryonic series of lizard development.
There are six questions regarding the interpretation of
the skeletal elements that compose lizard limbs that
need developmental data in order to be answered.
One, is there an intermedium in the lizards carpus?
The intermedium, both as embryonic and as ossified element, is free in turtles (Burke and Alberch, 1985; Sheil,
2003, 2005). An embryonic condensation representing
the intermedium fuses with the radiale condensation in
crocodiles and birds (Hinchliffe and Hecht, 1984; Müller
and Alberch, 1990; Burke and Feduccia, 1997). In lizards, some authors have identified an ossified element
as an intermedium in the carpus of some Anguidae
(Renous-Lécuru, 1973), Iguanidae (Avery and Tanner,
1964), Lacertidae (Rieppel, 1992b; Maisano, 2001), Teiidae (Fischer and Tanner, 1979), Varanidae (Rieppel,
1992c), and Xantusiidae (Maisano, 2002b). Others
(Mathur and Goel, 1976) have described this structure
as a transient cartilage that disappears during the embryonic development of the lacertid Calotes versicolor. To
answer this question, it is necessary to review developmental and interspecific variation in order to identify
the mentioned intermedium as an embryonic cartilage
and as an ossified element.
Two, are there two centralia in the lizard carpus? The
intermedium bifurcates to form condensations of the
centralia (Fig. 1). The chelonian carpus has three centralia (Burke and Alberch, 1985; Sheil, 2003, 2005). The
carpus of crocodiles presents a single centrale that forms
distal to the fused radiale-intermedium after distal carpalia are fully formed (Müller and Alberch, 1990), and
no centralia differentiate in the wing of birds (Hinchliffe
and Hecht, 1984; Müller, 1991). Some authors have
pointed out two elements as centralia in lizards: one in
a median position named lateral centrale, and the second one proximal to metacarpale I, named medial centrale (Maisano, 2002a, 2002b). For other authors (e.g.,
Renous-Lécuru, 1973), the medial centrale is the distal
carpale 1. Data on morphogenesis of primary cartilages
could reveal the identity of this condensation as a second
centrale or as part of the digital arch.
Three, is there homology among the lizard proximal
tarsalia, and the same cartilages in turtles and crocodiles? The tarsus of reptiles has two proximal tarsalia
representing the ossified calcaneum (fibulare) and astragalus that may fuse into a large proximal tarsale.
The number and identity of the primary cartilages forming the astragalus have been discussed in several contexts (Holmgren, 1933; Mathur and Goel, 1976; Rieppel,
1993b). Embryological studies showed that the astragalus is formed by the intermedium and centralia in turtles (Burke and Alberch, 1985; Sheil, 2005) and the
intermedium and a single centrale in crocodiles (Müller
and Alberch, 1990). In lizards, the proximal cartilage
that is positioned directly anterior to the fibulare was
described as the astragalus (Rieppel, 1992a; Shapiro,
2002) and its identity was discussed in at least two studies (Holmgren, 1933; Mathur and Goel, 1976). Revision
of early stages of hindlimb development in lizards is
necessary to update the discussion on the homologies of
proximal tarsalia among reptiles.
Four, does digit V belong to the embryonic series of
primary cartilages of the digital arch? Shubin and
Alberch (1986) suggested digit V is formed as a condensation de novo, independently of the digital arch, and
therefore it would not be equivalent to other digits. Patterns of connectivity between digit V and cartilages of
the primary axis and digital arch were described for
anurans (Fabrezi and Barg, 2001) but has not been studied yet in lizards.
Five, is the pisiform an element of the autopodium
plan? Shubin and Alberch (1986) described the pisiform
through ontogeny as a de novo condensation in the reptilian carpus; other authors recognized it as a sesamoid
(Haines, 1969). It is necessary to review and discuss the
pisiform as an element in the limb plan.
Six, should the patterns of ossification be similar to
cartilage morphogenesis? Embryological evidence provides strong arguments to identify limb skeletal elements and interpret their homologies (Feduccia et al.,
2005). However, some authors have criticized the morphogenetic plan of tetrapod limbs (Fig. 1), claiming that
the ossification sequence in lizards does not show the
same pattern as the differentiation of primary cartilages; and so, the identity of ossified elements could not
be the same as that of primary cartilages (Maisano,
2002a, 2002b). This issue could be solved by the analysis
of the differences between cartilage morphogenesis and
Here we present a study of lizard limbs in adult specimens belonging to 41 taxa (see Appendix) and ontogenetic series of Liolaemus multicolor, L. quilmes, L. ruibali, L. zullyi, and Tupinambis merianae in order to
describe the morphogenesis of primary cartilages as well
as set the embryological basis for interpreting the adult
ossified elements; address differences between morphogenesis and ossification processes affecting the limb morphologies; and establish interspecific variation in carpus
and tarsus as well as discuss the constraints. We propose
a scheme to interpret the lizard limb elements with an
embryological basis. The description of skeletogenic patterns of a selection of lizards in the present study
attempts to fill in the gap of limited evidence for the
group, providing useful arguments for the Shubin and
Alberch (1986) scheme, and to serve for future comparative analyses of limb homologies in lizards and tetrapods.
In this study, different analyses were performed:
description of primary cartilage development in embryonic series; study of ossification pattern in ontogenetic
series; and examination of interspecific variation of carpalia and tarsalia in a sample of 41 species belonging to
12 lizard families.
All observations were made in clearing and double
staining with Alcian Blue and Alizarin Red whole
mounts obtained following the procedure described in
Wassersug (1976), and histological serial sections of 7
mm thick, stained with hematoxyilin-eosin (Martoja and
Martoja, 1970). Descriptions, illustrations, and photographs were made with a stereo dissection microscope
Nikon SMZ1000 and light microscope Leica DM
equipped with digital camera and camera lucida.
Fig. 2. Dorsal view of forelimb bud in Liolaemus quilmes embryo at
early paddle-shaped stage (stage 30). A: The primary axis and digital
arch display proximodistal and posteroanterior morphogenesis (bold
lines). This image agrees with Shubin and Alberch’s interpretation
(1986). B: The same view in detail showing radius, ulna, ulnare, distal
carpale 4, and metacarpale IV. Differentiation of distal carpale 3 has
begun. White arrows point out embryonic connectivities between ulna
and ulnare, and ulnare and distal carpale 4. da, digital arch; pa, primary axis; pre, preaxial axis. Scale bar ¼ 0.2 mm.
Primary cartilage development was examined in embryonic specimens staged following Dufaure and Hubert
(1961). This table of development was chosen because
stages can be identified on the basis of limb bud morphologies. The embryonic series were selected from museum collections, and studied specimens are Liolaemus
multicolor (stages 32, 34, 36, and 40), Liolaemus quilmes
(stages 30, 32, 34, 35, and 36), Liolaemus zullyi (stage
Fig. 3. Earlier chondrogenic foci in an embryo of Tupinambis merianae at paddle-shaped stage of limb development (stage 33). A: Right
forelimb where primary axis condensations, distal carpale 3, metacarpalia V–II, and centrale are differentiated. The centrale appears distal
to the ulnare. B: Right hindlimb with cartilages of primary axis, distal
tarsale 3, and metatarsalia V–II become evident. A diffuse condensation is present distal to the fibula and tibia ends. This condensation is
interpreted as the primary fusion of intermedium and centrale. Scale
bar ¼ 0.2 mm.
39), and Tupinambis merianae (stages 33, 37, 40, 49,
and 50). Embryos at limb paddle-shaped stages of Liolaemus spp. were removed from preserved gravid
females. Left limbs of Liolaemus zullyi were chosen for
histological sections and all specimens were cleared and
Patterns of ossification were analyzed in whole
mounts of cleared and double-stained specimens of ontogenetic series of Liolaemus multicolor and Liolaemus
ruibali. Because the Alizarin Red S is a specific dye for
the histochemical detection of calcium, ossification sequence is inferred when positive Alizarine Red S coloration is observed. However, we must notice that bone development may start before calcification.
Whole mounts of cleared and double-stained adult
specimens of 41 taxa of Anguidae, Chamaleontidae, Gekkonidae, Gerrhosauridae, Gymnophthalmidae, Lacertidae, Leiosauridae, Liolaemidae, Polychrotidae, Scincidae, Teiidae, and Tropiduridae were studied in order to
describe interespecific carpal and tarsal variation. Species, specimen numbers, and collection data are listed in
the Appendix. All specimens are deposited in the herpetological collections of Instituto de Herpetologı́a, Fundación Miguel Lillo, Tucumán (Argentina); Museo de Ciencias Naturales, Universidad Nacional de Salta (Argentina); Museo de Zoologı́a, San Pablo (Brazil); and the
private collection of Richard Thomas.
in proximodistal direction (to elongate and give rise to
phalanges) and postaxial-preaxial direction (to differentiate digits II and I; Figs. 3A and 4A and B). Thereafter,
a medial condensation appears distal to the ulnare in
Tupinambis merianae (Fig. 3A). Based on its position,
this condensation is identified as the centrale; however,
the absence of connectivity between this centrale cartilage and the ulnare was a reason to prefer its identification as the intermedium (Mathur and Goel, 1976;
Shapiro, 2002). Distal to the radius, a bilobed cartilage
representing the radiale becomes evident and grows
medially (Fig. 5A and B). Differentiation of digit II progresses and the cartilage of distal carpale 2 is better
defined. In Liolaemus spp., condensation of the centrale
appears after the metacarpale I cartilage is fully formed
(Fig. 5A and B). Segmentation of distal carpale 1 from
distal carpale 2 was observed in embryos of Liolaemus
spp. and Tupinambis merianae (Fig. 6). The origin of
distal carpale 1 from distal carpale 2 confirms the identity of this cartilage as a distal carpale and invalidates
any argument to name it as a centrale or medial centrale (Gauthier et al., 1988; Carroll and Currie, 1991;
Maisano, 2002a, 2002b).
Patterns of connectivity among digital arch cartilages
as depicted in Figure 20 (Fig. 1 here) of Shubin and
Alberch (1986) have been found in limb buds of a malformed embryo of L. quilmes with asymmetrical limb development (Fig. 7A).
Primary Cartilages Morphogenesis
Forelimbs. In lizards, primary axis and digital arch
differentiation were observed in the embryo of Liolaemus quilmes, where connectivities among ulna and ulnare, ulnare and distal carpale 4 are still evident (Fig.
2). The primary axis and digital arch cartilages develop
Hindlimbs. In the same species and at similar
stages of development (Figs. 3B and 4C and D), the primary axis cartilages that are already differentiated correspond to the fibula, fibulare, distal tarsale 4, and
metatarsale IV. At these early stages, there is a diffuse
and heterogeneous condensation between fibula and
tibia and anterior to the fibulare. In Liolaemus spp., this
Fig. 4. Left limb buds at paddle-shaped stage in
Liolaemus multicolor embryos. A: Forelimb with primary axis cartilages (stage 32). B: The following
stage (stage 34), forelimb where digital arch has
started to develop. C: Hindlimb showing primary
axis foci and a medial condensation distal to the
tibia and fibula ends (stage 32). D: The following
stage (stage 34), hindlimb displaying digital arch differentiation and better development of the medial
tarsal condensation. Scale bar ¼ 0.2 mm.
condensation grows medially from the distal end of the
tibia (Fig. 4B and C). This cartilaginous focus and the
fibulare will fuse to form the large proximal tarsale in
later stages (Fig. 5C and D).
Cartilages of metatarsalia and phalanges grow distally. Connections among metatarsale V and distal tarsalia 4–3, and fibula and fibulare were observed in a malformed embryo of L. quilmes (Fig. 7B).
The complete set of primary cartilages of limbs differentiates simultaneously when the disappearance of
interdigital tissue has ended and digits are free.
Ossification Patterns
The skeleton of limbs ossifies from preformed cartilages, a process called chondral ossification. Chondral
ossification happens simultaneously with cartilage
growth. However, growth of cartilage and ossification
are two different and independent processes that are
controlled by intrinsic (genetic and programmed growth)
and extrinsic (hormones, nutrition) factors (Hinchliffe
and Johnson, 1983).
There are four mechanisms of deposition and bone
growth in cartilages (Hall, 2005): periosteal ossification,
endosteal ossification, perichondral ossification, and
endochondral ossification. Perichondral and endochondral ossifications are observed in reptiles and take place
in mineralized cartilage or following removal of mineralized cartilage by cells brought into the marrow cavity by
invading blood vessels (Fig. 8). In lizard limbs, perichondral ossification precedes endochondral ossification.
Perichondral ossification centers appear in diaphyses
of long cartilages (stylopodium, zeugopodium, metapodium, and phalanges; Fig. 8A and B). Calcifications, as
is observed in whole mounts, suggest that they start to
differentiate in a proximodistal direction after development of primary cartilages (Figs. 9A and 10A). Endochondral ossification occurs in carpalia and tarsalia in
Fig. 6. Dorsal view in right hand. The distal carpale 1 arising from
distal carpale 2 in Tupinambis merianae at the end of paddle-shaped
stage embryo (stage 37). Scale bar ¼ 0.5 mm.
Fig. 5. Right limbs of Liolaemus quilmes embryos in advanced
paddle-shaped stages with interdigital tissues in regression. A: Stage
35, the hand exhibits advanced differentiation of primary condensations of the digital arch. The radiale cartilage becomes evident distal
to the radius. B: Stage 36, differentiation of the centrale has took
place and the radiale condensation became more defined distal to the
radius. C: Stage 35, differentiation of primary cartilages in the tarsus
has ended and development of phalanges is in progress. Cartilages of
the fibulare and intermedium-centrale are separated. D: Stage 36,
fusion between fibulare and intermedium-centrale has started in the
tarsus. Scale bar ¼ 1 mm.
later stages of embryonic development, but it increases
in postnatal stages (Figs. 8C and F, 9B and C, and 10B
and E). Most cartilages of carpalia/tarsalia show single
calcified centers but there are two centers in the proximal tarsale and radiale. Calcification centers in proximal
tarsale differentiate at different times; the first one to
appear corresponds to the preaxial and medial portion,
which forms the astragalus, followed by calcification of
the postaxial portion (fibulare) that develops into the
calcaneum. Differentiation of two ossifications in the
proximale tarsale is common to all lizards, with the
exception of Chamaleo spp. (this paper and Rieppel,
1992a), in which there is only one ossification center
identified as astragalus (Rieppel, 1992a). In the radiale
cartilage, we observed two calcification centers; the first
one to differentiate is anterior and the second one is
medial (Fig. 9C). The anterior center of calcification was
identified as the radiale ossification center, and the posterior one as an accessory ossification center, as was
described in xantusiids and phrynosomatids (Maisano,
2002a, 2002b). Development of two ossification centers
in the radiale seems to be common to all lizards.
Secondary centers of ossification develop in epiphyses
in advanced embryonic stages. During postnatal growth,
they may fuse with diaphyses in adult stages when development rates become slow (Figs. 9D and 10E).
Sesamoids are ectopic elements that appear related to
the limb skeleton; they are formed by cartilaginous nodules that may ossify. Sesamoids originate in tendinous
or ligamentous tissues, especially where tendons cross
an articulation (Hall, 2005). Differentiation of sesamoids
starts in embryonic stages after morphogenesis of primary cartilages. The first sesamoid to appear is the pisiform (Figs. 8C and 10A–D). It locates ventrally to the
articulation between ulna and ulnare. Other sesamoids
differentiate in a proximodistal direction but they vary
among species (Fig. 9D). Ossification of each sesamoid is
endochondral and takes place during postnatal growth.
Interspecific Variation of Carpal Elements in
Adult Lizards
Most lizard species with well-developed limbs show
similar forelimbs with a carpus formed by two proximal
elements, the ulnare and radiale; one medial element,
the centrale; and five distal elements, distal carpalia 1–
5. Distal carpale 4 is always the largest of the distal series. The radiale, ulnare, and centrale articulate with
distal carpalia. The pisiform is also present in the articulation between distal epiphysis of ulna and ulnare.
Deviation from this pattern was observed in Chamaleo
unicornis (Fig. 11A). In this species, the radiale and ulnare articulate with a single and large distal carpale,
representing the fusion of the centrale with distal carpalia 4, 3, and 2 (Renous-Lécuru, 1973), placed medially
and bearing five metacarpals; the centrale is absent.
Fig. 7. Pattern of cartilage connectivity in Liolaemus quilmes
embryo at stage 32, in which condensation events in right limbs are
more advanced than in left ones but segmentations are retained. A:
Hand with embryonic connectivities between ulna and ulnare, ulnare
and digital arch, distal carpalia 5 and 4, distal carpalia 4 and 3, distal
carpale 2 and digit I. This image shows the origin of digit I (distal car-
pale 1 and metacarpale I) from distal carpale 2, and the relationship
between digit V with the digital arch. B: Foot displaying connectivities
between metatarsale V and distal tarsalia 4–3, and fibula and fibulare.
This image exhibits connectivity of metatarsale V with digital arch.
Curved arrows indicate embryonic connectivities. Scale bar ¼ 0.2 mm.
Fig. 8. Light microscopic cross-sections of Liolaemus zullyi limbs at the end of embryonic development (stage 39). A: Perichondral ossification in proximal diaphyses of metatarsalia III, IV, and V. Scale
bar ¼ 0.2 mm. B: Perichondral ossification at level
of expanded head of metatarsale V. Scale bar ¼ 0.2
mm. C: Pisiform, epiphysis of ulna, ulnare, and radiale. Hyperthrophic cells indicate the endochondral
ossification in the ulnare. Scale bar ¼ 0.2 mm. D:
Endochondral ossification in the ulnare. Scale bar ¼
0.2 mm. E: Proximal tarsalia displaying astragalus
and fibulare ossification centers. Scale bar ¼ 0.2
mm. F: Detail of cartilaginous hyperthrophic cells in
the fibulare. Scale bar ¼ 0.5 mm. coas, ossification
center of the astragalus; cof, ossification center of
the fibulare; eu, distal epiphysis of the ulna; ps,
Fig. 9. Sequence of ossification in Liolaemus multicolor, dorsal
view of left forelimbs. A: Advanced embryo at stage 40. Black arrows
point out perichondral ossifications in radius, ulna, metacarpalia, and
phalanges. B: Juvenile specimen. Black arrows show endochondral
ossification in ulnare, centrale, radiale (a medial center), and distal carpalia 1–5. White arrows depict centers in distal epiphysis of ulna, and
proximal epiphyses of metacarpalia I–V. C: Juvenile specimen. Black
arrows point out a second center of endochondral ossification in the
radiale, and ossification in pisiform. Epiphyses ossifications are indicated with white arrows. D: Adult specimen. A fully ossified manus;
no distinct ossification centers are evident. Open arrow points out a
suprarticular sesamoid. Scale bars ¼ 0.1 mm (A); 0.2 mm (B–D).
The metacarpalia are short, have similar lengths, and
articulate with the large distal carpale in two directions.
Metacarpalia V and IV articulate with the distal carpale
in postaxial position, and metacarpalia III, II, and I
articulate with the distal carpale in preaxial position.
Thus, digits form two divergent groups (zygodactylia).
In some species of Scleroglossa (Panaspis breviceps
and Gerrhosaurus nigrolineatus), we found a small ossified element between ulnare and radiale (Fig. 11B). A
similar osseous element has been identified as the intermedium (Avery and Tanner, 1964; Renous-Lécuru, 1973;
Fischer and Tanner, 1979; Rieppel, 1992b, 1992c; Maisano, 2001, 2002b).
Interspecific Variation of Tarsal Elements in
Adult Lizards
The tarsus is formed by a large proximal tarsale and
distal tarsalia 4 and 3. The proximal tarsale articulates
proximally with the tibia and fibula, and distally with
distal tarsalia 4 and 3 and metatarsalia V, II, and I. The
stereotypical hooked metatarsale V of lizards is short
and has an expanded proximal head that articulates
with proximal tarsale and distal tarsale 4.
Fig. 10. Sequence of ossification in Liolaemus multicolor, dorsal
view of left hindlimbs. A: Advanced embryo at stage 40. Perichondral
ossifications in diaphyses of fibula, tibia, metatarsalia I–V, and phalanges (black arrows). B: Posthatched specimen. Astragalus, calcaneum, distal tarsalia 4 and 3, and metatarsale V are the endochondral
centers in the tarsus (black arrows). Distal epiphyses of metatarsalia
are indicated with white arrows. C: Juvenile specimen. Distal epiphyses of the tibia and fibula show ossification centers; the same is
observed in proximal epiphyses of metatarsalia (white arrows). D: Juvenile specimen. Sesamoids and accessory calcifications are pointed
with open arrows; sesamoid are present between distal tarsale 4 and
metatarsale V, and a lateral plantar tubercle on the metatarsale V. Two
ossified centers as epiphyses are identified in the proximal tarsale
(white arrows). E: Fully ossified pes in adult specimen. Scale bar ¼
0.2 mm.
The tarsus of Chamaleo unicornis differs also from
the tarsus of most lizards (Fig. 11C); the proximal tarsale is reduced in size, placed between the distal ends
of the tibia and fibula (which are convergent), and
articulated with a single distal tarsale, representing an
early fusion of distal tarsalia cartilages. Metatarsalia
are short and form divergent groups. Metatarsalia V,
IV, and III articulate with the distal tarsale and are
oriented in postaxial direction. Metatarsale II articulates with the distal tarsale and metatarsale I articulates with the proximal tarsale, both oriented in preaxial direction.
Another variation from the basic lizard pattern was
observed in some Gekkonidae (Garthia gaudichaudii,
Hemidactylus mabouia, and Phyllopezus pollicaris). In
these species, there is a small bone proximal to the
epiphyses of metatarsalia I and II, which articulates
with proximal tarsale (Fig. 11D). This bone has been
considered a preaxial distal tarsale 1 (Mathur and
Goel, 1976; Khalil and Sabri, 1977; Mohammed, 1989)
or the fusion of distal tarsale 2 and 1 (Holmgren,
1933). Embryological data to support its identity are
absent. At present, we prefer to name it anterior distal
Fig. 12. Skeletal elements of the left limbs of Ophiodes striatus. This
species lack forelimbs. The primary axis elements are conserved in the
vestigial hindlimbs that are represented by the ossification of fibula, calcaneum (fibulare), and metatarsale IV. The astragalus ossification is also
retained. as, astragalus; ca, calcaneum. Scale bar ¼ 0.5 mm.
Fig. 11. Carpal and tarsal elements in selected adult lizards. A:
Dorsal view of carpus in Chamaleo unicornis. The radiale, ulnare, and
pisiform lack ossification. A single distal carpale, representing the
fusion of distal carpalia, with an endochondral ossification center
bears five short metacarpalia. Cartilages are in gray. B: Dorsal view of
carpus in Gerrhosaurus nigrolineatus. A small ossification between
ulna distal epiphysis and radiale is identified as the intermedium. C:
Dorsal view of tarsus in Chamaleo unicornis. The proximal tarsale has
only the astragalus ossification and a single distal tarsale articulates
with five short metatarsalia. D: Dorsal view of tarsus in Phyllopezus
pollicaris. There is a preaxial distal tarsale between the tarsale proximale and metatarsalia II and I. cd, distal carpale; td, distal tarsale;
tda, anterior distal tarsale; tp, proximal tarsale. Scale bars ¼ 1 mm
(A–C); 1.5 mm (D).
Pattern of Primary Cartilages Morphogenesis
The scheme proposed by Shubin and Alberch (1986)
represents cartilage morphogenesis, which defines the
tetrapod limb plan. Morphogenesis of cartilages is different from chondrogenesis. Morphogenesis of cartilage
implies the generation and emergence of a variety of less
easily defined three-dimensional shapes of cartilaginous
entities, whereas chondrogenesis involves cell differentiation (Thorogood, 1983). Shubin and Alberch (1986)
described the limb skeleton based on spatial connections
during early stages of limb morphogenesis, where skeletal condensations first appear proximally and yield other
condensations through segmentation and bifurcation
events that occur predominantly along the posterior side
of the limb (Fig. 1). The study of cartilage morphogenesis
of limbs has confirmed the existence of an early primary
axis in Tetrapods (Mathur and Goel, 1976; Hinchliffe
and Hecht, 1984; Burke and Alberch, 1985; Shubin and
Alberch, 1986; Müller and Alberch, 1990; Fabrezi
and Alberch, 1996; Burke and Feduccia, 1997; Fabrezi
and Barg, 2001; Feduccia et al., 2005; Sheil, 2005). The
early differentiation of a primary axis that invariably
passes through digit IV in early limb development is a
morphological tool that allows one to interpret the identity and homology of digits and specific elements of the
autopodium, as well as identify and discuss the relative
positions of structures and directions of growth.
Primary axis development in lizard limbs as we show
it (Fig. 2) has been described in other studies (Goldschmidt, 1943; Mathur and Goel, 1976; Shapiro, 2002)
and is conserved in those taxa with strong limb reductions (Fig. 12).
In forelimbs of crocodiles and birds, after differentiation of primary axis, a condensation continuous with the
end of the ulna and the end of the radius develops and
segments, giving rise to the intermedium, after fusing to
the radiale (Müller and Alberch, 1990; Burke and Feduccia, 1997). In turtles, the intermedium is segmented from
the distal end of the ulna as a single cartilage, from it
centralia 4 and 3 originate, and the radiale is absent
(Burke and Alberch, 1985; Sheil, 2003, 2005). In the lizard Calotes versicolor, the intermedium was described as
a condensation of mesenchyme that may disappear by
necrosis, and the radiale differentiates after disappearance of intermedium (Mathur and Goel, 1976). Our
observations of the lizard carpus development failed to
find an embryonic intermedium and showed the origin of
the radiale to be a condensation from the end of the radius. However, the origin of the intermedium should be
studied in those taxa, e.g., some Scleroglossa such as
Panaspis breviceps and Gerrhosaurus nigrolineatus, with
adults having an ossified intermedium to elucidate its origin. In spite of embryological data showing the intermedium of lizards as being weak, the presence of a centrale
suggests the possibility that the intermedium differentiates only as a mesenchyme condensation and may be
incorporated to the centrale in those taxa in which the
intermedium is absent in adults. Differing from what is
the case in turtles, the lizard carpus shares with crocodiles the development of a distinct and single radiale condensation.
In amniote hindlimbs, the pattern of morphogensis of
proximal tarsalia is complex. The fibulare forms as part
of the primary axis, the medial condensation anterior to
the fibulare in which the astragalus ossifies is interpreted as the intermedium-centrale, and the tibiale is
absent (Burke and Alberch, 1985; Müller and Alberch,
1990; Rieppel, 1993b; Sheil, 2005). In lizards, we
observed both cartilages, and the anterior condensation
seems to be formed by two foci without connectivity with
the distal end of the tibia (Fig. 3B). In crocodiles, the cartilage of the intermedium-centrale differentiates as a single chondrogenic condensation with two foci; the proximal focus is the intermedium and the distal focus is the
centrale (Müller and Alberch, 1990). Heterochrony produces the failure of the centrale to separate completely
from the intermedium (Müller and Alberch, 1990). In
turtles, the well-defined and continuous condensations of
the intermedium and proximal centrale appear in a proximodistal sequence and the centrale 4 differentiates as
an independent element to be incorporated into the growing condensation of the intermedium-centrale (Burke
and Alberch, 1985; Sheil, 2003, 2005). We propose that
the medial condensation where the astragalus ossifies in
lizards represents the intermedium-centrale and is
equivalent to that described in crocodiles sharing the
heterochronic change, for which the event of segmentation of the centrale represents a primary modification of
the pattern (Müller, 1991). Therefore, it seems that in
most reptiles, the astragalus forms by ossification of the
intermedium and central, whereas in turtles it is formed
by the inclusion of additional centralia elements.
Differentiation of digital arch cartilages in lizards
with well-developed limbs shows a sequence and connectivities in agreement with Shubin and Alberch’s
interpretation (1986). There are five digits and the carpus has five distal carpalia. Distal carpale 1 was named
medial centrale by some authors (Gauthier et al., 1988;
Carroll and Currie, 1991; Maisano, 2002a, 2002b), but
our observations confirm the identity of this element as
part of the digital arch and distal carpal series (Figs. 6
and 7A). Shubin and Alberch (1986) recognized the
digit posterior to the primary axis as digit V. The participation of digit V in the primary axis and digital
arch has not been discussed and there are few references of the origin of digit V in the literature (Fabrezi
and Barg, 2001). Shubin and Alberch (1986) mentioned
the differentiation of digit V as a de novo condensation
in turtles based on Burke and Alberch (1985). Fabrezi
and Barg (2001) described distal carpale 5 and metacarpale V as included in the global morphogenetic events
involved in the postaxial autopodium development
showing patterns of connectivity between ulnare and
the fused distal carpalia 5 and 4 in forelimbs of some
species of Neobatrachia. In this study, we found the
first evidence that digit V develops as part of the digital arch and it is not a de novo condensation in reptiles
(Fig. 7). However, this finding is limited to the right
limbs of a single abnormal specimen, and more embryological studies are needed to confirm digit V is part of
the digital arch.
Digit V and the pisiform were described as de novo
condensations by Shubin and Alberch (1986). Different
from other primary cartilages of the limb, including
those of digit V, the pisiform does not exhibit spatial connections with any condensation of the autopodium.
Haines (1969) described it as a sesamoid, and as most
sesamoids, it develops into a tendon and links muscle
and bone. However, the pisiform is a highly conserved
sesamoid associated with the reptilian carpus (Carroll
and Currie, 1991).
Ossification Patterns of Lizard Limbs
Morphogenesis of the cartilages of limbs seems to happen during paddle-shaped embryonic stages (this study;
Mathur and Goel, 1976; Shapiro, 2002). Ossification begins
when primary cartilages are fully differentiated. Perichondral ossification is characteristic of diaphyses, whereas
endochondral ossification occurs in carpal and tarsal elements, epiphyses, and sesamoids. Perichondral ossifications start to calcify before endochondral ossifications.
What type of ossification will ensue is related to the
shape of the preformed cartilage; in anurans, perichondral calcification usually occurs in diaphyses, and
because proximal tarsals are long, they calcify perichondrally before other tarsal and carpal cartilages. Perichondral calcification progresses in proximodistal
sequence in diaphyses, whereas during advanced embryonic development, the first ossification centers appear in
postaxial carpal and tarsal cartilages (Mathur and Goel,
1976; Rieppel, 1992b; 1993a; Shapiro, 2005). Ossification
of sesamoid and epiphyses seems to take place at postembryonic stages with variable patterns (Rieppel, 1992a,
1992b, 1993a; Maisano 2002a, 2002b; Shapiro, 2002).
Limb development involves cartilage morphogenesis,
cartilage growth, and ossification. These are developmental processes that may happen simultaneously, but
they can be regarded as independent and different (Hinchliffe and Johnson, 1983; Thorogood, 1983). Morphogenesis of cartilages defines a primary pattern that may
be altered by heterochrony and a secondary pattern
involving modifications to primary pattern (Müller,
1991). Secondary modifications are earlier than ossification and thus ossification takes place on preformed cartilages. At present, data on skeletal lizard limb development suggest that ossification does not deviate from a
conservative cartilaginous pattern. Ossification sequences may exhibit great variation without consequences on
the identity of the elements of the limb plan. We do not
agree with Maisano (2002a, 2002b), who stated that the
proximodistal gradient, primary axis, and digital arch
are not appropriate bases for either predicting postnatal
ossification sequences or identifying ossified elements.
Interespecific Variation in Lizard Carpus and
A similar variation of ossified carpus/tarsus elements
to the one we found in our study is described in the literature. We summarized it as follows.
There is a small osseous intermedium between the ulnare and radiale in Ameiva spp. and Cnemidophorus
spp. (Fischer and Tanner, 1979), anguids (RenousLécuru, 1973), lacertids (Rieppel, 1992b; Maisano, 2001),
Sauromalus, Ctenosaura, and Crotaphytus (Avery and
Fig. 13. Schematic representation of primary chondrogenic foci of
lizard limbs. A: In the forelimb, the primary axis and digital arch represent the first cartilages to differentiate. Digit V could arise from the
digital arch. The radiale is segmented from the radius end. An intermedium condensation was absent in our observations in these embryonic
series, but it is present in adults of some species. No connectivity
between the only centrale of the carpus and primary axis cartilages
has observed. The ossified carpus in most lizards with pentadactyl
forelimbs exhibits this pattern of primary cartilages. Chamaleontidae
have reductions that could represent an early modified pattern. B: In
the hindlimb, the primary axis and digital arch represent the first cartilages to differentiate. Digit V could have relationships with digital arch.
Proximal tarsale is formed by the fusion of fibulare and the condensation of intermedium-centrale. This last develops the ossification center
named astragalus. Distal tarsalia show a reduced pattern with only
distal tarsale 4 and 3 differentiated. In some Gekkonidae, an anterior
distal tarsale is present. The ossified tarsus in most lizards with pentadactyl hindlimb exhibits this pattern. Chamaleontidae have reductions
that could represent a modified developmental pattern.
Tanner, 1964), varanids (Rieppel, 1992c), and xantusiids
(Maisano, 2002b). Distal carpale 1 is absent in the carpus of Callisaurus draconoides (Maisano, 2002a).
The number of distal carpalia/tarsalia that corresponds to a pentadactyl pattern is reduced only in chamaleontids, representing a modified early limb pattern
that includes absence of postaxial ossification (fibularecalcaneum) in the tarsus (Gasc, 1963; Renous-Lécuru,
1973; Rieppel, 1993a).
The anterior distal tarsale, anterior to distal tarsale 3,
is present in species of gekkonids and lacertids (Siebenrock, 1893; Wellborn, 1933; Stephenson, 1960; Mathur
and Goel, 1976; Mohammed, 1988; Bauer, 1990).
The elements of the primary axis are conserved (Fig.
12) in those lizard taxa with reduced or vestigial limbs
(Shapiro, 2003).
These data reveal that the lizard carpus and tarsus are
conservative in their formation and have strong developmental constraints for which variation is limited.
Observed variation, such as the failure of some primary
cartilages to segment (e.g., absence of distal carpale 1, absence of the centrale) or the progress in segmentation of
distal anterior tarsale, may be interpreted as primary
modifications by heterochrony in respect to those patterns
of limb morphogenesis of turtles and crocodiles (Müller,
1991). Variation related to absence of ossification in primary cartilages does not imply a modified limb pattern,
but rather a modification of the sequence of ossification.
The identification and determination of equivalent
entities is the basis of any comparative analysis. Morphogenesis of cartilages underlies and determines the
form and identity of a large part of the endoskeleton of
vertebrates. The cartilaginous primordium provides the
structural template for subsequent ossification in the
bones that arise by endochondral and perichondral ossification (Thorogood, 1983). Shubin and Alberch (1986)
described the cartilage morphogenesis of the tetrapod
limb and proposed a scheme of spatial connections
among primary cartilaginous condensations, providing a
tool to interpret the skeletal elements of limbs. From
this framework, we have analyzed some aspects of lizard
limb development, and we found some evidence in agreement with data presented in primary literature to answer the following questions.
One, is there an intermedium in the lizard carpus?
Adults of some taxa present an ossified element placed
between the ulnare and radiale that may be interpreted
as the intermedium, but embryological evidence is weak
and more taxonomically comprehensive examination of
limb development at paddle-shaped embryonic stages is
needed to confirm its identity.
Two, are there two centralia in the lizard carpus? No,
the carpal previously identified as a medial centrale
(Gauthier et al., 1988; Carroll and Currie, 1991; Maisano, 2002a, 2002b) is identified herein as distal carpale
1. There is a single centrale in the lizard carpus.
Three, is there homology among the lizard proximal
tarsalia, and the same cartilages in turtles and crocodiles? Yes, lizards share with other reptiles the presence
of a cartilaginous condensation of the fibulare and an
anterior condensation representing the intermediumcentrale.
Four, does digit V belong to the embryonic series of
primary cartilages of the digital arch? We present evidence of patterns of connectivity between digit V and
digital arch in lizard’s fore- and hindlimbs. However,
more embryological studies supporting digit V forms
part of the primary axis are needed.
Five, is the pisiform an element of the autopodium
plan? No, the pisiform is one of the numerous sesamoids
that develop without spatial connectivities with the primary cartilages of the limb.
Six, should the patterns of ossification be similar to
cartilage morphogenesis? No, cartilage morphogenesis
and ossification are different. The pattern of morphogenesis of cartilages defines the cartilaginous primordia in
which ossifications occur, but the ossification sequences
seem to have variable patterns. The later requires further examination.
At present, the morphogenetic approach of Shubin
and Alberch (1986) provides a satisfactory hypothesis to
interpret the origin and identification of the skeletal elements of lizard limbs. On this basis, we depicted a particular pattern of primary cartilage morphogenesis for
fore- and hindlimbs in lizards, from which most variations known in ossified elements can be interpreted
using developmental arguments (Fig. 13). Nevertheless,
we emphasize that these conclusions need a more taxonomically comprehensive examination of lizard limb ontogeny.
The authors are grateful to two anonymous reviewers
for comments, criticisms, and suggestions made on the
submitted draft of this article. They also thank Dr.
Natalia von Ellenrieder for reading and improving the
English. Specimens referred to in this study were kindly
provided by Marta Cánepa and Sonia Ziert (Instituto de
Herpetologı́a, Fundación Miguel Lillo, Tucumán, Argentina), Juan Daza (personal collection of Dr. Thomas),
Paulo Vanzolini (Museo de Zoologı́a, San Pablo, Brazil),
and the technical staff of Museo de Ciencias Naturales
(Universidad Nacional de Salta, Argentina).
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FML: Instituto de Herpetologı́a, Fundación Miguel
Lillo, Tucumán, Argentina.
MCN: Museo de Ciencias Naturales, Universidad
Nacional de Salta, Argentina.
MZUSP: Museo de Zoologı́a, San Pablo, Brazil.
RT: private collection of Richard Thomas.
Anguidae: Ophiodes sp. (FML 2000, one adult specimen); Ophiodes striatus (FML 2001, one adult specimen).
Chamaleontidae: Chamaleo unicornis (MCN 2151, one
adult specimen).
Gekkonidae: Bogertia lutzae (MZUSP 54747, one adult
specimen); Garthia gaudichaudii (MZUSP 45329, one
adult specimen); Garthia penai (MZUSP 60938, one
adult specimen); Hemidactylus mabouia (FML 2421, two
adult specimens); Homonota borelli (FML 933, two adult
specimens; FML 2409, one adult specimen; FML 2414,
one adult specimen); Homonota darwini (FML 794, two
adult specimens); Homonota fasciata (FML 062, one
adult specimen; FML 1495, two adult specimens; FML
777, one adult specimen; FML 1751, one adult specimen;
FML 2415, one adult specimen); Homonota underwoodi
(FML 1310, one adult specimen; FML 1490, one adult
specimen; FML 2031, two adult specimens); Homonota
uruguayensis (FML 1746, two adult specimens); Homonota whitii (FML 3547, one adult specimen); Phyllodactylus gerrhopygus (FML 1563, two adult specimens);
Phyllopezus pollicaris (FML 2813, two adult specimens);
Thecadactylus rapicauda (MZUSP 11476, one adult
specimen); Sphaerodactylus sp. (RT 13875-13848-1385513873-14137, five adult specimens); Vanzoia klugei
(MZUSP 59135, two adult specimens).
Gerrhosauridae: Gerrhosaurus nigrolineatus (MCN
2148, one adult specimen).
Gymnophthalmidae: Pantodactylus schreibersii (FML
731, two adult specimens).
Lacertidae: Podarcis sicula (FML 03714, one adult
specimen); Poromera fordi (MCN 2149, one adult specimen).
Leiosauridae: Leiosaurus paronae (FML 00035, one
adult specimen); Leiosaurus catamarcensis (FML 00670,
one adult specimen); Leiosaurus sp. (FML 7496, one
adult specimen); Pristidactylus achalensis (FML 61816182, two adult specimens).
Liolaemidae: Liolaemus bitaeniatus (FML 2441, one
adult specimen); Liolaemus cuyanus (FML 1803,
one adult specimen); Liolaemus dorbingy (FML 1757,
one adult specimen); Liolaemus multicolor (FML s/n,
seven juvenile specimens, between 5–7 days posthatched; MCN 2142, posthatched specimen 29.8 mm
SVL; MCN 2143, juvenile specimen 42.4 mm SVL; MCN
2144, juvenile specimen, 40.8 mm SVL; MCN 2141, juvenile specimen 48.4 mm SVL; MCN 2140, adult specimen;
MCN 2152, embryo at stage 32; MCN 2153, embryo at
stage 34; MCN 2154, embryo at stage 3; MCN 2155,
embryo at stage 40); Liolaemus cf quilmes (FML 1227,
one adult specimen); Liolaemus quilmes (FML s/n, eight
embryos at stages 30, 32, 34, 35, and 36; FML 1227, one
adult specimen); Liolaemus ramirezae (FML 1228-2288,
two adult specimens); Liolaemus ruibali (FML s/n, eight
juvenile specimens, between 5 and 7 posthatched); Liolaemus scapularis (FML 1846, one adult specimen); Liolaemus zullyi (MCN 2139, embryo at stage 39).
Polychrotidae: Polychrus acutirostris (FML 48156, one
adult specimen).
Scincidae: Mabuya dorsivittata (FML 0896-1979, two
adult specimens); MCN 2150 Panaspis breviceps (FML
0896-1979, one adult specimen).
Teiidae: Cnemidophorus longicauda (FML 1619, one
adult specimen), Kentropix lagartija (FML 1186, two
adult specimens), Kentropyx viridistriga (FML 1204,
two adult specimens), Teius cyanogaster (FML 02941978, two adult specimens), Tupinambis merianae (FML
s/n, two embryos at stages 49 and 50; FML s/n, three
embryos at stages 33, 37, and 40); Tupinambis rufescens
(FML 2559, one adult specimen).
Tropiduridae: Tropidurus etheridgei (FML 1984–1986,
two adult specimens); Tropidurus melanopleurus (FML
2055, one adult specimen).
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development, limba, homology, lizard, basic
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