Limb development in the gekkonid lizard gonatodes albogularis: A reconsideration of homology in the lizard carpus and tarsus

Abstract

Despite the attention squamate lizards have received in the study of digit and limb loss, little is known about limb morphogenesis in pentadactyl lizards. Recent developmental studies have provided a basis for understanding lizard autopodial element homology based on developmental and comparative anatomy. In addition, the composition and identity of some carpal and tarsal elements of lizard limbs, and reptiles in general, have been the theme of discussions about their homology compared to non-squamate Lepidosauromorpha and basal Amniota. The study of additional embryonic material from different lizard families may improve our understanding of squamate limb evolution. Here, we analyze limb morphogenesis in the gekkonid lizard Gonatodes albogularis describing patterns of chondrogenesis and ossification from early stages of embryonic development to hatchlings. Our results are in general agreement with previous developmental studies, but we also show that limb development in squamates probably involves more chondrogenic elements for carpal and tarsal morphogenesis, as previously recognized on the grounds of comparative anatomy. We provide evidence for the transitory presence of distal carpale 1 and intermedium in the carpus and tibiale, intermedium, distal centralia, and distal tarsale 2 in the tarsus. Hence, we demonstrate that some elements that were believed to be lost in squamate evolution are conserved as transitory elements during limb development. However, these elements do not represent just phylogenetic burden but may be important for the morphogenesis of the lizard autopodium.

Digit evolution in gymnophthalmid lizards

“…A group that is underrepresented in developmental studies is the Squamata. Understanding the evolution and diversification of the reptile limb has been the focus of studies in several research fields, including evolutionary biology, paleontology, ecology, anatomy, physiology, functional morphology and, to a lesser degree, developmental biology (Gans, 1975; Lande, 1978; Withers, 1981; Greer, 1991; Caldwell, 2002; Shapiro, 2002; Shapiro et al ., 2003; Whiting et al ., 2003; Crumly and Sanchez-Villagra, 2004; Kearney and Stuart, 2004; Kohlsdorf and Wagner, 2006; Wiens et al ., 2006, Brandley et al ., 2008; Kohlsdorf et al ., 2008; Russel and Bauer, 2008; Skinner et al ., 2008; Bergmann and Irschick, 2009; Jerez and Tarazona, 2009; Young et al ., 2009; Leal et al ., 2010; Hugi et al ., 2012; etc).…”

“…Even though an incredible diversity of limbs is observed among squamate reptiles (lizards, snakes and amphisbaenians), little is known about the mechanisms involved in limb development within the group. Most of the studies concern morphological analyses of limb development, which are important for laying the anatomical foundations for further functional investigations (for example, Howes and Swinnerton, 1901; Mathur and Goel, 1976; Rieppel, 1994; Shapiro, 2002; Fabrezi et al ., 2007; Leal et al ., 2010; Roscito and Rodrigues, 2012a,b), but still few studies (Raynaud, 1990; Raynaud et al ., 1998; Cohn and Tickle, 1999; Shapiro et al ., 2003; Young et al ., 2009) attempted to undercover the molecular mechanisms behind limb development in natural populations of squamate species.…”

Digit evolution in gymnophthalmid lizards

“…As discussed before, from the morphological point of view, multiple embryological evidences (Shubin and Alberch, 1986;Müller and Alberch, 1990;Chiang et al, 2001;Noro et al, 2009;Young et al, 2009;Leal et al, 2010;Shapiro, 2002, and many others) show that: i) the condensation corresponding to dIV is the first one to form in the limb buds; ii) digits most often form sequentially in a posterior-anterior order (IV>III>II/V>I; although Zhu et al, 2008 evidences claim for more detailed observations of digit development); and iii) that digits are lost in the reverse order of their development, which makes dIV the last one to disappear (Morse, 1872;Sewertzoff, 1931;Chiang et al, 2001;Shapiro et al, 2002).…”

“…Most of the studies comprise morphological analyses of limb development, and are important for laying the anatomical foundations for further functional investigations (for example, Howes and Swinnerton, 1901;Mathur and Goel, 1976;Rieppel, 1994;Shapiro, 2002;Fabrezi et al, 2007;Leal et al, 2010;Roscito and Rodrigues, 2012a,b), but few studies (Raynaud, 1990;Raynaud et al, 1998;Cohn and Tickle, 1999;Shapiro et al, 2003;Young et al, 2009) attempted to undercover the molecular mechanisms behind limb development in natural populations of squamate species.…”

Identity of the avian wing digits: Problems resolved and unsolved

“…In C. chalcides, the three digits of both the fore-and hindlimb seem to have undergone a frame shift in identity. As in birds, in C. chalcides, the position of the primary axis in the developing autopod indicates that the digits develop in positions 2, 3, and 4 (Steiner and Anders, 1946;Young et al, 2009); however, shape of the anterior-most metacarpal/tarsal, fusion of anterior-most distal carpal and metacarpal (thought to be an anatomical characteristic of digit I; Steiner and Anders, 1946;Rieppel, 1992;Leal et al, 2010), and the phalangeal formula of the two anterior digits (Caputo et al, 1995) are indicative of digits I, II, and possibly III identities (Fü rbringer, 1870;Steiner and Anders, 1946;Renous-Lecuru, 1973;Young et al, 2009). Recently the suspected frame shift has been further supported using molecular data.…”