Universality of indeterminate growth in lizards rejected: the micro-CT reveals contrasting timing of growth cartilage persistence in iguanas, agamas, and chameleons

Abstract

Squamate reptiles are considered to exhibit indeterminate growth. Nevertheless, current literature disputes the available definitions of this growth type, presents new theoretical models, and questions its universality in cold-blooded vertebrates. We have followed up on our previous research employing micro-CT to explore growth plate cartilage (GPC) in the epiphysis of long bones, which is responsible for longitudinal skeletal growth by the endochondral ossification process. We focused on numerous and highly diversified group of the Iguania clade comprising Acrodonta (agamas and chameleons) and Pleurodonta ("iguanas"). We recorded the absence of GPC in most of the examined adult Pleurodonta specimens and interpret it as an irreversible arrest of skeletal growth. This finding clearly rejects the universality of indeterminate growth in lizards. On the other hand, we found apparent GPC preservation in most of the adult specimens belonging to Acrodonta. This suggests a preserved ability to continue body growth throughout most of their life. We discuss the uncovered disparity between Acrodonta and Pleurodonta and emphasize the importance of GPC degradation timing.

Figure 1

Phylogenetic pattern of the growth plate cartilage (GPC) across Iguania. Visualization of GPC presence (green) and absence (black) within the Iguania clade comprising Acrodonta (agamas and chameleons) and Pleurodonta (“iguanas”). Reconstruction of ancestral states was done using the parsimony method implemented in Mesquite (Maddison and Maddison 2015). Monitor lizards (Varanidae), the beaded lizard (Helodermatidae) and Chinese crocodile lizard (Shinisauridae) were used as outgroup (Anguimorpha).

Figure 2

Visualisation of proximal part of the femur by micro-CT. Frontal cross-section of the proximal part of the femur. The epiphyseal growth plate is present in adult Uromastyx ornatus (a) and completely absent in adult old Chamaeleo calyptratus. (b) Abbreviations: Epiphysis (Epi), Metaphysis (Met), Diaphysis (Dia), Suture (Sut), Epiphyseal growth plate (asterisk).

Figure 3

Relationship between growth plate cartilage state and body size. The presence (+GPC:1) and absence (• GPC:0) of growth plate cartilage (GPC) in agamas (a), chameleons (b), and Pleurodonta (c) plotted with respect to body size (SVL) and size relative to maximum SVL reported in the literature (SVL_rel). This allows to check for the relationship between the state of GPC and body size (SVL) of the studied species, as well as between the state of GPC and the percent of attained maximal body size (SVL_rel in %).