Determinate growth is predominant and likely ancestral in squamate reptiles

Abstract

Body growth is typically thought to be indeterminate in ectothermic vertebrates. Indeed, until recently, this growth pattern was considered to be ubiquitous in ectotherms. Our recent observations of a complete growth plate cartilage (GPC) resorption, a reliable indicator of arrested skeletal growth, in many species of lizards clearly reject the ubiquity of indeterminate growth in reptiles and raise the question about the ancestral state of the growth pattern. Using X-ray micro-computed tomography (µCT), here we examined GPCs of long bones in three basally branching clades of squamate reptiles, namely in Gekkota, Scincoidea and Lacertoidea. A complete loss of GPC, indicating skeletal growth arrest, was the predominant finding. Using a dataset of 164 species representing all major clades of lizards and the tuataras, we traced the evolution of determinate growth on the phylogenetic tree of Lepidosauria. The reconstruction of character states suggests that determinate growth is ancestral for the squamate reptiles (Squamata) and remains common in the majority of lizard lineages, while extended (potentially indeterminate) adult growth evolved several times within squamates. Although traditionally associated with endotherms, determinate growth is coupled with ectothermy in this lineage. These findings combined with existing literature suggest that determinate growth predominates in both extant and extinct amniotes.

Keywords: determinate growth; endothermy; growth plate cartilage; indeterminate growth; micro-CT; squamata.

Figure 1.

Epiphyseal growth plate cartilage visualization. Longitudinal section of the proximal part of the femur by µCT in three representative species of basal clades (Gekkota, Scincoidea and Lacertoidea). The epiphyseal growth plate is present in a subadult (a) and absent in an adult of the crested gecko Correlophus ciliatus (b); present in a subadult (c) and absent in an adult of Karsten's girdled lizard Zonosaurus karsteni (d), present in a subadult (e) and absent in an adult of Moroccan eyed lizard Timon tangitanus (f). Asterisks indicate the growth plate cartilages. Abbreviations: Dia, diaphysis; Epi, epiphysis; Met, metaphysis; Sut, suture. Note the completely different inner structure in the metaphysis in a, c, e and b, d, f. Scale bars, 500 μm.

Figure 2.

Ancestral state reconstruction of growth type in squamates. A circular tree depicting the growth plate cartilage (GPC) state in whole Squamata as revealed by µCT examination of the proximal part of femoral bones. Ancestral state reconstruction using maximum-likelihood with hidden state speciation and extinction models was employed to uncover the evolution of growth type (determinate versus indeterminate) in Squamata. The plotted ancestral states are reconstructed under the best model based on AIC (HiSSE equal rate, see electronic supplementary material, for more details). Presence and absence of the GPC imply extended (potentially indeterminate) and determinate body growth, respectively. Tuatara (Sphenodon punctatus), as a sister group of Squamata, was included as an outgroup. The state of tuatara is according to the presence of an external fundamental system and recapture growth data suggesting the determinate type of body growth [24,64]. Species marked with asterisk were scored according to the GPC state from the literature [26]. Species marked with † were very old individuals (for details of age see [30,31]).

Figure 3.

Two scenarios for the evolution of body growth type in amniotes. (a) Scenario based on maximum-parsimony predicting that the last common ancestors of the Lepidosauria (node 5), Archosauria (4), Archelosauria (3) and Sauropsida (2) were determinate growers. (b) More conservative scenario considering the possibility of multiple evolutionary transitions between determinate and extended (potentially indeterminate) growth on long branches does not allow conclusive inferences about the ancestral growth type for the above-mentioned nodes. Importantly, this ambiguity should not be taken as evidence in favour of extended (potentially indeterminate) growth. Both scenarios are inconclusive as far as the last common ancestor of the Amniota (1) is concerned, due to lack of data on growth type in the most basal sauropsids and synapsids. Groups were scored according to the presence/absence of growth plate cartilage, external fundamental system and capture–recapture field studies. See text for details.