PG-18: turtles reach adult shell shapes at about 65% maximum carapace length

Abstract

Ontogenetic shell shape changes of turtles are often only documented for individual species. It is currently unclear how shell shape changes during ontogeny across species, if there are common trends, and at what point in ontogeny individuals reach their adult morphology. Inspired by questions of whether some morphologies are too juvenile to be included into macroevolutionary studies of shell shape, we develop ontogenetic shell shape curves based on landmarked 3D shell shapes of turtles. Species-specific allometric shape regressions confirm that turtles show marked ontogenetic shell shape change. Geometric morphometric analysis shows that juvenile turtles have rounded shells, and ontogenetic differentiation between species increases adult turtle disparity. Disparity analysis indicates that juvenile shells across turtle clades are more similar than adult shapes, suggesting an important role of developmental constraints on early turtle shell shape, and possible adaptive post-natal ontogenetic changes that produce the observed adult shell shape disparity. Ontogenetic shell shape curves indicate when turtles converge onto adult morphologies, here quantified as 85% the distance between juvenile shape and maximum size adult shape. This happens at about 65% of the species-specific maximum carapace sizes. Sexual shell shape dimorphism is comparatively low across turtles even in the presence of pronounced sexual size dimorphism. These preliminary results provide guidance for studying shell shape macroevolution, but need to be scrutinized further in the future by data addition.

Supplementary information: The online version contains supplementary material available at 10.1186/s13358-025-00395-0.

Keywords: Allometry; Morphometrics; Ontogeny; Sexual dimorphism; Shape change; Shell shape; Turtles.

Fig. 1

Ontogenetic shape changes in turtle shells across selected species. Landmark configurations shown for the 5% (left column) and 95% (middle column) percentiles of CAC values of A Podocnemis expansa, B Eretmochelys imbricata, C Chelonoidis niger, and D Kinosternon creaseri. Right column shows normalized Euclidean distances between landmarks of each configuration, whereby bluer points in the colour gradient denote greater morphological change. For each species, shells are shown in left lateral (top rows) and dorsal views (bottom rows)

Fig. 2

Ontogenetic shell shape curves for selected species. Bivariate plots of the common allometric component (CAC) against straight carapace length (SCL, in mm). A Kinosternon creaseri, B Trachemys ornata, C Manouria emys, D Podocnemis expansa. The size-range for adult CAC shape, based on our 85%-adult shape threshold, is indicated by grey boxes. The red vertical line indicates the size threshold at which CAC values reach 85% of the shape of record-sized specimens, with corresponding female and male percentages of maximum SCL indicated at the top of the line. Datapoints are colour-coded according to their cluster assignments (‘small’, ‘intermediate’ or ‘large’), and symbols represent sex. (X/Y%) values at largest datapoint indicates percentage of maximum female/male SCL recorded for the species. Solid lines are Gompertz curves fit across all data points. Dashed horizontal lines represent the lower 95% interval at which the asymptotic CAC value is reached according to the Gompertz functions

Fig. 3

Ontogenetic shell shape curves for selected species. Bivariate plots of multivariate shape against straight carapace length (SCL, in mm). A Chelus fimbriata, B Trachemys scripta, C Manouria emys, D Orlitia borneensis. The size-range for adult multivariate shape, based on our 85%-adult shape threshold, is indicated by grey boxes. The red vertical line indicates the size threshold at which multivariate shape values reach 85% of the shape of record-sized specimens, with corresponding female and male percentages of maximum SCL indicated at the top of the line. Datapoints are colour-coded according to their cluster assignments (‘small’, ‘intermediate’ or ‘large’), and symbols represent sex. (X/Y%) values at largest datapoint indicates percentage of maximum female/male SCL recorded for the species. Solid lines are Gompertz curves fit across all data points. Dashed horizontal lines represent the lower 95% interval at which the asymptotic multivariate shape value is reached according to the Gompertz functions

Fig. 4

Comparisons of allometric and sexual dimorphism effects on shell shape for selected species. A Difference in effect-sizes (Z-scores) of ‘shell shape ~ size + sex’ regressions for 15 turtle species. Negative values indicate sex effects are larger than size effects. Numbers correspond to: 1 - Astrochelys radiata, 2 - Centrochelys sulcata, 3 - Chelodina oblonga, 4 - Chelus fimbriata, 5 - Cuora flavomarginata, 6 - Dermatemys mawii, 7-  Emydura macquarii, 8 - Heosemys grandis, 9 - Heosemys annandalii, 10 - Kinosternon creaseri, 11 - Leucocephalon yuwonoi, 12 - Manouria emys, 13 - Mauremys sinensis, 14 - Mauremys rivulata, 15 - Orlitia borneensis, 16 - Pelomedusa subrufa, 17 - Phrynops hilarii, 18 - Podocnemis vogli, 19 - Stigmochelys pardalis, 20 - Trachemys ornata, 21 - Trachemys scripta. B Violin plots showing the distributions of Z-scores of size and sex effects across species-specific regressions. C Landmark configurations of similar-sized female and male specimens (female FMNH 261568, SCL = 186 mm; male FLMNH 109835, SCL = 183 mm) in the species with the largest effect of sex in shell shape regressions (Leucocephalon yuwonoi). D Landmark configurations of the smallest (AMNH 145108, SCL = 67 mm) and largest (FLMNH 111310, SCL = 215 mm) specimens in the species with the largest effect of sex in shell shape regressions (Leucocephalon yuwonoi). E Landmark configurations of the largest specimen of the species with the largest sex effect on shell shape (Leucocephalon yuwonoi) and of the largest specimen of the most closely related species for which we had data (Notochelys platynota, FMNH 151017, SCL = 230 mm). Right column in (C–E) shows normalized Euclidean distances between landmarks of each configuration, whereby bluer points denote greater morphological change. For each species, shells are shown in left lateral (top rows) and dorsal views (bottom rows)

Fig. 5

Morphological variation across ontogenetic stages in turtles. A First and second PCA axes illustrating main trends of turtle shell shape variation. Landmark configurations at the bottom indicate minimum (left) and maximum (right) PC1 values, whereas points on the right indicate minimum (bottom) and maximum (top) PC2 values. Grey points denote all specimens used in our analyses and different coloured points represent the different ontogenetic stages (‘small’, ‘intermediate’ and ‘large’). B, C Disparity ranges across ontogenetic stages in turtles using (B) sum of ranges (SoR) and (C) Procrustes variances. Asterisks (***) between ‘small’ and ‘intermediate’, and ‘small’ and ‘large’ groups indicate statistically non-overlapping confidence intervals of disparity values (P-values < 0.001; Table 2). Silhouettes are of different sized Emys orbicularis individuals in exhibition at the Natural History Museum of Fribourg (Switzerland)