Turtle body size evolution is determined by lineage-specific specializations rather than global trends

Abstract

Organisms display a considerable variety of body sizes and shapes, and macroevolutionary investigations help to understand the evolutionary dynamics behind such variations. Turtles (Testudinata) show great body size disparity, especially when their rich fossil record is accounted for. We explored body size evolution in turtles, testing which factors might influence the observed patterns and evaluating the existence of long-term directional trends. We constructed the most comprehensive body size dataset for the group to date, tested for correlation with paleotemperature, estimated ancestral body sizes, and performed macroevolutionary model-fitting analyses. We found no evidence for directional body size evolution, even when using very flexible models, thereby rejecting the occurrence of Cope's rule. We also found no significant effect of paleotemperature on overall through-time body size patterns. In contrast, we found a significant influence of habitat preference on turtle body size. Freshwater turtles display a rather homogeneous body size distribution through time. In contrast, terrestrial and marine turtles show more pronounced variation, with terrestrial forms being restricted to larger body sizes, up to the origin of testudinids in the Cenozoic, and marine turtles undergoing a reduction in body size disparity after the extinctions of many groups in the mid-Cenozoic. Our results, therefore, suggest that long-term, generalized patterns are probably explained by factors specific to certain groups and related at least partly to habitat use.

Keywords: Cope's rule; Testudinata; ancestral states estimation; evolutionary models.

FIGURE 1

Ancestral body sizes (log₁₀ maximum dorsal carapace length in millimeters) mapped onto Testudinata phylogeny (“St18”), with (a) complete tree and (b) extant‐only subtree. Ancestral body size for different taxonomic groups (c); small gray dots indicate all taxa within that lineage; colored triangles represent the ancestral estimates of stem‐groups; circles represent ancestral estimates of the crown groups; and squares represent ancestral estimates of the crown groups without the fossil taxa. Gray area indicates sizes between 200 and 500 mm. The numbers indicate the same groups in a–c.

FIGURE 2

(a) Through‐time patterns of Testudinata body size disparity (standard deviation of log₁₀ maximum dorsal carapace length in millimeters) and paleotemperature (δ¹⁸O isotopic data from Zachos et al., 2008) during the last ~70 Ma. Error bars were calculated by bootstrapping the disparity data 500 times. δ¹⁸O is used as proxy for paleotemperature and is inversely proportional to temperature. (b) Linear regression (OLS) between turtle body size disparity and δ¹⁸O data (regression results shown in Table 2).

FIGURE 3

Temporal distribution of body sizes (log₁₀ maximum dorsal carapace length in millimeters) in turtles for different ecological habitats. Gray dots represent all taxa, whereas colored dots represent taxa subdivided into three ecological categories. (a) terrestrial taxa (red dots); (b) freshwater taxa (light green dots); (c) and marine taxa (light blue dots). Horizontal gray segments represent the range of occurrence of each taxon; (d) Boxplot showing body size of different ecological categories divided into time intervals. Silhouettes adapted from Jaffe et al. (2011).

FIGURE A1

The “Ev19” time‐calibrated supertree, represented by the 50% majority rule tree. Blue bars represent the 95% highest posterior density (HPD) age ranges for each node.

FIGURE A2

The “St18” time‐calibrated supertree, represented by the 50% majority rule tree. Blue bars represent the 95% highest posterior density (HPD) age ranges for each node.

FIGURE A3

Ancestral body sizes (log₁₀ maximum dorsal carapace length in millimeters) mapped onto Ev19 supertree, with (a) complete tree and (b) extant‐only subtree. Ancestral body size for different taxonomic groups (c); small gray dots indicate all taxa within that lineage; colored triangles represent the ancestral estimates of stem‐groups; circles represent ancestral estimates of the crown groups; and squares represent ancestral estimates of the crown groups without the fossil taxa. Gray area indicates sizes between 200 and 500 mm. The numbers indicate the same groups in a–c.