The postembryonic transformation of the shell in emydine box turtles

Abstract

A key trend in the 210-million-year-old history of modern turtles was the evolution of shell kinesis, that is, shell movement during neck and limb retraction. Kinesis is hypothesized to enhance predator defense in small terrestrial and semiaquatic turtles and has evolved multiple times since the early Cretaceous. This complex phenotype is nonfunctional and far from fully differentiated following embryogenesis. Instead, kinesis develops slowly in juveniles, providing a unique opportunity to illustrate the postembryonic origins of an adaptive trait. To this end, we examined ventral shell (plastral) kinesis in emydine box turtles and found that hatchling plastron shape differs from that of akinetic-shelled relatives, particularly where the hinge that enables kinesis differentiates. We also demonstrated shape changes relative to plastron size in juveniles, coinciding with a shift in the carapace-plastron structural connection, rearrangement of ectodermal plates, and bone repatterning. Furthermore, because the shell grows larger relative to the head, complete concealment of the head and extremities is only achieved after relative shell proportions increase. Structural alterations that facilitate the box turtle's transformation are probably prepatterned in embryos but require functioninduced changes to differentiate in juveniles. This mode of delayed trait differentiation is essential to phenotypic diversification in turtles and perhaps other tetrapods.

Behavioural and physiological responses to simulated predator-induced stress in the eastern box turtle, Terrapene carolina carolina

“…4). This suggests that older turtles may utilize shell closure as an antipredator mechanism more successfully than younger, typically smaller turtles (Cordero et al, 2019). Our results indicate that there is a correlation between the size of a box turtle and its shell closing strength.…”

Skeletal repatterning enhances the protective capacity of the shell in African hinge‐back tortoises (Kinixys)

“…The resulting phenotypes may be subject to natural selection, as supported by experimental and mathematical models on the genetic pathways that control the spatial configuration of carapace scutes in turtle embryos (Moustakas-Verho et al, 2014). The phenotypic effects of such heritable genetic changes may emerge much later in life, as exemplified by Kinixys and emydine box turtles (Cordero et al, 2018;Cordero et al, 2019).…”

“…517–519) proposed that aberrant carapace phenotypes may arise if the coordinated expansion of serially arranged developmental units is modified: “If the horny plates grow ever so little faster than the bones below, they will fail to fit, will overcrowd one another, and will be forced to bulge or wrinkle.” The resulting phenotypes may be subject to natural selection, as supported by experimental and mathematical models on the genetic pathways that control the spatial configuration of carapace scutes in turtle embryos (Moustakas‐Verho et al, 2014). The phenotypic effects of such heritable genetic changes may emerge much later in life, as exemplified by Kinixys and emydine box turtles (Cordero et al, 2018; Cordero et al, 2019). The observed ossification pattern in juvenile Kinixys suggests that this clade retains the ground state condition (i.e., an incompletely ossified carapace) for Testudinidae at the onset of post‐hatching development (see Testudo ; Cherepanov, 2017).…”

“…Beyond histological descriptions in parrots (Tokita, 2003), few studies have managed to capture the tissue alterations associated with the construction and functional activation of skeletal kinesis. Nonetheless, similar histological changes (suture remodeling) were linked to the convergent evolution of shell kinesis in turtles (Cordero et al, 2018;Cordero et al, 2019). Dermally derived bones of the ventral shell (plastron) initially exhibit normal growth and suture formation in most kinetic-shelled turtles studied thus far, that is, Kinosternon, Sternotherus, Pelusios, and Emydinae (Cordero, 2021;Cordero et al, 2018).…”

“…By contrast, the carapacial hinge in K. natalensis, the smallest species in the genus, is confined to peripherals 7-8 (Boycott & Jacobsen, 1988;Broadley, 1997), which is similar to smaller adults of the larger Kinixys species. This size dependence may be explained as follows: (a) The mechanical strain exerted on the carapace by hindlimb retraction scales positively with body size in turtles (Aiello et al, 2013;Fish & Stayton, 2014), (b) As shell size increases, internal space to accommodate the limbs and head might also increase during retraction (Cordero et al, 2019), thereby augmenting the mechanical strain transferred to the carapacial buttresses (Polly et al, 2016); and (c) Disproportionate and redirected growth of peripheral 7 may further stimulate suture degeneration as body size increases.…”