The origin and loss of periodic patterning in the turtle shell

Abstract

The origin of the turtle shell over 200 million years ago greatly modified the amniote body plan, and the morphological plasticity of the shell has promoted the adaptive radiation of turtles. The shell, comprising a dorsal carapace and a ventral plastron, is a layered structure formed by basal endochondral axial skeletal elements (ribs, vertebrae) and plates of bone, which are overlain by keratinous ectodermal scutes. Studies of turtle development have mostly focused on the bones of the shell; however, the genetic regulation of the epidermal scutes has not been investigated. Here, we show that scutes develop from an array of patterned placodes and that these placodes are absent from a softshelled turtle in which scutes were lost secondarily. Experimentally inhibiting Shh, Bmp or Fgf signaling results in the disruption of the placodal pattern. Finally, a computational model is used to show how two coupled reaction-diffusion systems reproduce both natural and abnormal variation in turtle scutes. Taken together, these placodal signaling centers are likely to represent developmental modules that are responsible for the evolution of scutes in turtles, and the regulation of these centers has allowed for the diversification of the turtle shell.

Genetic analyses in Lake Malawi cichlids identify new roles for Fgf signaling in scale shape variation

“…In addition, loss-of-function mutations in Fgf receptors were found to be associated with independent scale loss in two cyprinid lineages (domesticated carp 15 ; Phoxinellus 16 ). These insights are consistent with roles for Fgf signaling in the development of other epithelial appendages, including feathers 17 and turtle shell scutes 18 . In instances of scale loss, the causative mutation likely disrupts placode formation, leading to loss of the organ.…”

Skeletal remodelling suggests the turtle's shell is not an evolutionary straitjacket

“…Instead, its differentiation is probably a plastic side-effect of constrained scapula growth within an exceptionally flattened shell, as suggested by the positive correlation of scapula mass and shell height. These observations contribute to a growing consensus on fundamental developmental differences between hard-and soft-shelled turtles [3,[8][9][10]17]. Skeletal morphology may vary due to epigenetic tissue remodelling induced by novel mechanical stimuli experienced in development [2,23].…”

“…Exploring this ecological diversity may demonstrate how developmental change has contributed to subsequent evolution of the basic turtle body plan [4]. Recent studies focusing on two distantly related species revealed surprising variation in how the shell forms [8][9][10]. Still, as an outcome of shell development, all extant species share a similar anatomical configuration: the shoulder girdle is situated anteriorly to the rib cage and is encapsulated within the shell [11].…”

Comparative analysis of pleurodiran and cryptodiran turtle embryos depicts the molecular ground pattern of the turtle carapacial ridge

“…Care should be taken in the future as to the expression patterns found and the conclusions to be drawn from them. We propose that future research must be very specific in (i) the stage of embryos assayed, always according to stan- (ii) utilization of unequivocal probes, with special care in the case of close paralogues (for instance, by avoiding probes based in conserved domains); and (iii), when possible, use embryos from different turtle clades, in order to be able to, on the one hand, infer common patterns, and on the other to distinguish between different developmental modules, as soft-shelled turtles are expected to have lost patterns seen related with scutes development (see Moustakas-Verho et al, 2014).…”