Are diminutive turtles miniaturized? The ontogeny of plastron shape in emydine turtles

Abstract

Miniaturization, or the evolution of a dramatically reduced body size compared to related lineages, is an extraordinarily widespread phenomenon among metazoans. Evolutionary biologists have been fascinated by miniaturization because this transition has occurred numerous times, often among close relatives, providing a model system for studying convergent evolution and its underlying mechanisms. Much of the developmental work describing the ontogeny of miniature species suggests that paedomorphosis is the predominant avenue of miniaturization. Nevertheless, specific alterations to ontogeny appear highly variable, so that even related lineages with similar miniaturized traits produce those similarities via distinct ontogenetic paths. One major vertebrate group that has been overlooked in research on miniaturization is turtles. In the present study, we examined patterns of shape change in the plastron (the ventral part of the shell) over the course of ontogeny in a small clade of turtles (Emydinae) aiming to investigate whether two independently evolved diminutive members of the clade (Glyptemys muhlenbergii and Clemmys guttata) should be considered as miniaturized. We employ geometric morphometric methods to quantify the patterns of shape change these potentially miniaturized species and their relatives undergo during ontogeny, and use molecular phylogenetic trees to reconstruct ancestral conditions and provide information on the polarity of shape changes. We find that differing changes in ontogenetic parameters relative to ancestral conditions accompany the evolution of small size in emydines: G. muhlenbergii changes the duration of ontogeny and rate of shape change, whereas C. guttata changes growth rate. The observed ontogenetic repatterning of these species is reminiscent of changes in ontogeny and life history often found in miniaturized taxa. However, we conclude that C. guttata and G. muhlenbergii are not truly miniaturized because they still produce typical adult shell morphologies, and larger emydines display comparable ontogenetic flexibility. Because no emydines carry juvenile shell features forward into adulthood, we speculate that few, if any turtles, will show paedomorphic shell traits without corresponding changes in defensive strategy because such shells may offer insufficient protection. © 2013 The Linnean Society of London

Combining geometric morphometrics and finite element analysis with evolutionary modeling: towards a synthesis

“…Although these habitat preferences would be consistent with relaxed selective pressure for a streamlined shape compared to highly aquatic taxa such as many of the Trachemys or Pseudemys species in our analysis, continued interaction with aquatic environments by the Glyptemys species may mean that they still experience more selection than highly terrestrial species such as Terrapene ornata, which favors grasslands and spends very little time in standing or flowing water (Ernst et al, 1994). Alternatively, there may be other factors that favor a shell with a small cross-sectional area in Glyptemys, such as the need to navigate in dense wetland vegetation or leaf litter, climbing ability, or even constraints imposed by the unusually small body size of G. muhlenbergii (see Angielczyk and Feldman [2013] for a discussion of the effects of size and ontogeny on plastron shape in Glyptemys).…”

Intraspecific variation inAegla longirostri(Crustacea: Decapoda: Anomura) revealed by geometric morphometrics: evidence for ongoing speciation?

“…When divergent taxonomic characters are absent, the identification can be made through geometric morphometric techniques, which allow the direct quantification and analysis of biological forms (Rohlf & Marcus, ; Adams, Rohlf & Slice, ). This methodology has been used to investigate ecological and evolutionary questions, including inter‐ and intraspecific relationships (Adams & Rohlf, ; Hopkins & Thurman, ; Worthington, Berns & Swallow, ; Angielczyk & Feldman, ; Milankov et al ., ). Geometric morphometry is also reliable for evaluating morphological variation in apparently identical characters, and is consequently useful in discriminating cryptic species (Adams & Funk, ; Alibert et al ., ; Villemant, Simbolotti & Kenis, ; Tofilski, ).…”

The postembryonic transformation of the shell in emydine box turtles

“…Similar to Angielczyk and Feldman (), analyses were conducted on the averaged coordinates of symmetric plastron landmarks to avoid redundancy and inflation of degrees of freedom in statistical analyses (Cardini, ; M. L. Zelditch, Swiderski, & Sheets, ). Thus, we analyzed a reduced set of 12 landmarks (five averaged symmetric+seven midline landmarks).…”

“…Here, we revisit the ontogeny of plastral kinesis to further address the expectation that prepatterning of skeletal traits in embryos facilitates gradual and modular morphogenetic changes in growing turtles. Using emydine box turtles as a model, we tested the hypothesis that hatchlings of akinetic‐ versus kinetic‐shelled species already feature functionally relevant plastron shape differences, similar to adults (Angielczyk & Feldman, ; Angielczyk et al, ). We then tested the hypothesis that plastron shape changes relative to size are associated with hinge differentiation during the posthatching ontogeny of T. carolina (Cordero et al, ).…”

“…We then tested the hypothesis that plastron shape changes relative to size are associated with hinge differentiation during the posthatching ontogeny of T. carolina (Cordero et al, ). Shape variation related to the hinge has been primarily observed in the anterior plastron of emydine box turtles (Angielczyk & Feldman, ; Claude, ). We therefore tested for changes in the extent to which the anterior and posterior plastral lobes display shape covariance (i.e., modularity and integration) across ontogeny.…”