doi: 10.1038/s41598-020-62179-5.
Feeding biomechanics suggests progressive correlation of skull architecture and neck evolution in turtles
Affiliations
- PMID: 32218478
- PMCID: PMC7099039
- DOI: 10.1038/s41598-020-62179-5
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Feeding biomechanics suggests progressive correlation of skull architecture and neck evolution in turtles
Sci Rep.
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Abstract
The origin of turtles is one of the most long-lasting debates in evolutionary research. During their evolution, a series of modifications changed their relatively kinetic and anapsid skull into an elongated akinetic structure with a unique pulley system redirecting jaw adductor musculature. These modifications were thought to be strongly correlated to functional adaptations, especially to bite performance. We conducted a series of Finite Element Analyses (FEAs) of several species, including that of the oldest fully shelled, Triassic stem-turtle Proganochelys, to evaluate the role of force distribution and to test existing hypotheses on the evolution of turtle skull architecture. We found no support for a relation between the akinetic nature of the skull or the trochlear mechanisms with increased bite forces. Yet, the FEAs show that those modifications changed the skull architecture into an optimized structure, more resistant to higher loads while allowing material reduction on specific regions. We propose that the skull of modern turtles is the result of a complex process of progressive correlation between their heads and highly flexible necks, initiated by the origin of the shell.
Conflict of interest statement
The authors declare no competing interests.
Figures
Stress plots resulting from biomechanical analysis of turtles simulated for bilateral biting. (A–M), von Mises stress contour plots on a time-calibrated phylogeny (modified from Joyce et al.). (A), †Proganochelys quenstedtii, (B), †Kayentachelys aprix, (C), †Eubaena cephalica, (D), Podocnemis expansa, (E), Pelomedusa subrufa, (F), Chelodina oblonga, (G), Emydura subglobosa, (H), Pelodiscus sinensis, (I), Platysternon megacephalum, (J), Graptemys geographica, (K), Terrapene carolina, (L), Emys orbicularis, (M), Chelydra serpentina. Contour plots are scaled to the same size and 5 MPa peak stress. Dotted curves represent the margins of the emarginations. The purple “α” and the blue “β” rectangles represent the first and second proposed selective regimes described below and on Fig. 5. Caption: 1a, enlarged otic chamber, but shallow tympanic cavity; 1b, enlarged otic chamber and deep tympanic cavity (largest); 2, adductor chamber extending posterior to otic chamber; 3a, basipterygoid process sutured and facing ventrally (low possible kinesis); 3b, basipterygoid process sutured and facing laterally (lower possible kinesis); 3c, basipterygoid process absent (definitive akinesis); 4, secondary lateral braincase wall; 5a, reduced interpterygoid vacuities; 5b, closed interpterygoid vacuities; 6, reduced foramen palatinum posterius; 7, reduced temporal roof by emarginations; 8, trochlear process; *, reversals.
Von Mises stress contour plots of the ventral region of the skull. Contour plots are scaled to the same size and 5 MPa peak stress. Red and black arrows represent the bite and constrained points, respectively. Dotted curves anteriorly and posteriorly, identify the triturating surface and the basipterygoid articulation/suture.
Ventral and left lateral von Mises stress contour plots for hypothetical models of †Proganochelys quenstedtii and †Eubaena cephalica. †Proganochelys quenstedtii with (A), basipterygoid suture, (B), supraoccipital crest, and (C), both modifications; (D), †Eubaena cephalica with a hypertrophied pterygoid process and both trochlear loads simulated. Contour plots are all scaled to the same size and 5 MPa peak stress. Dotted curves in ventral view, anteriorly and posteriorly, identify the triturating surface and the basipterygoid articulation/suture, and in lateral view the anteroventral and posterodorsal emarginations. Abbreviations: ptp, pterygoid trochlear process; soc, supraoccipital crest.
Bite force and efficiency in turtles. (a–b), Boxplots of bite efficiency based on (a), FEA estimates and (b), in vivo measurements (scaled bite force calculated by dividing measured bite force by carapace size). (c), Bite force estimates based on FEA for sampled taxa.
Hypothesis of progressive correlation between neck and head during turtle evolution. The origin of the turtle shell initiates the first selective regime (α) in which muscle rearrangements enable more flexible necks that overcome the lack of mobility of the shelled body, but also exert distinct compression and tension loads on the skull. This is compensated by an increasing stiffness (through palatoquadrate fusion, closure of basipterygoid region (1), secondary braincase lateral wall (2) formation). The new, stiffened skull architecture can withstand higher loads at the same time allowing material reduction in the temporal region, opening the path to a second selective regime (β). Longer and flatter skulls (6) evolve, together with posterior expansion of temporal crests (5) and the enlarged otic chamber (3), both features reducing available volume inside the adductor chamber and triggering the appearance of a trochlear mechanism (4). Broader insertion sites for neck musculature offered by expanded temporal crests (5) support a new round of neck modifications, resulting in longer necks and modern types of neck retraction (7). Temporal emarginations (8) evolve in response to new forces generated by more powerful neck musculature. Model of †Eubaena cephalica as in Supplementary Fig. 9.
References
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- Bels, V. & Herrel, A. Feeding, a Tool to Understand Vertebrate Evolution Introduction to “Feeding in Vertebrates”. In Feeding in Vertebrates: Evolution, Morphology, Behavior, Biomechanics (eds. Bels, V. & Whishaw, I. Q.) 1–18 (Springer International Publishing. 10.1007/978-3-030-13739-7_1 (2019).
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- Ferreira, G. S. & Werneburg, I. Evolution, Diversity, and Development of the Craniocervical System in Turtles with Special Reference to Jaw Musculature. in Heads, Jaws, and Muscles, Fascinating Life Sciences 171–206 (Springer Nature Switzerland AG). 10.1007/978-3-319-93560-7_8 (2019).
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- Werneburg, I. Functional categories and ontogenetic origin of temporal skull openings in amniotes. Front. Earth Sci. 10.3389/feart.2019.00013 (2019).
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