The evolutionary biomechanics of locomotor function in giant land animals

Abstract

Giant land vertebrates have evolved more than 30 times, notably in dinosaurs and mammals. The evolutionary and biomechanical perspectives considered here unify data from extant and extinct species, assessing current theory regarding how the locomotor biomechanics of giants has evolved. In terrestrial tetrapods, isometric and allometric scaling patterns of bones are evident throughout evolutionary history, reflecting general trends and lineage-specific divergences as animals evolve giant size. Added to data on the scaling of other supportive tissues and neuromuscular control, these patterns illuminate how lineages of giant tetrapods each evolved into robust forms adapted to the constraints of gigantism, but with some morphological variation. Insights from scaling of the leverage of limbs and trends in maximal speed reinforce the idea that, beyond 100–300 kg of body mass, tetrapods reduce their locomotor abilities, and eventually may lose entire behaviours such as galloping or even running. Compared with prehistory, extant megafaunas are depauperate in diversity and morphological disparity; therefore, turning to the fossil record can tell us more about the evolutionary biomechanics of giant tetrapods. Interspecific variation and uncertainty about unknown aspects of form and function in living and extinct taxa still render it impossible to use first principles of theoretical biomechanics to tightly bound the limits of gigantism. Yet sauropod dinosaurs demonstrate that >50 tonne masses repeatedly evolved, with body plans quite different from those of mammalian giants. Considering the largest bipedal dinosaurs, and the disparity in locomotor function of modern megafauna, this shows that even in terrestrial giants there is flexibility allowing divergent locomotor specialisations.

Adaptation to graviportality in Rhinocerotoidea? An investigation through the long bone shape variation in their hindlimb

“…Finally, the addition of the results on hind limb (this study) to those obtained on forelimb (Mallet et al, in press) enables the critical evaluation of the concept of graviportality and its application to Rhinocerotoidea (Hutchinson, 2021). The shape of the limb bones in Rhinocerotoidea diversified broadly during the more than 50 Ma of evolution of this group, while its variation still carries a strong phylogenetic signal.…”

“…As Rhinocerotoidea hardly display the anatomical criteria classically associated with graviportality, two possible assessments arise: either Rhinocerotoidea should not be considered graviportal, or the graviportal framework is too limited to describe the diverse conditions by which species adapt to heavy weight (Hutchinson, 2021). The limitations of the framework of Gregory (1912) and Osborn (1929) may be related to the archetypal groups used to define graviportality (and cursoriality), as they mainly considered elephants and extinct groups with a similar limb architecture like Dinocerata in this regard (Osborn, 1900).…”

“…Except in their general increase of robustness, Rhinocerotoidea show no clear convergence of shape or limb construction with that of Proboscidea, especially in extremely large but gracile taxa like Paraceratheriidae. Most criteria associated with graviportality in elephants are thus not universally shared in heavy quadrupeds showing that the classic graviportal framework should be considered with caution (Hutchinson, 2021). Therefore, it may be more relevant to search for the features repeatedly encountered in diverse taxa showing a high body mass before defining a general concept such as graviportality.…”

The evolution of asymmetrical gaits in gnathostome vertebrates

“…A second possibility is that the lack of asymmetrical gaits in several clades could be due to the lack of the required neural circuits or a change in musculoskeletal anatomy. Gigantism is thought to limit the use of galloping gaits as a result of biomechanical challenges of extreme bone loading (Hutchinson, 2021). In this case, selection for very large body size results in myriad phenotypic changes that make galloping mechanically impossible or at least very dangerous, which may explain why elephants do not gallop.…”

Convergent evolution of quadrupedality in ornithischian dinosaurs was achieved through disparate forelimb muscle mechanics

“…[1]) and how patterns of anatomical change may be influenced (or limited) by physical constraints on biological form (e.g. [2]). The secondary evolution of quadrupedality from bipedal ancestors is rare in tetrapods.…”