Evolutionary Change in Locomotion Close to the Origin of Amniotes Inferred From Trackway Data in an Ancestral State Reconstruction Approach

Abstract

Among amniote and non-amniote tetrapod trackways from late Carboniferous to early Permian deposits, certain trackway measures vary notably. Some of this variability can be attributed to evolutionary changes in trackmaker anatomy and locomotion style close to the origin of amniotes. Here we demonstrate that steps in early amniote locomotion evolution can be addressed by applying methods of ancestral state reconstruction on trackway data – a novel approach in tetrapod ichnology. Based on (a) measurements of 186 trackways referred to the Carboniferous and early Permian ichnogenera Batrachichnus, Limnopus, Hylopus, Amphisauropus, Matthewichnus, Ichniotherium, Dimetropus, Tambachichnium, Erpetopus, Varanopus, Hyloidichnus, Notalacerta and Dromopus, (b) correlation of these ichnotaxa with specific groups of amphibian, reptiliomorph, synapsid, and reptilian trackmakers based on imprint morphology and (c) known skeletal-morphology-based phylogenies of the supposed trackmakers, we infer ancestral states for functionally controlled trackway measures in a maximum likelihood approach. The most notable finding of our analysis is a concordant change in trackway parameters within a series of ancestral amniote trackmakers, which reflects an evolutionary change in locomotion: In the ancestors of amniotes and diadectomorphs, an increase in body size was accompanied by a decrease in (normalized) gauge width and glenoacetabular length and by a change in imprint orientation toward a more trackway-parallel and forward-pointing condition. In the subsequent evolution of diadectomorph, synapsid and reptilian trackmakers after the diversification of the clades Cotylosauria (Amniota + Diadectomorpha) and Amniota, stride length increased whereas gauges decreased further or remained relatively narrow within most lineages. In accordance with this conspicuous pattern of evolutionary change in trackway measures, we interpret the body size increase as an underlying factor that triggered the reorganization of the locomotion apparatus. The secondary increase in stride length, which occurred convergently within distinct groups, is interpreted as an increase in locomotion capability when the benefits of reorganization came into effect. The track-trackmaker pair of Ichniotherium sphaerodactylum and Orobates pabsti from the early Permian Bromacker locality of the Thuringian Forest, proposed in earlier studies as a suitable ancestral amniote track-trackmaker model, fits relatively well with our modeled last common ancestor of amniotes – with the caveat that the Bromacker material is younger and some of the similarities appear to be due to convergence.

Stride frequency or length? A phylogenetic approach to understand how animals regulate locomotor speed

“…Some evidence suggests that the tendency to primarily increase speed through stride frequency may be attributable to the conserved nature of locomotor motor patterns (Buchwitz et al, 2021;Cuff et al, 2019;Goslow et al, 1989;Lauder and Shaffer, 1988;Peters and Goslow, 1983;Wainwright et al, 1989). Utilizing a salamander model, Ijspeert and colleagues (2006Ijspeert and colleagues ( , 2007Ijspeert and colleagues ( , 2008 demonstrated that spinal stimulation of increasing intensity results in frequency-related changes in axial and appendicular movements.…”

“…Furthermore, Granatosky et al (2019a) show that while limb joint kinematics are highly labile across evolutionary history, much of the diversity in limb kinematics is a recent, suggesting mammalian, innovation. Finally, utilizing trackway evidence, Buchwitz et al (2021), proposed that temnospondyls (extinct primitive amphibians) showed little ability to modulate stride length. Such capabilities do not appear in the ichnofossil record until the emergence of Cotylosauria (Amniota+Didectomorpha).…”

“…With these considerations in mind, we explored the interrelationships between stride length, stride frequency and locomotor speed across a broad phylogenetic sample of tetrapods. We used this sample to assess whether patterns of these three variables are primarily driven by mechanical (Heglund and Taylor, 1988;Reilly et al, 2007;Strang and Steudel, 1990), allometric (Reilly et al, 2007), phylogenetic (Buchwitz et al, 2021;Larson et al, 2001) or ecological factors (Granatosky et al, 2019b;Karantanis et al, 2017;Nyakatura et al, 2008).…”

A new method to calculate limb phase from trackways reveals gaits of sauropod dinosaurs

“…Previous attempts to interpret gaits from fossil trackways remain speculative or inconclusive. 3,4 Stevens et al 5 demonstrated that trackmakers that only slightly differ in body length but employ different limb phases may produce identical footfall patterns. Given this ambiguity, it seemed that limb phase could not be estimated from trackways unless body size and shape of the trackmaker can be precisely constrained 5 -a task that is notoriously difficult to achieve when the assumed trackmaker taxon is extinct.…”

Skull Sutures and Cranial Mechanics in the Permian Reptile Captorhinus aguti and the Evolution of the Temporal Region in Early Amniotes

“…319 Ma ago; Ford and Benson, 2020). In contrast to the majority of coeval limbed vertebrates, the earliest amniotes and their closest extinct relatives adopted a predominantly or even exclusively terrestrial lifestyle (Sumida, 1997;Nyakatura et al, 2019;Buchwitz et al, 2021). This ecological shift had been accomplished by innovations in their developmental strategies (e.g., Packard and Seymour, 1997;Werneburg, 2019;Blackburn and Stewart, 2021) and was accompanied by further changes in their general anatomy, involving the appendicular skeleton and vertebral column (Sumida, 1997), as well as the skull (Bramble and Wake, 1985;Iordansky, 1990).…”