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Alligator hindlimb muscles involved in the high walking for which electromyographical data have been recorded. Lines of actions are indicated for muscles active in either stance phase (red), swing phase (blue) or with activity in both phases (black); gray shading in arrows indicates that the muscle lies medial to the femur. AMB1, ambiens, head 1; ADD1, adductor femoris 1; CFL, caudofemoralis longus; FMTI, femorotibialis internus; FTE, flexor tibialis externus; FTI2, flexor tibialis internus, head 2; G, gastrocnemius; ILFEM, iliofemoralis; ILFIB, iliofibularis; ILTIB1/2 iliotibialis, head 1/2; PIFE2/3, puboischiofemoralis externus, head 2/3; PIFI2, puboischiofemoralis internus, head 2; PIT, puboischiotibialis; TA, tibialis anterior. Data for muscles marked with asterisks are taken from Gatesy (1997). The continuation of the AMB1 tendon through the extensor sheet and into the Achilles tendon is not shown.
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... The weight of the hindlimb muscles of quadrupedal tetrapod species accounts for a large proportion of body weight. Compared with the hindlimbs of other vertebrate groups, the hindlimbs of alligators have stronger compliant muscles, which enhances their mobility [23][24][25]. Alligators are unusual among tetrapods in their ability to use a wide range of hindlimb postures, even over a restricted range of speeds [26,27]. Research conducted on the skeletal muscles of hibernating animals demonstrates that their skeletal muscles exhibit well-maintained strength and anti-fatigue capabilities throughout the period of hibernation [28][29][30]. ...
Many ectotherms hibernate to increase their chances of survival during harsh winter conditions. The role of DNA methylation in regulating gene expression related to hibernation in ectotherms remains unclear. Here, we employed whole-genome bisulfite sequencing (WGBS) technology to construct a comprehensive genome-wide DNA methylation landscape of the hindlimb muscles in the Chinese alligator during hibernation and active periods. The results indicated that methylation modifications were most abundant at CG sites, identifying 9447 differentially methylated regions (DMRs) and 2329 differentially methylated genes (DMGs). KEGG pathway enrichment analysis of the DMGs revealed significant enrichment in major pathways such as the neurotrophin signaling pathway, the MAPK signaling pathway, the GnRH signaling pathway, the biosynthesis of amino acids, and the regulation of the actin cytoskeleton, which are closely related to lipid metabolism, energy metabolism, and amino acid metabolism. Among these, 412 differentially methylated genes were located in promoter regions, including genes related to energy metabolism such as ATP5F1C, ATP5MD, PDK3, ANGPTL1, and ANGPTL2, and genes related to ubiquitin-proteasome degradation such as FBXO28, FBXO43, KLHL40, and PSMD5. These findings suggest that methylation in promoter regions may play a significant role in regulating the adaptive hibernation mechanisms in the Chinese alligator. This study contributes to a further understanding of the epigenetic mechanisms behind the hibernation of the Chinese alligator.
... Additionally, tail elevation might impact loads on the hindlimb to a greater extent than loads on the forelimb. To better understand the limb-specific interactions between posture and motor patterns in the forelimb and hindlimb, integrated data on limb kinematics, external forces, motor patterns, and bone strains (Reilly et al., 2005) from both limbs would be required. ...
The evolution of archosaurs provides an important context for understanding the mechanisms behind major functional transformations in vertebrates, such as shifts from sprawling to erect limb posture and the acquisition of powered flight. While comparative anatomy and ichnology of extinct archosaurs have offered insights into musculoskeletal and gait changes associated with locomotor transitions, reconstructing the evolution of motor control requires data from extant species. However, the scarcity of electromyography (EMG) data from the forelimb, especially of crocodylians, has hindered understanding of neuromuscular evolution in archosaurs. Here, we present EMG data for nine forelimb muscles from American alligators during terrestrial locomotion. Our aim was to investigate the modulation of motor control across different limb postures and examine variations in motor control across phylogeny and locomotor modes. Among the nine muscles examined, m. pectoralis, the largest forelimb muscle and primary shoulder adductor, exhibited significantly smaller mean EMG amplitudes for steps in which the shoulder was more adducted (i.e., upright). This suggests that using a more adducted limb posture helps to reduce forelimb muscle force and work during stance. As larger alligators use a more adducted shoulder and hip posture, the sprawling to erect postural transition that occurred in the Triassic could be either the cause or consequence of the evolution of larger body size in archosaurs. Comparisons of EMG burst phases among tetrapods revealed that a bird and turtle, which have experienced major musculoskeletal transformations, displayed distinctive burst phases in comparison to those from an alligator and lizard. These results support the notion that major shifts in body plan and locomotor modes among sauropsid lineages were associated with significant changes in muscle activation patterns.
... of the body into the direction of travel (Riskin et al., 2016), greater overall capacity for speed (Reilly et al., 2005;Fuller et al., 2011), and reduced torsional stresses at limb long bone midshafts (Blob, 2001). Our results thus lend further tentative support to the possibility of such advanced locomotion (as outlined in the previous sentence) already present in the last common ancestor of diadectids and crown amniotes. ...
... Animals generally engage in diverse behaviors that often involve larger joint excursions and thus also muscle strains than cyclic steady-state walking. Orobates was potentially capable of locomotion at different body heights (cf. the "low walks" and "high walks" of crocodiles, e.g., Gatesy, 1991;Reilly et al., 2005). Regardless, the results derived from our modeling approach should be considered tentative steps into the incorporation of soft tissue anatomy into the reconstruction of locomotor properties. ...
About this Research Topic
The fish to tetrapod transition transformed the tetrapod body plan, eventually allowing tetrapods to move, eat, breathe, and reproduce on land. Reconstruction of soft tissues in early tetrapods and their relatives has the potential to solve controversies about the behavior and ecology of the earliest terrestrial vertebrates. This task has been attempted many times in many different ways, from detailed drawings made in the 1920s to modern biomechanical models.
We aim to present soft tissue descriptions and an overview of current soft tissue reconstruction methods and what they can tell us about functional anatomy in extinct animals. By doing so, we can help to define remaining challenges and project the next advances in this field.
We are interested in manuscripts that explore the use of various reconstruction methods and what they can tell us about the evolution of soft tissue anatomy and function surrounding the tetrapod water-land transition. These should include studies using a wide variety of methods, taxa, and anatomical structures. Especially welcome are studies on:
• Taxa closely related to stem tetrapods, particularly sarcopterygian fish, stem tetrapods, stem and early amniotes, and stem lissamphibians
• Methods grounded in experimental data from extant taxa, such as comparative anatomy, development, and phylogenetic relationships
• Paleontological methods such as exceptionally preserved fossils and high-resolution scans
• Virtual methods such as biomechanical models
• Soft tissue structures such as muscles, cartilage, vessels, and nerves
Keywords: Sarcopterygia, fossil, fin-limb, muscle, biomechanics
With 13 contributions by 48 authors, incl.: Ryan M. Campbell, Gabriel Vinas, Maciej Henneberg and Rui Diogo; Alice M. Clement, Corinne L. Mensforth, T. J. Challands, Shaun P. Collin and John A. Long; Virginia Abdala, Luciana Cristobal, Mónica C. Solíz and Daniel A. Dos Santos; Nikolay Natchev, Kristina Yordanova, Sebastian Topliceanu, Teodora Koynova, Dimitar Doichev and Dan Cogălniceanu; Michelle Zwafing, Stephan Lautenschlager, Oliver E. Demuth and John A. Nyakatura; Julia Molnar; Tatsuya Hirasawa, Camila Cupello, Paulo M. Brito, Yoshitaka Yabumoto, Sumio Isogai, Masato Hoshino and Kentaro Uesugi; Rohan Mansuit and Anthony Herrel; Ingmar Werneburg and Pascal Abel; Jacob B. Pears, Carley Tillett, Rui Tahara, Hans C. E. Larsson and Catherine A. Boisvert; Pascal Abel, Yannick Pommery, David Paul Ford, Daisuke Koyabu and Ingmar Werneburg; Zhikun Gai, Min Zhu, Per Erik Ahlberg and Philip Donoghue
https://www.frontiersin.org/research-topics/14838
https://www.frontiersin.org/research-topics/14838/tetrapod-water-land-transition-reconstructing-soft-tissue-anatomy-and-function#articles
... Intriguingly, our representative trial had similarities to the fourth subject described by Gatesy (1991) that tended to adduct its hip in stance; unlike the other, more abducted alligators; but our subject did not extend its knee in the same way. These motions and forces otherwise compare favourably with data from high-walking alligators (Gatesy 1991;Blob and Biewener 2001;Reilly et al. 2005;Tsai et al. 2020;Manafzadeh et al. 2021;Iijima et al. 2021), so the general patterns observed in C. niloticus appear to be ancestral for Crocodylia. How, then, do these hindlimb dynamics compare with those of birds? ...
... Considering the above walking dynamics for Crocodylia and Aves (including other studies by Gatesy 1991; Rubenson et al. 2004Rubenson et al. , 2007Willey et al. 2004;Reilly et al. 2005;Kambic et al. 2014Kambic et al. , 2015Schwaner et al. 2022), there are common general patterns for Archosauria studied to date (see also Manafzadeh et al. 2021). Most notably, vertical GRFs have two peaks (much more subtle in Crocodylia) during a stance phase of walking, and the mediolateral GRF vector is medially oriented, of comparable peak magnitude to the horizontal GRF vector (Table 1). ...
... Yet as Bishop et al. (2021c) noted, quite a few muscles show secondary bursts of activity in the opposite phase from their main burst (e.g., ITCa, p; IFE; PIFI2; ADD1; FTE; AMB). Similar biphasic or pulsatile bursts also are evident in some extant archosaurian muscles (Gatesy 1997(Gatesy , 1999Reilly et al. 2005;Cuff et al. 2019). ...
Archosauria diversified throughout the Triassic Period before experiencing two mass extinctions near its end ∼201 Mya, leaving only the crocodile-lineage (Crocodylomorpha) and bird-lineage (Dinosauria) as survivors; along with the pterosaurian flying reptiles. About 50 years ago, the “locomotor superiority hypothesis” (LSH) proposed that dinosaurs ultimately dominated by the Early Jurassic Period because their locomotion was superior to other archosaurs’. This idea has been debated continuously since, with taxonomic and morphological analyses suggesting dinosaurs were “lucky” rather than surviving due to being biologically superior. However, the LSH has never been tested biomechanically. Here we present integration of experimental data from locomotion in extant archosaurs with inverse and predictive simulations of the same behaviours using musculoskeletal models, showing that we can reliably predict how extant archosaurs walk, run and jump. These simulations have been guiding predictive simulations of extinct archosaurs to estimate how they moved, and we show our progress in that endeavour. The musculoskeletal models used in these simulations can also be used for simpler analyses of form and function such as muscle moment arms, which inform us about more basic biomechanical similarities and differences between archosaurs. Placing all these data into an evolutionary and biomechanical context, we take a fresh look at the LSH as part of a critical review of competing hypotheses for why dinosaurs (and a few other archosaur clades) survived the Late Triassic extinctions. Early dinosaurs had some quantifiable differences in locomotor function and performance vs. some other archosaurs, but other derived dinosaurian features (e.g., metabolic or growth rates, ventilatory abilities) are not necessarily mutually exclusive from the LSH; or maybe even an opportunistic replacement hypothesis; in explaining dinosaurs’ success.
... de realização de movimentos amplos em terra, o que nos seus primórdios, já lhes permitia a caça ativa de diapsidas menores. Trata-se de animais, que podem galopar, e que a partir da postura normal, com os membros lateralizados e em extensão, assumem uma postura dos mesmos, quase vertical, sob o corpo, realizando uma série de movimentos essenciais (Reilly et. al. 2004;Britton 2009). ...
... O m. iliotibial 1 foi identificado no presente estudo com origem cranial, dorsolateral na asa ilíaca e inserção na tuberosidade da tíbia, no mesmo nível do m. iliotibial 2. Em A. mississipienses (Reilly et al. 2004) o m. iliotibial 1, além de extensor e abdutor do joelho, como referido em C. crocodilus e C. latirostris , foi descrito como estabilizador da cintura pelvina e joelho. Trata-se de um músculo com localização profunda ao m. iliotibial 2, diferente do que foi identificado no presente estudo e nas demais espécies utilizadas para comparação. ...
... odylia (Allen et al. 2014). Em C. crocodilus, a cabeça 1, interdigita fibras musculares com a cabeça 2, e a cabeça 3 foi identificada caudal em relação ao m. adutor 1, com ação de adução e flexão da coxa, comum ao grupo , Gatesy 1997. Em A. mississipienses o mesmo grupo muscular foi destacado em ação significativa de estabilização na fase de apoio (Reilly et. al. 2004 A origem do m. puboisquiofemoral interno 1 (figura 2, 6) foi identificada em C. crocodilus na asa ilíaca em localização ventral e medial, e da cabeça 2, nos processos transversos das vértebras lombares, bem como, inserção medial e lateral, respectivamente, em relação ao quarto trocanter. Em P. gracilis (Schachner et al. 2011), a origem ...
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... The association of greater humeral adduction and lesser humeral axial rotation in alligators matches expectations from other taxa, but the finding of greater femoral adduction and greater femoral axial rotation was unexpected. Even with more erect limb posture, internal rotation of the femur may play an important role during stance in alligators, given the potential for a strong internal rotation moment about the femoral long axis exerted by the femoral retractor M. caudofemoralis longus (CFL) (Blob, 2000;Gatesy, 1990Gatesy, , 1997Reilly et al., 2005). However, some debate about this possibility also exists, as CFL has been regarded as an external rotator of the femur in some recent studies of crocodylians (Allen et al., 2021;Wiseman et al., 2021). ...
As animals increase in size, common patterns of morphological and physiological scaling may require them to perform behaviors such as locomotion while experiencing a reduced capacity to generate muscle force and an increased risk of tissue failure. Large mammals are known to manage increased mechanical demands by using more upright limb posture. However, the presence of such size-dependent changes in limb posture has rarely been tested in animals that use non-parasagittal limb kinematics. Here, we used juvenile to subadult American alligators (total length 0.46–1.27 m, body mass 0.3–5.6 kg) and examined their limb kinematics, forces, joint moments, and center of mass to test for ontogenetic shifts in posture and limb mechanics. Larger alligators typically walked with a more adducted humerus and femur and a more extended knee. Normalized peak joint moments reflected these postural patterns, with shoulder and hip moments imposed by the ground reaction force showing relatively greater magnitudes in the smallest individuals. Thus, as larger alligators use more upright posture, they incur relatively smaller joint moments than smaller alligators, which could reduce the forces that the shoulder and hip adductors of larger alligators must generate. The center of mass (CoM) shifted nonlinearly from juveniles through subadults. The more anteriorly positioned CoM in small alligators, together with their compliant hindlimbs, contributes to their higher forelimb and lower hindlimb normalized peak vertical forces in comparison to larger alligators. Future studies of alligators that approach maximal adult sizes could give further insight into how animals with non-parasagittal limb posture modulate locomotor patterns as they increase in mass and experience changes in the CoM.
... Nevertheless, given these caveats, there appears to be little-to-no evidence of impact transient forces in many clades of tetrapods. This includes turtles and tortoises (Butcher & Blob, 2008;Jayes & Alexander, 1980), crocodilians (Nyakatura et al., 2019;Reilly, Willey, Biknevicius, & Blob, 2005), lizards (Blob & Biewener, 2001;McElroy, Wilson, Biknevicius, & Reilly, 2014;Nyakatura et al., 2019;Ritter, 1995), and salamanders (Kawano & Blob, 2013;Nyakatura et al., 2019). Frogs, which typically land forelimb-first and gather their hindlimb subsequent to landing (Nauwelaerts & Aerts, 2006;Reilly et al., 2016), therefore also lack hindlimb impact transient forces (Reilly et al., 2016). ...
The lateral and medial menisci are fibrocartilaginous structures in the knee that play a crucial role in normal knee biomechanics. However, one commonly cited role of the menisci is that they function as “shock absorbers.” Here we provide a critique of this notion, drawing upon a review of comparative anatomical and biomechanical data from humans and other tetrapods. We first review those commonly, and often exclusively, cited studies in support of a shock absorption function and show that evidence for a shock absorptive function is dubious. We then review the evolutionary and comparative evidence to show that (1) the human menisci are unremarkable in morphology compared with most other tetrapods, and (2) “shock” during locomotion is uncommon, with humans standing out as one of the only tetrapods that regularly experiences high levels of shock during locomotion. A shock‐absorption function does not explain the origin of menisci, nor are human menisci specialized in any way that would explain a unique shock‐absorbing function during human gait. Finally, we show that (3) the material properties of menisci are distinctly poorly suited for energy dissipation and that (4) estimations of meniscal energy absorption based on published data are negligible, both in their absolute amount and in comparison to other well‐accepted structures which mitigate shock during locomotion. The menisci are evolutionarily ancient structures crucial for joint congruity, load distribution, and stress reduction, among a number of other functions. However, the menisci are not meaningful shock absorbers, neither in tetrapods broadly, nor in humans.
... of the body into the direction of travel (Riskin et al., 2016), greater overall capacity for speed (Reilly et al., 2005;Fuller et al., 2011), and reduced torsional stresses at limb long bone midshafts (Blob, 2001). Our results thus lend further tentative support to the possibility of such advanced locomotion (as outlined in the previous sentence) already present in the last common ancestor of diadectids and crown amniotes. ...
... Animals generally engage in diverse behaviors that often involve larger joint excursions and thus also muscle strains than cyclic steady-state walking. Orobates was potentially capable of locomotion at different body heights (cf. the "low walks" and "high walks" of crocodiles, e.g., Gatesy, 1991;Reilly et al., 2005). Regardless, the results derived from our modeling approach should be considered tentative steps into the incorporation of soft tissue anatomy into the reconstruction of locomotor properties. ...
The stem amniote Orobates pabsti has been reconstructed to be capable of relatively erect, balanced, and mechanically power-saving terrestrial locomotion. This suggested that the evolution of such advanced locomotor capabilities preceded the origin of crown-group amniotes. We here further investigate plausible body postures and locomotion of Orobates by taking soft tissues into account. Freely available animation software BLENDER is used to first reconstruct the lines of action of hindlimb adductors and retractors for Orobates and then estimate the muscle strain of these muscles. We experimentally varied different body heights in modeled hindlimb stride cycles of Orobates to find the posture that maximizes optimal strains over the course of a stride cycle. To validate our method, we used Caiman crocodilus. We replicated the identical workflow used for the analysis of Orobates and compared the locomotor posture predicted for Caiman based on muscle strain analysis with this species’ actual postural data known from a previously published X-ray motion analysis. Since this validation experiment demonstrated a close match between the modeled posture that maximizes optimal adductor and retractor muscle strain and the in vivo posture employed by Caiman, using the same method for Orobates was justified. Generally, the use of muscle strain analysis for the reconstruction of posture in quadrupedal vertebrate fossils thus appears a promising approach. Nevertheless, results for Orobates remained inconclusive as several postures resulted in similar muscle strains and none of the postures could be entirely excluded. These results are not in conflict with the previously inferred moderately erect locomotor posture of Orobates and suggest considerable variability of posture during locomotion.
... The general kinematics of these gaits have been previously well-studied (e.g. Blob & Biewener, 2001;Brinkman, 1980;Gatesy, 1991;Parrish, 1986;Reilly & Blob, 2003;Reilly & Ellias, 1998;Reilly et al., 2005;Whitaker & Andrews, 1988), in addition to faster modes of locomotion such as asymmetrical bounding and galloping gaits Renous et al., 2002). ...
... Importantly, unlike the hip adductors and extensors, as well as the ankle extensors and MTP flexors, not all muscles with knee flexor moment arms are predominantly active in stance phase in Crocodylia. Electromyographic activity (mostly for Alligator high walks) during the stance phase has been measured for the flexor cruris muscles (flexor tibialis heads and puboischiotibialis) and the caudofemoralis longus (some knee flexor forces may be transmitted via its secondary tendon to the lower limb); unlike iliofibularis Gatesy, 1997;Reilly et al., 2005). Hence stance phase knee flexor leverage might be less crucial than knee extensor leverage, particularly for iliofibularis. ...
We developed a three‐dimensional, computational biomechanical model of a juvenile Nile crocodile (Crocodylus niloticus) pelvis and hindlimb, composed of 47 pelvic limb muscles, to investigate muscle function. We tested whether crocodiles, which are known to use a variety of limb postures during movement, use limb orientations (joint angles) that optimise the moment arms (leverages) or moment‐generating capacities of their muscles during different limb postures ranging from a high walk to a sprawling motion. We also describe the three‐dimensional (3D) kinematics of the crocodylian hindlimb during terrestrial locomotion across an instrumented walkway and a treadmill captured via X‐ray Reconstruction of Moving Morphology (biplanar fluoroscopy; ‘XROMM’). We reconstructed the 3D positions and orientations of each of the hindlimb bones and used dissection data for muscle lines of action to reconstruct a focal, subject‐specific 3D musculoskeletal model. Motion data for different styles of walking (a high, crouched, bended and two types of sprawling motion) were fed into the 3D model to identify whether any joints adopted near‐optimal poses for leverage across each of the behaviours. We found that (1) the hip adductors and knee extensors had their largest leverages during sprawling postures and (2) more erect postures typically involved greater peak moment arms about the hip (flexion‐extension), knee (flexion) and metatarsophalangeal (flexion) joints. The results did not fully support the hypothesis that optimal poses are present during different locomotory behaviours because the peak capacities were not always reached around mid‐stance phase. Furthermore, we obtained few clear trends for isometric moment‐generating capacities. Therefore, perhaps peak muscular leverage in Nile crocodiles is instead reached either in early/late stance or possibly during swing phase or other locomotory behaviours that were not studied here, such as non‐terrestrial movement. Alternatively, our findings could reflect a trade‐off between having to execute different postures, meaning that hindlimb muscle leverage is not optimised for any singular posture or behaviour. Our model, however, provides a comprehensive set of 3D estimates of muscle actions in extant crocodiles which can form a basis for investigating muscle function in extinct archosaurs.
... We hypothesise that the space between the most posterior trunk ribs and the pelvis was occupied by an unusually large puboischiofemoralis internus 2 (PIFI2). In modern alligators, PIFI2 originates on the centra of the lumbar vertebrae (most posterior presacrals) as well as on the ventral surfaces of their transverse processes, and inserts on the anterodorsal aspect of the proximal femur (Reilly et al. 2005). In Eldeceeon, the origin of the PIFI2 fibres may have extended further forward along the posterior half of the vertebral column than in a modern alligator, such that a considerably greater number of presacrals may have provided sites for muscle attachment. ...
The late Viséan anthracosauroid Eldeceeon rolfei from the East Kirkton Limestone of Scotland is re-described. Information from two originally described and two newly identified specimens broadens our knowledge of this tetrapod. A detailed account of individual skull bones and a revision of key axial and appendicular features are provided, alongside the first complete reconstructions of the skull and lower jaw and a revised reconstruction of the postcranial skeleton. In comparison to Silvanerpeton , the only other anthracosauroid from East Kirkton, Eldeceeon is characterised by a proportionally wider semi-elliptical skull, comparatively smaller nostrils set farther apart, smaller and more rounded orbits, a shorter skull table with gently convex lateral margins, and a deeper suspensorium with a straight posterior margin and a small dorsal embayment. The remarkably large hind feet and elongate toes of Eldeceeon presumably represent an adaptation for attaining high locomotory speed through increased stride length and reduced stride frequency. This would necessitate great muscle force but few muscle contractions. At the beginning of a new stride cycle, repositioning the pes anteriorly and lifting the toes off the ground would require a strong and large muscle to pull the femur upward and rotate it inward and forward. It is hypothesised that such muscle might correspond to the puboischiofemoralis internus 2 , which would extend along the posterior half of the vertebral column, consistent with the occurrence of long, curved ribs in the anterior half of the trunk. Using maximum parsimony and Bayesian inference, cladistic analyses of all major groups of stem amniotes retrieve a sister group relationship between Eldeceeon and Silvanerpeton , either as the most plesiomorphic stem amniote clade or as a clade immediately crownward of anthracosauroids.