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. 2012 Mar;220(3):212-32.
doi: 10.1111/j.1469-7580.2011.01469.x. Epub 2012 Jan 3.

Computational modelling of locomotor muscle moment arms in the basal dinosaur Lesothosaurus diagnosticus: assessing convergence between birds and basal ornithischians

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Computational modelling of locomotor muscle moment arms in the basal dinosaur Lesothosaurus diagnosticus: assessing convergence between birds and basal ornithischians

Karl T Bates et al. J Anat. 2012 Mar.

Abstract

Ornithischia (the 'bird-hipped' dinosaurs) encompasses bipedal, facultative quadrupedal and quadrupedal taxa. Primitive ornithischians were small bipeds, but large body size and obligate quadrupedality evolved independently in all major ornithischian lineages. Numerous pelvic and hind limb features distinguish ornithischians from the majority of other non-avian dinosaurs. However, some of these features, notably a retroverted pubis and elongate iliac preacetabular process, appeared convergently in maniraptoran theropods, and were inherited by their avian descendants. During maniraptoran/avian evolution these pelvic modifications led to significant changes in the functions of associated muscles, involving alterations to the moment arms and the activation patterns of pelvic musculature. However, the functions of these features in ornithischians and their influence on locomotion have not been tested and remain poorly understood. Here, we provide quantitative tests of bipedal ornithischian muscle function using computational modelling to estimate 3D hind limb moment arms for the most complete basal ornithischian, Lesothosaurus diagnosticus. This approach enables sensitivity analyses to be carried out to explore the effects of uncertainties in muscle reconstructions of extinct taxa, and allows direct comparisons to be made with similarly constructed models of other bipedal dinosaurs. This analysis supports some previously proposed qualitative inferences of muscle function in basal ornithischians. However, more importantly, this work highlights ambiguities in the roles of certain muscles, notably those inserting close to the hip joint. Comparative analysis reveals that moment arm polarities and magnitudes in Lesothosaurus, basal tetanuran theropods and the extant ostrich are generally similar. However, several key differences are identified, most significantly in comparisons between the moment arms of muscles associated with convergent osteological features in ornithischians and birds. Craniad migration of the iliofemoralis group muscles in birds correlates with increased leverage and use of medial femoral rotation to counter stance phase adduction moments at the hip. In Lesothosaurus the iliofemoralis group maintains significantly higher moment arms for abduction, consistent with the hip abduction mode of lateral limb support hypothesized for basal dinosaurs. Sensitivity analysis highlights ambiguity in the role of musculature associated with the retroverted pubis (puboischiofemoralis externus group) in ornithischians. However, it seems likely that this musculature may have predominantly functioned similarly to homologous muscles in extant birds, activating during the swing phase to adduct the lower limb through lateral rotation of the femur. Overall the results suggest that locomotor muscle leverage in Lesothosaurus (and by inference basal ornithischians in general) was more similar to that of other non-avian dinosaurs than the ostrich, representing what was probably the basal dinosaur condition. This work thereby contradicts previous hypotheses of ornithischian-bird functional convergence.

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Figures

Fig. 1
Fig. 1
Dinosaurian relationships, showing major clades discussed in the text and the phylogenetic position of Lesothosaurus diagnosticus. Although Lesothosaurus has been recovered in a number of different positions in recent cladistic analyses (Sereno, 1999; Butler et al. 2008, 2010), this is to be expected from a taxon that displays few autapomorphies but shares numerous features with basal members of all ornithischian lineages, representing the ‘ancestral’ condition. We follow Sereno (1999) herein, in line with Maidment & Barrett (2011). a, avian pelvis in right lateral view; b, basal ornithischian pelvis in right lateral view; both after Maidment & Barrett (2011) and not to scale. 1, elongate preacetabular process of the ilium; 2, retroversion of the pubis; 3, habitual quadrupedal stance.
Fig. 2
Fig. 2
Myological reconstruction of the pelvis and hind limb of Lesothosaurus diagnosticus based on Maidment & Barrett (2011). (A,B) Pelvis in: (A) lateral; and (B) medial views. (C–F) Femur in: (C) cranial; (D) medial; (E) caudal; and (F) lateral views. (G) The 3D musculoskeletal model of Lesothosaurus in right lateral view. See Table 1 for muscle abbreviations. Scale bar equal to 0.05 m (a–f modified from Maidment & Barrett, 2011).
Fig. 3
Fig. 3
Sensitivity analysis for key muscles with poorly constrained origins, insertions and/or 3D paths in Lesothosaurus and other basal ornithischians. The sensitivity analysis investigated the differences between ‘ornithischian-biased’ and ‘theropod-biased’ reconstructions of the pelvic musculature of Lesothosaurus (see text). Specifically, relative to the original ‘ornithischian-biased’ model, the analysis tested the effect of a more proximal origin for (A) ADD1 and (B) ADD2, (C) a more proximal insertion for ISTR, (D) more lateral via points for ITBa and ITBp, (E) a more proximal origin for PIFE, and (F) a craniolateral insertion and also an origin from the dorsal vertebrae for PIFI2.
Fig. 4
Fig. 4
Hip muscle moment arm predictions for (a) AMB, (b) CFB, (c) CFL, (d) FTE, (e) FTI3, (f) IFB, (g) IFMa, (h) IFMp and (i) PIFI1 for a range of hip flexion/extension angles in Lesothosaurus. A positive hip joint angle (x-axis) indicates hip extension (femoral retraction), while a negative hip joint angle indicates hip flexion (femoral protraction), as shown by the small images of the pelvis of Lesothosaurus in the left lateral view along the x-axis of each graph. A negative moment arm (y-axis) for flexion/extension is a moment arm for flexion; a negative moment arm for abduction/adduction is a moment arm for abduction; a negative moment arm for long axis rotation is a moment arm for medial rotation. FlexExt, flexion/extension; ABDADD, abduction/adduction; LAR, long axis rotation.
Fig. 5
Fig. 5
Hip muscle moment arm predictions for (a) ADD1, (b) ADD2, (c) ISTR, (d) ITBa, (e) ITBp, (f) PIFE, (g) PIFI2, the muscles for which the sensitivity analysis was performed, for a range of hip flexion/extension angles in Lesothosaurus. A positive hip joint angle (x-axis) indicates hip extension (femoral retraction), while a negative hip joint angle indicates hip flexion (femoral protraction), as shown by the small images of the pelvis of Lesothosaurus in the left lateral view along the x-axis of each graph. A negative moment arm (y-axis) for flexion/extension is a moment arm for flexion; a negative moment arm for abduction/adduction is a moment arm for abduction; a negative moment arm for long axis rotation is a moment arm for medial rotation. FlexExt, flexion/extension; ABDADD, abduction/adduction; LAR, long axis rotation. SA indicates the results of the sensitivity analysis in a–f; CLI indicates the results using the alternative insertion for PIFI2; VO indicates the results using the alternative origin for PIFI2 in g (see text for details).
Fig. 6
Fig. 6
Sum of (a) hip extensor, (b) hip flexor, (c) adduction, (d) abduction, (e) lateral femoral rotation and (f) medial femoral rotation muscle moment arms normalized by segment length for Lesothosaurus and other dinosaurian bipeds (for further comparisons, see Fig. S1 in Supporting Information).
Fig. 7
Fig. 7
(a) CFB flexion–extension, (b) abduction–adduction and (c) long axis rotation moment arm predictions for Lesothosaurus and other dinosaurian bipeds over a range of hip joint flexion–extension angles. CFB is reconstructed as passing dorsolateral to the joint centre yielding a weak abduction moment arm in (d) Lesothosaurus, while in non-avian theropods like (e) Allosaurus and (f) ostrich it extends caudoventral to the hip joint centre producing a weak adduction moment arm. Green cylinder in d–f shows the abduction–adduction axis running through the hip joint centre. ABD-ADD, abduction/adduction; FL, femoral length; Flex-Ext, flexion/extension; LAR, long axis rotation; MA, moment arm.
Fig. 8
Fig. 8
Predicted Iliofemoralis group muscle moment arms for hip (a, d) flexion–extension, (b, e) abduction–adduction and (c, f) long axis rotation in Lesothosaurus and other dinosaurian bipeds over a range of hip joint flexion–extension angles. The cranial part of iliofemoralis approximately corresponds to the avian iliotrochantericus caudalis; the caudal part of iliofemoralis approximately corresponds with the avian iliofemoralis externus. Pelvis, femur and IFM in right lateral view in (g) Lesothosaurus, (h) Allosaurus and (i) Struthio (not to scale). IFMa is located much farther cranial to the joint centre in the ostrich (i), causing higher medial rotation moment arms. ABD-ADD; abduction/adduction; FL, femoral length; Flex-Ext, flexion/extension; LAR, long axis rotation; MA, moment arm.
Fig. 9
Fig. 9
Predicted pubioischiofemoralis externus group muscle moment arms for hip (a, d) flexion–extension, (b, e) abduction–adduction and (c, f) long axis rotation in Lesothosaurus and other dinosaurian bipeds over a range of hip joint flexion–extension angles. (a–c) PIFI1; (d–f) PIFI2. Pelvis, femur and PIFI in right lateral view in (g) Lesothosaurus, (h) Allosaurus and (i) Struthio (not to scale). PIFI is located cranial to the joint centre in Allosaurus, but caudal to it in Lesothosaurus and ostrich due to retroversion of the pubis. ABD-ADD, abduction/adduction; FL, femoral length; Flex-Ext, flexion/extension; LAR, long axis rotation; MA, moment arm.

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