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. 2021 Mar 4:9:e10855.
doi: 10.7717/peerj.10855. eCollection 2021.

Maniraptoran pelvic musculature highlights evolutionary patterns in theropod locomotion on the line to birds

Matthew M Rhodes  1 , Donald M Henderson  2 , Philip J Currie  1
Affiliations

Maniraptoran pelvic musculature highlights evolutionary patterns in theropod locomotion on the line to birds

Matthew M Rhodes et al. PeerJ. .

Abstract

Locomotion is a fundamental aspect of palaeobiology and often investigated by comparing osteological structures and proportions. Previous studies document a stepwise accumulation of avian-like features in theropod dinosaurs that accelerates in the clade Maniraptora. However, the soft tissues that influenced the skeleton offer another perspective on locomotory adaptations. Examination of the pelvis for osteological correlates of hind limb and tail musculature allowed reconstruction of primary locomotory muscles across theropods and their closest extant relatives. Additionally, the areas of pelvic muscle origins were quantified to measure relative differences within and between taxa, to compare morphological features associated with cursoriality, and offer insight into the evolution of locomotor modules. Locomotory inferences based on myology often corroborate those based on osteology, although they occasionally conflict and indicate greater complexity than previously appreciated. Maniraptoran pelvic musculature underscores previous studies noting the multifaceted nature of cursoriality and suggests that a more punctuated step in caudal decoupling occurred at or near the base of Maniraptora.

Keywords: Cursoriality; Functional morphology; Locomotion; Maniraptora; Morphology; Myology; Theropod.

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Conflict of interest statement

The authors declare there are no competing interests.

Figures

Figure 1
Figure 1. Simplified phylogeny of non-avian maniraptorans among other theropods and extant relatives.
Taxa along top indicate what each reconstruction represents, and asterisks (*) indicate novel pelvic muscle reconstructions. See Methods for details on phylogenetic treatment of study taxa. Phylogeny based on Hendrickx, Hartman & Mateus (2015).
Figure 2
Figure 2. Osteological correlates of pelvic musculature in Falcarius.
Pelvis in left lateral view (A) with ilium CEUM 77189, pubis UMNH VP 14540 (reversed; courtesy of Natural History Museum of Utah), and ischium CEUM 74717 (reversed). Ilium CEUM 77189 in ventral view (B) and oblique view of cuppedicus fossa (C). Pelvis in medial view (D) with the same specimens as in lateral view. Anterolateral view of proximal end of pubis CEUM 52424 (E). Close-up of obturator process (F) of ischium CEUM 52482 (reversed; proximal to top). Pubis UMNH VP 14540 in anterior (G) and posterior (H) views with close-up of the apron (I). Abbreviations: ace, acetabulum; bf, brevis fossa; cf, cuppedicus fossa; dist, distal ischial tubercle; isa, ischial apron; isp, ischiadic peduncle; op, obturator process; pa, pubic apron; pah, preacetabular hook; pb, pubic boot; pist, proximal ischial tubercle; pos, postacetabulum; pre, preacetabulum; pt, preacetabular tubercle; pup, pubic peduncle; rdg, ridge; str, striations.
Figure 3
Figure 3. Osteological correlates of pelvic musculature in Caenagnathidae indet.
Ilium UALVP 59791 in left lateral (A), ventral (B), and medial (C) views. Pelvis in left lateral view (D) with ilium TMP 1979.020.0001, pubis UALVP 56638, and ischium TMP 1979.020.0001 (reversed). Ilium TMP 1979.020.0001 in ventral view (E). Pelvis in medial view (F) with the same specimens as in lateral view except for pubis TMP 1980.016.2095. Close-up of obturator process (G) of ischium TMP 1979.020.0001. Pubes UALVP 56638 in anterior (H) and posterior (J) views. Refer to Fig. 2 for anatomical abbreviations.
Figure 4
Figure 4. Osteological correlates of pelvic musculature in Sinovenator (A–J) and Jianianhualong (K–L).
Ilia IVPP V12615 and IVPP V12583 in left lateral (A–B) and ventral (C–E) views (A, C, and E reversed). In the stippled line drawings, dashed lines indicate broken edges and grey represents matrix-obscured areas. Pubis IVPP V12583 in lateral (F, reversed), medial (G, reversed), anterior (H), and posterior (I) views. Pubes IVPP V12615 in posterior view (J). Pelvic region of Jianianhualong (K) with close-up of left ischium DLXH 1218 (L). Refer to Fig. 2 for anatomical abbreviations.
Figure 5
Figure 5. Osteological correlates of pelvic musculature in derived Troodontidae indet.
Pelvis in left lateral view (A) with ilium and pubis UALVP 55804 (reversed) and ischium AMNH 6516. Pelvis UALVP 55804 (reversed) in ventral view (B). Pelvis in medial view (C) with the same specimens as in lateral view. Ischium UMNH VP 19479 (reversed; courtesy of Natural History Museum of Utah) in dorsal (D) and lateral (E) views. Pubis UALVP 55804 in anterior view (F). Pubes UALVP 55804 in lateral (G, close-up in H), anterior (I), posterior (J, close-up in K), and medial (L, close-up in M) views. Refer to Fig. 2 for anatomical abbreviations.
Figure 6
Figure 6. Pelvic myology of non-avian maniraptorans.
Pelvis of Falcarius in left lateral view (A), ilium in ventral view (B), pelvis in medial view (C), and pubes in anterior (D) and posterior (E) views. Pelvis of Caenagnathidae indet. in left lateral view (F), ilium in ventral view (G), pelvis in medial view (H), and pubes in anterior (I) and posterior (J) views. Pelvis of Sinovenator in left lateral view (K), ilium in ventral view (L), pelvis in medial view (M), and pubes in anterior (N) and posterior (O) views. Pelvis of derived Troodontidae indet. in left lateral view (P), ilium in ventral view (Q), pelvis in medial view (R), and pubes in anterior (S) and posterior (T) views. See Table 2 for muscle abbreviations.
Figure 7
Figure 7. Pelvic myology of other study taxa.
Pelvis of Varanus in left lateral (A) and medial (B) views. Pelvis of Alligator in left lateral (C) and medial (D) views, and pubes in dorsal (E) and ventral (F) views. Pelvis of Caiman in left lateral (G) and medial (H) views, and pubes in dorsal (I) and ventral (J) views. Pelvis of Allosaurus in left lateral view (K), ilium in ventral view (L), pelvis in medial view (M), and pubes in anterior (N) and posterior (O) views. Pelvis of Albertosaurus in left lateral view (P), ilium in ventral view (Q), pelvis in medial view (R), and pubes in anterior (S) and posterior (T) views. Pelvis of Ornithomimidae indet. in left lateral view (U), ilium in ventral view (V), pelvis in medial view (W), and pubes in anterior (X) and posterior (Y) views. Pelvis of Saurornitholestes in left lateral view (Z), ilium in ventral view (AA), pelvis in medial view (BB), and pubes in anterior (CC) and posterior (DD) views. Pelvis of Struthio in left lateral (EE) and medial (FF) views. Pelvis of Dromaius in left lateral (GG) and medial (HH) views. Pelvis of Gallus in left lateral (II) and medial (JJ) views. See Table 2 for muscle abbreviations and refer to Supplemental Figures for individually labeled origins.
Figure 8
Figure 8. Area of attachment across all pelvic muscles and by conventional anatomical groups.
(A) Equal-area chart showing the proportion of individual muscles to the total area of all muscles. (B) Paired bar charts representing anatomical groups with results from Corel DRAW! (left bars) and ImageJ (right bars). See Table 2 for muscle abbreviations.
Figure 9
Figure 9. Area of attachment by functional groups.
(A) Antagonistic pairs of all taxa sampled. (B) Antagonistic pairs of taxa pruned to reflect general results of past studies. Abbreviations: Ab, abduction; Ad, adduction; E, extension; F, flexion; M, medial; L, lateral; LAR, long axis rotation.
Figure 10
Figure 10. Pelvic myology by functional groups.
Antagonistic pairs demonstrate general patterns in representatives of non-theropod Sauria (Alligator, A), non-maniraptoran Theropoda (Allosaurus, B), non-avian Maniraptora (Saurornitholestes, C), and Aves (Gallus, D). Abbreviations: Ab, abduction; Ad, adduction; E, extension; F, flexion; M, medial; L, lateral; LAR, long axis rotation.
Figure 11
Figure 11. Sensitivity analysis.
Comparison of Corel DRAW! and ImageJ under five tolerance levels performed on the Albertosaurus reconstruction (inset) shows no significant differences. Scatter plot (left) depicts individual muscle origin measurements, summarized in the box and whisker plot (right; coloured bars = interquartile range, black line = mean). See Table 2 for muscle abbreviations.
Figure 12
Figure 12. Phylogenetic Generalized Least Squares (PGLS) regressions on area of attachment and ilium length normalized to body mass (all log-transformed).
(A) Individual regressions on each major group with colour-coded regression lines (dashed). (B) Regressions on non-avian theropods. (C) Regressions on bipedal taxa. Bivariate comparisons are grouped by rows according to the dependent variable: area of attachment of all hip muscles, area of attachment of major extensors, and length of the ilium.
Figure 13
Figure 13. Area of attachment of major extensors.
Muscles and groups plotted as a proportion of the total area of all pelvic muscle origins, and grey lines represent 5% increments. Cursoriality categories adapted from Carrano (1999). Classes based on Jenks Natural Break optimization of the major extensors for five groups. See Table 2 for muscle abbreviations.
Figure 14
Figure 14. Pelvic musculature and other putative correlates of cursoriality.
(A) Pelvic muscle reconstructions in left lateral view grouped to show non-avian maniraptorans among other theropods and extant relatives. (B) Heat map comparing the area of attachment of major extensors (from Jenks Natural Breaks optimization in Fig. 13), proportional length of distal hind limb elements (sensu Carrano, 1999), ankle joint morphology/degree of metatarsal fusion (hinge-like > ball-and-socket; tarsometatarsus > arctometatarsus > subarctometatarsus > unspecialized), number of functional weight-bearing digits (fewer = higher), and foot symmetry. (C) Bar chart depicting a spectrum of inferred cursoriality averaged from the heat map above.
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Grants and funding

This work was supported by the Dinosaur Research Institute (MMR); Government of Alberta (MMR); Natural Sciences and Engineering Research Council of Canada (NSERC) Canada Graduate Scholarship (MMR) and Discovery Grant (PJC, No. RGPIN-2017-04715); University of Alberta Department of Biological Sciences (MMR); and University of Alberta Graduate Students’ Association (MMR). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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