Research Article

Evolutionary Biology

A new Heterodontosaurus specimen elucidates the unique ventilatory macroevolution of ornithischian dinosaurs

Evolutionary Studies Institute, University of the Witwatersrand, South Africa
Department of Earth and Environmental Sciences, University of Minnesota, United States
European Synchrotron Radiation Facility, France
Natural History Museum, Imaging and Analysis Centre, United Kingdom
Department of Cell Biology & Anatomy, School of Medicine, Louisiana State University Health Sciences Center, United States
School of Geography, Earth and Environmental Sciences, University of Birmingham, United Kingdom
Department of Geological Sciences, University of Cape Town, South Africa
Department of Biological Sciences, University of Alberta, Canada
Department of Earth Sciences, Albany Museum, South Africa
Division of Paleontology, American Museum of Natural History, United States

Jul 6, 2021

https://doi.org/10.7554/eLife.66036

Open access
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Figures
Tables
Additional files

14 figures, 2 tables and 6 additional files

Figures

Figure 1

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Overview of study specimen with emphasis on preserved gastralia.

(A) Specimen AM 4766 *Heterodontosaurus tucki* on left, with virtual anatomy reconstructed on the right. (B) Close-up of gastralia. (C) Stereopairs of anterior half of gastralial series. g: gastralia; f: femur (left); t: tibia (left); p: pubis; sr: sternal ribs. Arrows on figure labels point anteriorly.

Figure 2

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Sternal plates of *H. tucki*.

(A) Location of sternal plates in AM 4766, (B) segmented left sternal plate of AM 4766, and (C) sternal plates in SAM-PK-K1332. (D) Line drawing of sternal plates in SAM-PK-K1336. (E) Composite line drawing of *H. tucki* sternal plate anatomy informed by both specimens. ampr: anteromedial process; cpr: costal process; fen: fenestra; sp: sternal plate. Arrows on figure labels point anteriorly.

Figure 3

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Stereopairs of segmented sternal ribs preserved in AM 4766.

(A) Right lateral view and (B) left lateral view. st: sternal plate (left); L/R 1/2/3: left/right first, second, and third sternal ribs (anterior to posterior). Arrows on figure labels point anteriorly.

Figure 4

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Comparative details of sternal ribs in other ornithodirans.

(A) Stereopairs of AM 4766 in (left) dorsal and (right) anteroventrolateral views. (**B, C**) Idealized version of sternal ribs present in AM 4766. (**D, E**) Photo and line drawing of sternal complex in *Thescelosaurus neglectus* (NCSM 15728). (F) Schematic sternal complex of *Rhamphorhynchus*, modified from Claessens et al., 2009. (G) Schematic sternal complex of *Jeholornis*, modified from Zheng et al., 2020. Arrows and asterisks point to sternal and dorsal rib articulation points, respectively. dr: dorsal ribs; g: gastralia; L/R 1/2/3: left/right first, second, and third sternal ribs (anterior to posterior) of AM 4766; sr: sternal ribs; st: sternal plates. Arrows on figure labels point anteriorly.

Figure 5

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Accessory ossifications of pectoral girdle in *H. tucki*.

(**A, B**) Clavicles and suprascapula of AM 4766 (B is segmentation of μCT data); (C) suprascapula in SAM-PK-K1332. cl (L/R): left/right clavicle; h: humerus; sc: scapula; ss: suprascapula. Arrows on figure labels point anteriorly.

Figure 6

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Changing diapophyseal and parapophyseal relationships in AM 4766.

(A) Virtual reconstruction of cervicothoracic, thoracic, and sacral vertebrae of AM 4766; (B) Line drawing of (A) with diapophyses and parapophyses colour-coded in cyan and magenta respectively. Dashed lines indicate shifting position of parapophyses relative to the accompanying diapophyses. Arrows on figure labels point anteriorly.

Figure 7

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Phylogenetically corrected results of ornithischian pelvic element analysis.

Phylogenetically corrected generalized least squares residuals results of (A) evolution of the anterior pubic process, (B) pubic rod, and (C) ischial length. Closed circle, Genasauria; open triangle, Ornithopoda; closed triangle, Marginocephalia. Silhouettes represent (from left to right): *Heterodontosaurus*, Stegosauria, Parksosauridae, Neoceratopsia, and Hadrosauridae.

Figure 8

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Hypothesized stepwise evolution of the ornithischian pelvic bellows and accompanying skeletal modifications and myological innovations.

(A) Silesaurus (outgroup), (B) Heterodontosaurus, (C) Thescelosaurus, to (D) Corythosaurus. Lung size is an approximation; red and blue portions of the lung represent hypothetical reconstructions of non-compliant and compliant lung regions, respectively. APP: anterior pubic process; PPM: puboperitoneal muscle. Not to scale.

Appendix 1—figure 1

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Stratigraphic context and locality maps of the fossil specimens.

(A) Simplified geological map of the upper Karoo Supergroup in the central main Karoo Basin. Star marks the exact study locality in the Eastern Cape of South Africa. Map derived from Council for Geoscience (2008). (B) Simplified geological map of the study area west of the Siberia farmhouse. Fossil localities are <90 m apart in the streambed. Map derived from combining data of the Council for Geoscience (2008), Google Earth 2010, and own mapping. (C) Outcrop near the locality of AM 4765 (view from S), which is ~25 m below the contact of the upper Elliot and Clarens Formations. Inset shows the uneven basal contact of the Clarens Formation in the region (view from the NE; uEF: upper Elliot Formation). (D) Outcrop of upper Elliot Formation near the locality of AM 4766 (view from East), which is <90 m downstream from AM 4765.

Appendix 1—figure 2

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Sedimentological context of the fossil specimens in the upper Elliot Formation.

See legend for facies codes. (A) Outcrop view of the floodplain facies association. From base to top: clast-rich, massive, pedogenically altered (Cn, Rt) silty, very fine-grained sandstone bed (Sc); massive silty, very fine-grained sandstone bed (Sm) with erosive lower and gradational upper contacts; massive siltstone bed (Fm). (B) Close-up view of the erosive contact between facies Sc and Sm. (C) Horizontally laminated sandstone (Sh) overlain by clast-rich, massive silty, very fine-grained sandstone with rip-up clasts of laminated sandstone (Cs) and in situ pedogenic carbonate nodules (Cn). (D) Low-angle cross-bedded sandstone (Sl) under- and overlain by clast-rich, massive silty, very fine-grained sandstone. The upper Sc facies contains large, very angular rip-up clasts (see inset too) of ripple cross-laminated sandstone (Cs). (E) Outcrop view of the polygonal network of desiccation cracks (Dc) in facies Sc. Inset shows the close-up view of the calcretized desiccation cracks (Dc) and in situ pedogenic carbonate nodules (Cn). (F) Vertical root trace with mineral halo, clay lining, and pedogenic alteration in facies Sc. Preserved length of root (~15 cm) is marked by yellow arrows. (G) Network of invertebrate trace fossil (If), poorly sorted rip-up clasts (Cm), and in situ pedogenic carbonate nodules (Cn) in facies Sc. (H) Back-filled burrow cast of an invertebrate trace fossil (If) adjacent to a clay-lined root trace (Rt) in facies Sc. Note the poorly sorted rip-up clasts (Cm) and in situ pedogenic carbonate nodules (Cn). Inset shows the line drawing of the trace fossils.

Appendix 1—figure 3

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Possible gastralia in the *Tianyulong* holotype.

Inset shows close-up of tiny rod-like bones that bear some resemblance to the posteriorly diminished gastralia of AM 4766. g?: possible gastralia (fragments). Modified from Zheng et al., 2009.

Appendix 1—figure 4

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Matrix of correlations between measured variables for quantitative analysis of pelvic architecture.

Corr: correlation coefficient for relationship; logaleng: log APP length; logpubl: log pubic rod length; logischl: log ischial length; logfeml: log femoral length.

Appendix 1—figure 5

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Scatter plots and Q-Q plots of pubic measurements versus femoral length.

(**A–C**) Scatter plots of log femoral length versus log APP, log pubic rod, and log ischium length, respectively. (**D–F**) Q–Q plots of residuals for log APP, log pubic rod, and log ischium, respectively. Grey shading illustrates 95% confidence intervals.

Appendix 1—figure 6

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Phenograms of measured pelvic dimensions across Ornithischia.

(A) Anterior pubic process length, (B) length of pubic rod, and (C) length of the ischium.

Tables

Table 1

Akaike Information Criterion weights and likelihood ratio test (p) statistics for the evolutionary models analysed here (see Materials and methods).

Bold values indicate preferred explanatory model for each measured pelvic variable. Likelihood ratio tests are between the preferred model and the next most preferred model. BroMo: Brownian Motion; OU: Ornstein–Uhlenbeck.

	BroMo (%)	OU (%)	Early-burst (%)	Drift (%)	Stasis (%)	p =
APP length	0.00	0.00	99.99	0.00	0.00	1.33⁻⁰⁷
Pubis length	11.06	3.56	2.97	82.34	0.00	0.01
Ischium length	5.21	25.24	8.73	1.45	59.37	1.00

Appendix 1—table 1

List of taxa used in the study.

Asterisk (*) indicates measurements derived from mostly complete specimens scaled relative to each other in a shematic skeletal diagram

Taxon	Specimen no.	Source and notes
Heterodontosaurus tucki	AM 4766; SAM-PK-K1332	First-hand, Synchrotron X-ray µCT data
Eocursor parvus	SAM-PK-K8025	Butler et al., 2007
Scelidosaurus harrisonii	NHMUK R1111	Norman, 2020
Kentrosaurus aethiopicus	MFN mount	Mallison, 2010
Stegosaurus stenops	NHMUK PV R36730	Maidment et al., 2015
Agilisaurus louderbacki	ZDM 6011	Photographs
Hexinlusaurus multidens	ZDM T6001	Xl and Cai, 1984
Jeholosaurus shangyuanensis	IVPP 15719	Photographs, first-hand, **pubic rod length estimated relative to ischial length and phylogenetic position
Haya griva	IGM 100/2015	Photographs, Makovicky et al., 2011
Dryosaurus altus	YPM 1876	Marsh, 1878
Nanosaurus consors	BYU ESM-163R	Photographs
Thescelosaurus neglectus	NCSM 15728	Photographs, first-hand
Psittacosaurus neimongoliensis	IVPP 12-0888-2	Russell and Zhao, 1996
Centrosaurus apertus	AMNH 5351	Brown, 1917
Styracosaurus albertensis	AMNH 5372	Brown and Schlaikjer, 1937
Utahceratops gettyi*	UMNH VP specimens	Sampson et al., 2010,
Homalocephale calathocercos	GI-SPS 100/51	Maryanska and Pachycephalosauria, 1974
Tenontosaurus tilletti	AMNH 3040	Forster, 1990
Iguanodon bernissartensis	IRSNB 1534	Paul, 2008
Parasaurolophus cyrcocristatus	FMNH P27393	Ostrom, 1963
Lambeosaurus magnicristatus	TMP 66.04.01	Evans and Reisz, 2007
Corythosaurus casuarius	AMNH 5240	Brown, 1916
Brachylophosaurus canadensis	MOR 794	Prieto-Marquez, 2001
Edmontosaurus regalis	CMN 2289	Campione, 2015

Institutional abbreviations: AM: Albany Museum, Makanda, Eastern Cape, South Africa; AMNH: American Museum of Natural History, New York, United States; BYU: Brigham Young University Earth Science Museum; CMN: Canadian Museum of Nature, Ottawa, Ontario; FMNH: Field Museum of Natural History, Chicago, Illinois; GI-SPS: Geological Institute Section of Paleontology and Stratigraphy, Mongolian Academy of Sciences, Ulaanbataar, Mongolia; IGM: Institute of Paleontology and Geology, Mongolian Academy of Sciences, Ulaanbaatar, Mongolia; IRSNB: Institut Royal de Science Naturelle de Belgique, Brussels, Belgium; IVPP: Institute of Vertebrate Paleontology and Paleoanthropology, Beijing, China; MFN: Museum für Naturkunde, Berlin, Germany; MOR: Museum of the Rockies, Bozeman, Montana; NHMUK: Natural History Museum, London, England; NCSM: North Carolina Museum of Natural Sciences, Raleigh, North Carolina; SAM: Iziko South African Museum, Cape Town, South Africa; TMP: Royal Tyrrell Museum of Paleontology, Drumheller, Canada; UMNH: Utah Museum of Natural History, Salt Lake City, Utah; YPM: Yale Peabody Museum, New Haven, Connecticut; ZDM: Zigong Dinosaur Museum, Sichuan, China.