A high-resolution growth series of Tyrannosaurus rex obtained from multiple lines of evidence
Figure 2 Ontogram of Tyrannosaurus rex showing growth stages, synontomorphies, individual variation, individual specimens, and chronological ages. Arrowhead points to the most mature spe- cimen and the direction of the entire ontogenetic axis; that is, the least mature specimen is at the lower left whereas the most mature specimen is at the upper right. Asterisk indicates the type specimen. Individual variation occurs as progressions until young adulthood, where reversals are first seen. The maximum amount of change occurs at growth stages 5 and 6, which corresponds to the transition from a long and low skull and jaws to a deep and stout skull frame; this event, marked by the concentration of an extreme number of changes, is evidence that the ontogeny of T. rex is metamorphic (sensu Rose & Reiss, 1993). Each circle represents a numbered growth stage; these numbers do not correspond to those seen in Fig. 12. The star at growth stage 7 marks the ~3,000 kg threshold that separates T. rex from its closest, but smaller, relatives. Color key: red, small juveniles; orange, large juveniles; yellow, subadults; green, young adults; blue, adults; violet, senescent adults. See text for definition of growth categories. Skulls are to scale; AMNH FARB 5027 is scaled to a premaxilla to quadrate length of 1.3 m. Full-size DOI: 10.7717/peerj.9192/fig-2
Figure 1 Results of the cladistic analysis of 1,850 characters among 44 specimens of Tyrannosaurus rex. (A) Strict consensus of 50 MPTs showing the recovery of three primary growth stages separated by the specimen BMRP 2002.4.1. (B) The single ontogram recovered after the exclusion of wildcard specimens, reducing the number of OTUs to 31. Numbers to the left of the internodes are bootstrap and jackknife values, respectively; numbers to the right are Bremer decay indices. Asterisk indicates the type specimen. Ellipses enclose the regions of polytomies produced by the wildcard specimens, which are listed in the lower right hand corner of the corresponding ellipse. Note that the ellipses are limited to one side or the other relative to BMRP 2002.4.1, which corresponds to the topology of the strict consensus ontogram. Full-size DOI: 10.7717/peerj.9192/fig-1
Figure 3 Scatterplot showing the noncongruence in Tyrannosaurus rex between the completeness of specimens (i.e., number of characters scored) and the number of synontomorphies at each corresponding node. Per cent completeness (decreasing away from the origin) and the number of synontomorphies supporting the corresponding node (decreasing away from the origin) have been converted to ranks. A Spearman correlation test on these data results in a nonsignificant correlation coefficient; ergo, the number of synontomorphies at an internode is not an artifact of specimen completeness. Full-size DOI: 10.7717/peerj.9192/fig-3
Figure 4 Frequency distribution of unambiguously optimized synontomorphies during the growth of Tyrannosaurus rex. Growth stages (corresponding to the numbered nodes of the ontogram in Fig. 2) are along the x-axis and the number of changes are along the y-axis. The greatest number of changes are seen in the transition from large juvenile to subadult, or, from growth stage 5–6; the high concentration of change between these growth categories is evidence that T. rex ontogeny is metamorphic (sensu Rose & Reiss, 1993). Full-size DOI: 10.7717/peerj.9192/fig-4
Figure 5 Comparison of the frequency distributions of phylogenetic and nonphylogenetic synontomorphies in the ontogeny of Tyrannosaurus rex. Growth stage is along the x-axis (corresponding to the numbered nodes of the ontogram in Fig. 2) and number of synontomorphies is along the y-axis. Phylogenetic characters are in solid bars; nonphylogenetic characters are in hollow bars. The frequency distributions of both sets of data follow the same general pattern, aside from the flatter distribution of the phylogenetic synontomorphies relative to the nonphylogenetic synontomorphies and the reversed pattern seen at growth stages 7 and 8. Both types of changes occur throughout the lifespan of T. rex, indicating that ontogeny is not strictly congruent with phylogeny. Full-size DOI: 10.7717/peerj.9192/fig-5
Figure 6 Comparison of the frequency distributions of cranial and postcranial changes in the growth series of Tyrannosaurus rex. The growth stages are along the x-axis (corresponding to the numbered nodes of the ontogram in Fig. 2) and the y-axis corresponds to the number of synontomorphies. Cranial changes are shown in solid bars; postcranial chanages are shown in hollow bars. Cranial and postcranial changes tend to follow the same overall pattern although postcranial changes are exceeded by cranial changes, except at growth stages 7, 15, and 16. The relatively late occurrence of postcranial changes (at growth stage 6) is an artifact of the absence of postcranial material among the least mature specimens in the sample. Full-size DOI: 10.7717/peerj.9192/fig-6
Figure 7 Comparison of the frequency distribution of synontomorphies of the cranium with that of the mandibular ramus in the ontogeny of Tyrannosaurus rex. Growth stages are along the x-axis (corresponding to the numbered nodes of the ontogram in Fig. 2) and the y-axis corresponds to the number of synontomorphies. Skull changes are shown with solid bars; mandible changes are shown with hollow bars. Although a greater number of changes is seen in the cranium than in the mandibular ramus, the lower jaw completes its early phase of changes (stage 5) before the cranium (stage 6). Thereafter, the pattern of mandibular changes is generally congruent with the cranium. Full-size DOI: 10.7717/peerj.9192/fig-7
Figure 8 The frequency distribution of synontomorphies by cephalic pneumatic system in the growth series of Tyrannosaurus rex. Growth stages are along the x-axis (corresponding to the numbered nodes of the ontogram in Fig. 2) and the y-axis corresponds to the number of synontomorphies. Changes to the antorbital sinus system are dominant over others and are sustained though growth, in contrast to the other systems that occur in adulthood and are transient in occurrence. aosin, antorbital sinus system; pharyn, pharyngeal sinus system; subcon, subcondylar sinus system; tympcav, tympanic cavity. Full-size DOI: 10.7717/peerj.9192/fig-8
Figure 9 The frequency distribution of synontomorphies by apneumatic anatomical domain in the growth series of Tyrannosaurus rex. Growth stages are along the x-axis (corresponding to the numbered nodes of the ontogram in Fig. 2) and the y-axis corresponds to the number of synontomorphies. Changes to the skull frame are dominant over others and all are sustained throughout growth, aside from the dentition and cervical occiput. crv occ, cervical occiput; dntn, dentition; dtfo, dorsotemporal fossa; jnt srfc, joint surfaces; mscl scrs, muscle scars; nrvsc, neurovasculature; sbct srfc, subcutaneous surface; skl frm, skull frame. Full-size DOI: 10.7717/peerj.9192/fig-9
Figure 10 The frequency distribution of postcranial synontomorphies in the growth series of Tyrannosaurus rex. Growth stages are along the x-axis (corresponding to the numbered nodes of the ontogram in Fig. 2) and the y-axis corresponds to the number of synontomorphies. Changes to the appendicular skeleton dominate in the transition between juvenile and subadult, whereas changes to the pelvic girdle and axial skeleton occur late in adulthood. Full-size DOI: 10.7717/peerj.9192/fig-10
Figure 11 The frequency distribution of changes to the craniomandibular functional modules (sensu Werneburg et al., 2019) in the growth series of Tyrannosaurus rex. Growth stages are along the x-axis (corresponding to the numbered nodes of the ontogram in Fig. 2) and the y-axis corresponds to the number of synontomorphies. The onset of the changes to the skull roof, snout, mandibular ramus, and suspensorium modules occur early in growth, whereas the onset of changes to the parietal and braincase occur in adulthood. Changes continue throughout growth in all domains, aside from those to the parietal that cease at growth stage 14. Full-size DOI: 10.7717/peerj.9192/fig-11
Figure 13 Scatterplot showing the congruence in Tyrannosaurus rex between bite force (i.e., and maturity). Growth stage rank, corresponding to the increasing sequence of nodes in Fig. 2, is along the x-axis; growth stage rank refers to the relative maturity of the specimens for which bite force has been estimated. Increasing bite force rank is along the y-axis; raw bite force data are from Bates & Falkingham (2012) and Gignac & Erickson (2017). A Spearman correlation test on these data resulted in a significant correlation coefficient, indicating that bite force increases with maturity. Full-size DOI: 10.7717/peerj.9192/fig-13
Figure 14 Bivariate scatterplot showing the relationship between maxillary tooth count with maturity among 14 specimens of Tyrannosaurus rex. Growth rank increases away from the origin (i.e., maturity increases to the right) and corresponds to growth stages for which maxillary tooth count was available for a given specimen; that is, the rank does not correspond to growth stage. Maxillary tooth rank corresponds to relative tooth count, where low ranks correspond to high tooth counts and low ranks correspond to high tooth counts. Full-size DOI: 10.7717/peerj.9192/fig-14
Figure 15 Bivariate scatterplot showing the relationship between dentary tooth count with maturity among 16 specimens of Tyrannosaurus rex. Growth rank increases away from the origin (i.e., maturity increases to the right) and corresponds to growth stages for which dentary tooth count was available for a given specimen; that is, the rank does not correspond to growth stage. Dentary tooth rank corresponds to relative tooth count, where low ranks correspond to high tooth counts and low ranks correspond to high tooth counts. Full-size DOI: 10.7717/peerj.9192/fig-15
Figure 16 Bivariate scatterplot showing the relationship between chronological age with maturity among eight specimens of Tyrannosaurus rex. The comparison is limited to specimens that have been histologically aged; growth stages (x-axis) and chronological age (y-axis) have been converted to ranks. See Table 14 for the raw data. Full-size DOI: 10.7717/peerj.9192/fig-16
Figure 17 Bivariate scatterplots showing the relationship between size with maturity among 15 specimens of Tyrannosaurus rex. The comparison is limited to specimens that have comparable size data; growth stages (x-axis) and size (y-axis) have been converted to ranks. See Table 15 for the raw data. Full-size DOI: 10.7717/peerj.9192/fig-17
Figure 18 Bivariate scatterplots showing the relationship between mass with maturity among nine specimens of Tyrannosaurus rex. The comparison is limited to specimens that have published mass estimates; growth stages (x-axis) and mass (y-axis) have been converted to ranks. See Table 16 for the raw data. Full-size DOI: 10.7717/peerj.9192/fig-18
Figure 19 Bivariate scatterplot showing the relationship between geographic location with maturity among 28 specimens Tyrannosaurus rex. Growth stages (x-axis) and geographic location (y-axis) have been converted to ranks. See Table 17 for the ranked data. “Montana North” refers to the region of Dawson, Garfield, and McCone counties, and “Montana South” refers to the region of Yellowstone and Carter counties. Maturity increases to the right along the x-axis; the y-axis follows the north-south axis of North America. Full-size DOI: 10.7717/peerj.9192/fig-19
Figure 20 Bivariate scatterplot showing the relationship between stratigraphic position with maturity among nine specimens of Tyrannosaurus rex. Growth stages (x-axis) and stratigraphic position (y-axis) have been converted to ranks. See Table 18 for the raw and ranked data. Maturity rank increases to the right; stratigraphic rank decreases from the origin (i.e., the upper HCF is closest to the origin, whereas the lower HCF is furthest from the origin). Full-size DOI: 10.7717/peerj.9192/fig-20
Figure 21 Sex dimorphs and the taxon “Tyrannosaurus “x”” of Larson (2008) mapped onto the ontogram of Tyrannosaurus rex. A transitional pattern is not seen between gracile and robust morphs; if sexual dimorphism was present, then the “gracile” and “robust” morphs should group along separate branches, which is not seen. Also, specimens referred to the taxon “T. “x”” do not form a clade, indicating that it is not a valid taxon. The pattern seen here is what is expected for a species without sexual dimorphism. Specimens considered in Larson (2008) as gracile are in boldface italics with a boldface “G”; specimens considered in Larson (2008) as robust are in boldface with a boldface “R”; specimens considered in Larson (2008) as referable to “T. “x”” are in italics and marked with an “X”. Full-size DOI: 10.7717/peerj.9192/fig-21
Figure 22 Sex dimorphs of Larson (2008) mapped onto the growth curve of Tyrannosaurus rex. A transitional pattern is not seen between gracile and robust morphs; if sexual dimorphism was pre- sent, then the “gracile” and “robust” morphs should grade into each other, which is not seen. Likewise, an ontogenetic progression among the cranial and postcranial indices is not seen. See text for details. Key to specimens numbered on the growth curve is in Fig. 12. Full-size DOI: 10.7717/peerj.9192/fig-22
Figure 23 The results of Henderson (2002) mapped onto the growth curve of Tyrannosaurus rex. All measures of the correlates of orbital fenestra size and shape change from juvenile to adult categories. It is predicted here that this transition occurred early in ontogeny, at the subadult growth stage, given the presence of correlates of a tall skull in subadult specimens. Key to specimens numbered on the growth curve is in Fig. 12. Full-size DOI: 10.7717/peerj.9192/fig-23
Figure 24 Skull bending strength mapped onto the growth curve of Tyrannosaurus rex. The results of Snively, Henderson & Phillips (2006) showing that the subadult growth stage was an important functional transition point during ontogeny between the long and low skulls of adults and tall and sturdy skulls of more mature animals. Their results show a progression in strength of the skull frame and dentition throughout the adult categories. Key to specimens numbered on the growth curve is in Fig. 12. Full-size DOI: 10.7717/peerj.9192/fig-24
Figure 25 The results of Therrien, Henderson & Ruff (2005) compared with the growth curve of Tyrannosaurus rex. Vertical bending strength and relative bending strength (sensu Therrien, Henderson & Ruff, 2005) mapped onto the growth curve of T. rex. Values for juveniles are missing for mid-dentary dorsoventral strength and mid-dentary relative strength. In general, strength increases ontogenetically, a trend that becomes obscured in adulthood. Key to specimens numbered on the growth curve is in Fig. 12. Full-size DOI: 10.7717/peerj.9192/fig-25
Figure 26 Heat maps of the ontogenetic changes seen in the skull and mandible of Tyrannosaurus rex. Illustrations show per centage of the total number of unambiguously optimized synontomorphies per bone (A) and functional module (B). Darker shades of gray indicate higher proportions of growth change, whereas lighter shades indicate lower proportions of change. The results show that the greatest amount of growth changes are at the lacrimal (A) or along the dorsal skull roof (B). Hatchure indicates empty space; stipple indicates unprepared matrix. Full-size DOI: 10.7717/peerj.9192/fig-26
Figure 27 Comparison of the results of Henderson & Snively (2004) with the growth curve of Tyrannosaurus rex. The rotational inertia (RI) of smaller and progressively distant sister taxa of T. rex serve as predictive proxies for the RIs of young adult and juvenile T. rex. Given the larger size of T. rex in contrast to non-tyrannosaurine tyrannosaurids, the RI of young adult T. rex will almost certainly be more comparable to that of adult D. torosus than to adult A. libratus. The positions of the taxa, aside from T. rex (FMNH PR2081), are relative and are not intended to correspond to exact locations along the growth curve. Key to specimens numbered on the growth curve is in Fig. 12. Full-size DOI: 10.7717/peerj.9192/fig-27
Figure 28 Comparison of the results of Snively et al. (2019) with the growth curve of Tyrannosaurus rex. A comparison of the agility values between T. rex and other tyrannosaurids. The values for T. bataar and D.torosus serve as predictive proxies for the corresponding values in subadult and young adult T. rex. The values for T. rex are calibrated to the growth series, but those of the other taxa are positioned relative to the values seen in T. rex. Inset of the data in table form shows the trends in the data; low values for Albertosaurus libratus are in boldface italics. Key to specimens numbered on the growth curve is in Fig. 12. Al, Albertosaurus libratus; Dt, Daspletosaurus torosus; Tb, Tyrannosaurus bataar; Tr, Tyr- annosaurus rex. Full-size DOI: 10.7717/peerj.9192/fig-28
Figure 29 Reptile Encephalization Quotients (REQs) of Hurlburt, Ridgley & Witmer (2013) mapped onto the growth curve of Tyrannosaurus rex. The REQ is based on a brain mass to endocranial volume ratio of 37% and the parenthetical values following the REQs corresponds to the two different body mass estimates, in metric tonnes, from which the REQs were derived (see Hurlburt, Ridgley & Witmer, 2013 for details). Overall, the REQ of the juvenile greatly exceeds that of adults, and the adults show an increasing ontogenetic progression of REQ values, as first reported by Hurlburt, Ridgley & Witmer (2013). Key to specimens numbered on the growth curve is in Fig. 12. Full-size DOI: 10.7717/peerj.9192/fig-29
Figure 30 Comparison of recapitulatory synontomorphies of Tyrannosaurus rex with tyrannosauroid phylogeny. Ten unambiguously optimized synontomorphies are congruent with unambiguously optimized synapomorphies of tyrannosauroid phylogeny, providing limited evidence of recapitulation (see text for details). Numbers to the right correspond to the growth stages in Fig. 2. If recapitulation was present, then the growth stage numbers should increase with progressively exclusive clades; that pattern is not seen here. Full-size DOI: 10.7717/peerj.9192/fig-30
Figure 31 Bivariate scatterplot showing the test of ontogenetic recapitulation of phylogenetic novelties in Tyrannosaurus rex. Growth stage rank (increases away from the origin) is along the x-axis; clade rank (increases away from the origin) is along the y-axis. If recapitulation is present, then the ranks will increase montonically from the origin. A recapitulatory pattern is not seen in T. rex; see text for details. Full-size DOI: 10.7717/peerj.9192/fig-31
Figure 32 Bivariate scatterplot showing the congruence between individual variation per specimen per node compared with the number of unambiguously optimized synontomorphies per node in Tyrannosaurus rex. The number of synontomorphies per node are along the x-axis; the amount of individual variation (i.e., unambiguously optimized character states per branch) is along the y-axis. Both values increase away from the origin. If the amount of individual variation is controlled by the number of synontomorphies per node, then the variables should increase monotonically. In this case, no congruence is seen between the variables in T. rex. Full-size DOI: 10.7717/peerj.9192/fig-32
Figure 33 A simplified cladogram of living and extinct Archosauriformes showing 13 cranial and postcranial growth changes that are optimized as synapomorphies. Most of the growth changes are ancestral for Archosauriformes. The position of several characters at progressively exclusive clades is almost certainly an artifact of missing data (e.g., increase in mandible height, enlargement of muscle attachments, etc.) and they are predicted to be synapomorphic for Archosauriformes once the appropriate data are acquired. This comparison shows that highly derived species such as Tyrannosaurus rex do not deviate from the ancestral growth trends that first evolved in significantly smaller taxa. See text for sources; see Table 23 for the distribution of character states among the taxa. Full-size DOI: 10.7717/peerj.9192/fig-33