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Fig. S2. Variation in the nasal process of the premaxilla. ( A ) RTMP 2002.57.7, the holotype of Eotriceratops . ( B ) MOR 1120, collected from L3. ( C ) MOR 3011, collected from the lower part of M3. ( D ) MOR 3027, collected from upper M3. ( E ) MOR 3045, collected from upper M3. This specimen exhibits a pronounced peak on the nasal process (arrow) that is anterior to the posterior margin, a feature that is observed in juveniles from U3. ( F ) MOR 2574, collected from the lower U3. ( G ) MOR 2702, collected from the lower U3 (image mirrored for comparison). Specimens from U3 ( F and G ) exhibit a wider NPP; MOR 3045 represents the stratigraphically lowest occurrence of a wide NPP. MOR 2574 and MOR 2702 were collected from a multiindividual bone bed and exhibit variation in the morphology of the NPP. A trend toward an increased angle between the NPP and NS is noted in the HCF sample (Dataset S1). NPP, nasal process of the premaxilla. NS, narial strut. (Scale bars: 10 cm; B – G are to the same scale.)
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... taxon Titanoceratops ouranos . Longrich proposed that Titanoceratops represents the oldest member of the Triceratopsini, the clade that includes Triceratops , Torosaurus , “ Nedoceratops , ” and Ojoceratops (14). This specimen exhibits several features consistent with its stratigraphic position relative to HCF Triceratops . It has a relatively short epinasal, short arched nasals, a posteriorly inclined NPP, and elongate postorbital horn cores. Given the degree of ontogenetic transformation noted in several marginocephalians (1, 2, 16, 17), it is possible that many of the features considered to distinguish Titanoceratops from Pentaceratops (including large size, broad epiossifications, extensive cornual sinuses, strongly anteriorly curved postorbital horn cores, elongate premaxilla) (14) may instead represent ontogenetic or individual variation within the latter taxon (18), which would be consistent with the original diagnosis by Lehman (15). Further assessment of this specimen and its phylogenetic position is beyond the scope of the current study. Triceratopsin material from the southern region of the western interior of North America includes specimens that have been referred to Ojoceratops fowleri and Torosaurus utahensis (14, 19 – 23). Ojoceratops , from the Ojo Alamo Formation of New Mexico, appears to be closely related to Triceratops (3, 19, 24) and has been suggested to be synonymous with the latter taxon (14). Material referred to Ojoceratops thus far consists of isolated or fragmentary elements. Due to the missing morphological information for much of this material, specimens of O. fowleri were not included in the current cladistic analysis of HCF Triceratops . A nasal horn referred to this taxon [State Museum of Pennsylvania (SMP) specimen VP-1828] exhibits a morphology similar to that observed in several lower unit (L3)/lower M3 Triceratops , which is consistent with its stratigraphic position relative to the Hell Creek Formation of Montana. The holotype squamosal (SMP VP-1865) has a greatly reduced anterolateral projection of the squamosal, which has been used to distinguish it from Torosaurus utahensis . The degree to which this feature can distinguish Ojoceratops from other taxa is unclear; the HCF dataset demonstrates that the morphology of this projection varies within Torosaurus and Triceratops , and even within a single individual (MOR 2999). Variation in this feature has previously been noted by Hunt and Lehman (23). The incomplete or fragmentary nature of specimens that have been referred to Torosaurus utahensis has engendered debate regarding what material is referable to this taxon, its stratigraphic and biogeographic range, and which morphologic features, if any, distinguish it from other chasmosaurine taxa (22, 23). This material was not included in the current study of HCF specimens. Tatankaceratops sacrisonorum is represented by a fragmentary partial skull from the upper ( ∼ 20 m below the K/Pg boundary) HCF in South Dakota (25). The specimen exhibits an enlarged nasal horn and very small postorbital horn cores. As noted by Longrich (14), this specimen may represent T. prorsus , which would be consistent with its stratigraphic position. Triceratops Biogeography. Triceratops in the Frenchman Formation (Saskatchewan, Canada) and Laramie Formation (Colorado) appear to exhibit morphologies consistent with those expressed by specimens in the Hell Creek Formation (HCF), Montana. The base of the Frenchman Formation occupies the uppermost C30n magnetozone, with the majority of the unit residing in C29r up to the K-Pg boundary (26, 27), which indicates that the Frenchman Formation correlates largely to U3 of the HCF (28). Thus, we predict that most Triceratops skulls from the Frenchman Formation will exhibit T. prorsus morphologies. Diagnostic specimens pub- lished to date have been referred to T. prorsus (29). Conversely, the uppermost Laramie Formation exhibits reversed magnetic polarity, aligning it with magnetochron C30R (Castle Pines core) (30, 31) and making it slightly older than the HCF (28). Thus, specimens from the Laramie Formation should exhibit cranial morphologies similar to L3 Triceratops , and to date this hypothesis remains un- falsified (32). The Denver Formation is partly coeval with the HCF of Montana (33) and is predicted to yield a similar stratigraphically segregated Triceratops record. Thus far, specimens collected outside of Montana present morphologies that are consistent with their stratigraphic positions relative to the HCF sample. Increased stratigraphic resolution and sampling from the Lance Formation of Wyoming and other coeval formations will permit further testing of biogeographic hypotheses. The historical record remains unresolved and of limited utility. Stratigraphic Correlations of Specimens from Upper M3. MOR 3027, MOR 3045, and UCMP 113697 were all recovered from high in the middle unit of the HCF. The localities that produced MOR 3027 and MOR 3045 (Fig. S2) are within a mile of one another, which facilitates their relative stratigraphic placement. MOR 3027 was collected ∼ 5.5 m below the Apex Sandstone (the base of U3). MOR 3045 was collected from ∼ 7.5 m below this marker bed; thus, initially, it appeared that MOR 3045 was found stratigraphically lower than MOR 3027. However, the Apex Sandstone is thicker and cuts down further into the underlying strata just above the quarry that produced MOR 3027. There is a prominent organic-rich horizon that can be laterally traced above both quarries. MOR 3027 was found 5.3 m below this organic-rich bed whereas MOR 3045 was ∼ 3.3 m below. Thus, the quarry that produced MOR 3045 is higher stratigraphically relative to MOR 3027. UCMP 113697 was discovered 21.5 km to the east of these localities. Locally, the Apex Sandstone is ∼ 6 m above the base of the quarry that produced this specimen. An organic-rich horizon that may correlate with the organic-rich bed found above the two MOR localities is ∼ 3 m above the quarry, and thus UCMP 113697 appears to have been collected from roughly the same stratigraphic level as MOR 3045. Estimation of Basal-Skull Length. In this study, basal-skull length was considered the distance from the anteriormost point of the rostrum to the posterior surface of the occipital condyle (following previous researchers) (7, 12). Skull-length measurements for some specimens were taken from reconstructions (Dataset S1). For some largely complete specimens that do not preserve the occipital condyle or in which it is obscured (e.g., MOR 004), this distance was approximated by measuring the distance from the anteriormost point of the rostrum to the posterior margin of the lateral temporal fenestra (Dataset S1). For less complete, or disarticulated specimens, basal-skull length was estimated using linear regressions of basal-skull length against preserved cranial elements. Linear models relating basal-skull length to dentary length (measured from the anteriormost point to the posterior surface of the coronoid process), maxilla length (measured along the lateral surface), occipital condyle area (following ref. 34), and jugal length (measured from the base of the orbit to the distal tip) produced R 2 values of 0.995, 0.979, 0.944, and 0.980, respectively (Dataset S1). The use of multiple elements allowed more specimens to be included in quantitative comparisons. If multiple elements were preserved in a specimen (for example, MOR 2982 has a dentary and jugal), the estimated values for basal-skull length produced by the regression analyses were averaged. Cladistic Analysis. A cladistic analysis of cranial variation in HCF Triceratops initially used the heuristic search strategy of the program PAUP* 4.0b10 (35). Nexus files are available on MorphoBank (36) as project 1099. Analyses used the random addition sequence with tree-bisection-reconnection (TBR) branch swap- ping and 1,000 replicates; all most parsimonious trees were saved. Characters were unordered and unweighted. Maxtrees was set to 250,000. Analyses were initially performed using binary coding for morphological characters (37, 38). Additional analyses were performed using multistate coding that combined binary characters 10 and 11 (development of the epinasal-nasal protuberance), 25 and 26 (development of the anterolateral projection of the squamosal), and 29 and 30 (number of epiparietals). Support for clades was determined using nonparametric bootstrap resampling (39) in PAUP* 4.0b10; 10,000 bootstrap replicates were analyzed, with one tree retained per replicate. Application of bootstrap resampling to data in which multistate characters have been dis- tilled to binary characters is problematic (39) but was performed for comparative purposes. In addition, Bremer support indices were calculated using TreeRot.v3 (40) and PAUP* 4.0b10 (34). This analysis focused on features found to vary within the HCF Triceratops dataset. Eotriceratops was included in the analysis to test the hypothesis that it represents a taxon distinct from Triceratops . As such, characters found to distinguish Eotriceratops by Sampson et al. (24) and characters describing the relative height of the narial process and the morphology of the epijugal (41) were examined. Forster (12) noted five cranial characters that vary within Triceratops . Four of these characters were included in this analysis (Forster ’ s character 4, which describes rostrum shape, was modified in this analysis to reflect the influence of NPP orientation) (5). Forster ’ s character 1 (describing the postorbital, jugal, squamosal suture pattern) was not found to vary in the HCF dataset. Either all coded specimens exhibited the “ primitive ” state of the jugal contributing to the dorsal margin of the lateral temporal fenestra, or sutural relationships of this region were unpreserved or were obscured by fusion. Initially, specimens that were collected or stratigraphically relocated during the Hell Creek ...Context 2
... that development of the boss morphology was ontogenetic, as is seen in some centrosaurine ceratopsids (e.g., refs. 8 and 9.). The nasal boss morphology is not exhibited in all Torosaurus specimens [MOR 3081, MPM VP 6841, Yale Peabody Museum (YPM) 1830, and YPM 1831], and thus the degree to which this feature is developed may vary individually or stratigraphically. University of California Museum of Paleontology (UCMP) 128561 exhibits a low nasal boss (10, 11); however, due to the fragmentary nature of the specimen, it is unclear whether it represents the Torosaurus morphology. Morphology of the Rostrum. Forster (12) recognized rostrum morphology as one of the features that distinguish Triceratops horridus from Triceratops prorsus . T. horridus exhibits a low, elongate rostrum with a sinusoidal dorsal margin whereas, in T. prorsus , the rostrum is shorter and more convex. Longrich and Field (5) noted that specimens of T. prorsus have a more vertically oriented nasal process [ = ascending nasal process of the premaxilla (sensu ref. 13)], here referred to as the nasal process of the premaxilla (NPP)] compared with T. horridus . Rostrum morphology appears to be tied to the orientation of the NPP, with a more posteriorly inclined NPP contributing to a low, sinusoidal rostrum in some specimens [e.g., MOR 1120, American Museum of Natural History (AMNH) 5116, National Museum of Natural History (USNM) 1201, and YPM 1820]. The angle between the NPP and narial strut appears to increase stratigraphically in the HCF; specimens from the upper M3 and U3 exhibit a larger angle between the NPP and narial strut than specimens found lower in section (Fig. 2 C ). To quantify this shift in morphology, the angle between the NPP and narial strut (Fig. S2) was measured using the Ruler tool in Adobe Photoshop. This angle was measured between the approximate midlines of each process, parallel to the direction representing the primary trend (results presented in Dataset S1 and Fig. 2). We note that, in some more basal taxa (e.g., Anchiceratops ) (3), the NPP can be oriented nearly perpendicular to the narial strut and as such can give the rostrum a more convex appearance in lateral view. The width of the NPP also affects the rostrum morphology because a wider NPP reduces the apparent sinuosity of the anterior premaxilla. MOR 3027 and MOR 3045 (both recovered from upper M3) exhibit a more vertically inclined premaxillary articulation with the nasal than specimens found lower in the formation. MOR 3045 (collected ∼ 2 m above MOR 3027) exhibits the further derived feature of an anteroposteriorly expanded NPP, contributing to a rostrum that seems even more convex in lateral view. Rostrum length appears to vary both stratigraphically and ontogenetically. The largest specimens from U3 (e.g., MOR 004 and MOR 1625) exhibit more elongate rostra (Fig. 2 E and Dataset S1); however, even these large specimens do not exhibit the strongly posteriorly inclined NPP and sinusoidal dorsal margin of the rostrum exhibited in specimens referred to T. horridus . Evolutionary changes in rostrum morphology may reflect the development of an enlarged epinasal. Other Triceratopsin Taxa. Longrich (14) referred Oklahoma Museum of Natural History (OMNH) specimen 10165, a large ceratopsid specimen recovered from Campanian deposits of New Mexico and previously diagnosed as a gigantic specimen of Pentaceratops sternbergi (15), to the new taxon Titanoceratops ouranos . Longrich proposed that Titanoceratops represents the oldest member of the Triceratopsini, the clade that includes Triceratops , Torosaurus , “ Nedoceratops , ” and Ojoceratops (14). This specimen exhibits several features consistent with its stratigraphic position relative to HCF Triceratops . It has a relatively short epinasal, short arched nasals, a posteriorly inclined NPP, and elongate postorbital horn cores. Given the degree of ontogenetic transformation noted in several marginocephalians (1, 2, 16, 17), it is possible that many of the features considered to distinguish Titanoceratops from Pentaceratops (including large size, broad epiossifications, extensive cornual sinuses, strongly anteriorly curved postorbital horn cores, elongate premaxilla) (14) may instead represent ontogenetic or individual variation within the latter taxon (18), which would be consistent with the original diagnosis by Lehman (15). Further assessment of this specimen and its phylogenetic position is beyond the scope of the current study. Triceratopsin material from the southern region of the western interior of North America includes specimens that have been referred to Ojoceratops fowleri and Torosaurus utahensis (14, 19 – 23). Ojoceratops , from the Ojo Alamo Formation of New Mexico, appears to be closely related to Triceratops (3, 19, 24) and has been suggested to be synonymous with the latter taxon (14). Material referred to Ojoceratops thus far consists of isolated or fragmentary elements. Due to the missing morphological information for much of this material, specimens of O. fowleri were not included in the current cladistic analysis of HCF Triceratops . A nasal horn referred to this taxon [State Museum of Pennsylvania (SMP) specimen VP-1828] exhibits a morphology similar to that observed in several lower unit (L3)/lower M3 Triceratops , which is consistent with its stratigraphic position relative to the Hell Creek Formation of Montana. The holotype squamosal (SMP VP-1865) has a greatly reduced anterolateral projection of the squamosal, which has been used to distinguish it from Torosaurus utahensis . The degree to which this feature can distinguish Ojoceratops from other taxa is unclear; the HCF dataset demonstrates that the morphology of this projection varies within Torosaurus and Triceratops , and even within a single individual (MOR 2999). Variation in this feature has previously been noted by Hunt and Lehman (23). The incomplete or fragmentary nature of specimens that have been referred to Torosaurus utahensis has engendered debate regarding what material is referable to this taxon, its stratigraphic and biogeographic range, and which morphologic features, if any, distinguish it from other chasmosaurine taxa (22, 23). This material was not included in the current study of HCF specimens. Tatankaceratops sacrisonorum is represented by a fragmentary partial skull from the upper ( ∼ 20 m below the K/Pg boundary) HCF in South Dakota (25). The specimen exhibits an enlarged nasal horn and very small postorbital horn cores. As noted by Longrich (14), this specimen may represent T. prorsus , which would be consistent with its stratigraphic position. Triceratops Biogeography. Triceratops in the Frenchman Formation (Saskatchewan, ...Context 3
... S5 H ) (multistate coding: MPT 282; 52 steps; CI 0.7500; HI 0.3654; RI 0.8116) (Fig. 3 C ) recovered MOR 3045 as basal to U3 specimens and as more derived than UCMP 113697 and MOR 3027, which cluster together. Stratocladistic Analysis. Stratocladistics incorporates stratigraphic data into cladistic analyses (see, for example, refs. 43 – 48). A stratocladistic analysis was performed using the program StrataPhy, which produces trees that can indicate possible ancestor- descendant relationships (49). The multistate dataset was used for the analysis, with the specimens MOR 981, MOR 1604, and MOR 2978 removed from the analysis due to ambiguity over their precise stratigraphic position. Rather than coding specimens separately, specimens from the lower M3, upper M3, lower U3, and upper U3 were combined into operational units based on stratigraphic position. MOR 3081 and MOR 3005 were considered separately from other specimens from the same stratigraphic zones due to the distinct ontogenetic [(2) or, alternatively, taxonomic (4 – 6)] morphological differences between these specimens. MOR 3005 is a fragmentary specimen, but preserves thin sections of frill and thus may represent the Torosaurus morphology. A single stratigraphic character was added [stratigraphic position: (position 0) stratigraphically below the HCF; (position 1) lower L3; (position 2) upper L3; (position 3) lower M3; (position 4) upper M3; (position 5) lower U3; (position 6) upper U3]. Arrhinoceratops (ROM 796) was designated the outgroup. MAXTREES was set to 250,000, and all other pa- rameters were StrataPhy ’ s default settings (49). The initial analysis produced 61 trees with nine topologies (total debt = 64) (Fig. S6 A ). Aside from one tree that suggests all operational units arose via cladogenesis, specimens from the upper half of the formation were consistently found to represent an anagenetic succession. The position of operational units from the lower half of the formation varied and were not always consistent with stratigraphic position. This result is likely influenced by the fact that specimens from the lower half of M3 do not preserve features of the parietal-squamosal frill that would allow them to be distinguished from the Torosaurus morphology. MOR 2982 preserves an anterolateral projection of the squamosal, which is consistent with the morphology expressed in several other HCF specimens, including the Torosaurus specimen MOR 3081. Incorporation of Torosaurus specimens into Triceratops operational units (total debt = 67, nine trees, three topologies) (Fig. S6 B ) produced a single tree suggesting that all operational units arose via cladogenesis and two additional topologies that include ancestor-descendant relationships. In four trees, all operational units were recovered within an anagenetic lineage except the lower M3 group. This operational unit was recovered as basal to the upper L3 operational unit, suggesting a cladogenetic event. The remaining four trees exhibited a bifurcation event in L3 giving rise to two lineages. Given the lack of frill characters for the lower M3 operational unit, the influence of Torosaurus specimens on the results was examined by pruning all Torosaurus from the analysis. This pruning resulted in reduced total debt (57) and 12 trees (Fig. S6 C ). Four trees indicate that all HCF operational units represent a single anagenetic lineage with specimens exhibiting the T. horridus morphology evolving into T. prorsus (Fig. 4 A ). Eight trees recovered two lineages suggested to diverge at some point in L3 or before the deposition of the HCF. One lineage gave rise to lower M3 specimens and the other to U3 specimens. This result suggests that two anagenetic lineages, one comprising specimens referable to T. horridus and the other giving rise to T. prorsus , coexisted in the HCF (for at least some time) (Fig. 4 B ). Characters Incorporated in Cladistic Analysis. The first use in a cladistic study is cited. 1 ) Postorbital horn-core length: (code 0) long (postorbital horn-core/basal-skull length ratio: ≥ 0.64); (code 1) short (postorbital horn-core/basal-skull length ratio: < 0.64). [(50) character 58 modified; (12) character 2 modified]. 2 ) Cross-section of postorbital horn core: (code 0) circular to subcircular; (code 1) narrow. The postorbital horn cores of some specimens of Triceratops (e.g., MOR 2702 and MOR 2923) exhibit a markedly narrow morphology that does not appear to be a product of taphonomic distortion. MOR 2923 exhibits no evidence of lateral compression, and yet the postorbital horn cores of this specimen have a pronounced ventral keel. Specimens for which apparently laterally compressed postorbital horn cores are likely a result of taphonomic processes (e.g., MOR 2982 and MOR 3027) have been coded as “ ? ” . 3 ) Rostrum shape: (code 0) primary axis of nasal process of premaxilla (NPP) is strongly posteriorly inclined; (code 1) NPP vertical or nearly vertical [(12, 50) character 4 modified; (5) Fig. S2]. 4 ) Frontoparietal fontanelle: (code 0) open fontanelle; (code 1) closed or constricted due to fusion of frontals and parietals. [(50) characters 49 and 50 modified; (12) character 3 modified]. 5 ) Epijugal: (code 0) comes to a pronounced peak; (code 1) low and blunt [(51) character 102 modified; (24) character 50 modified). Epijugal morphology has been used in phylogenetic studies of chasmosaurines (e.g., refs. 14 and 24) and as a diagnostic feature of some taxa. In most specimens of Triceratops , the epijugal is a low, blunt element. Specimens exhibiting the Torosaurus morphology exhibit an epijugal that comes to a pronounced peak, similar to the condition noted in more basal taxa such as Eotriceratops (41). At least one large Triceratops with a nonfenestrated parietal (MOR 1625) also exhibits a peaked epijugal. 6 ) Quadratojugal notch: (code 0) present; (code 1) absent [sensu ref. 52, character 71; and (53) character 16]. The quadrates of Triceratops exhibit a pronounced ridge on the anterolateral surface. In many specimens, this ridge is interrupted ...Context 4
... pronounced notch; however, in some specimens, this notch is not present. ) Nasal-horn length: (code 0) short (length/width ratio < 1.85); (code 1) long (length/width ratio > 1.85). [(50) character 28 modified; (12) character 5 modified]. ) Dorsal surface of epinasal: (code 0) narrow to peaked; (code 1) broad. The posterior surface of the epinasal varies from being quite broad to nearly flat in some specimens, to being narrow and coming to a pronounced peak in others. The peaked condition is observed in the holotypes of Arrhinoceratops and Eotriceratops. ) Nasal: (code 0) short, arched; (code 1) elongate, straight. A short, arched nasal is observed in the holotype of T. horridus (YPM 1820) and several other specimens referred to this taxon. Specimens from U3 of the HCF exhibited a more elongate nasal morphology that lacks pronounced arching of the lateral margin. ) Anterior nasals and posterior portion of epinasal fused to form a protuberance posterior to epinasal: (code 0) present; (code 1) subtle or absent. Forster (12) noted a pronounced bump or boss posterior to the nasal horn in UCMP 113697. A similar structure is present in the holotype of Triceratops “ cal- icornis ” (USNM 4928) as noted by Ostrom and Wellnhofer (54). The structure appears to be formed by a combination of the anterior nasals and the posterior portion of the epinasal. Forster (12) suggested that this feature was due to the incomplete fusion of the epinasal to an underlying boss or horn core; disarticulated nasals reveal no underlying boss (13) but the anterior nasal can be somewhat thickened relative to the middle segment of this element. Presence of a homologous structure in mature individuals (MOR 1122) suggest that its presence is not a result of incomplete fusion although the degree to which this feature varies throughout ontogeny is currently unknown. Development of this feature may be tied to evolutionary elongation of the epinasal. ) Epinasal-nasal protuberance: (code 0) reduced or absent; (code 1) developed into pronounced boss. ) Anteromedial process on nasal: (code 0) present, pronounced; (code 1) reduced, constricted or absent (Fig. S3). Triceratops from the lower half of the HCF appear to exhibit a distinct process on the anteromedial surface of the nasal, medial to the rostroventral process (following the terminology of Fujiwara and Takakuwa) (55). In specimens from U3 in which this process is visible, it is greatly reduced. ) Posterior projection on epinasal: (code 0) present; (code 1) absent (Fig. S4). The posterior surface of some epinasals exhibits a small but pronounced posterior projection or shelf. The projection appears to be absent in observed specimens from U3. The projection may contribute to formation of the epinasal-nasal protuberance (see character 10). ) Nasal process of the premaxilla: (code 0) narrow; (code 1) expanded (Fig. S2). In some specimens of Triceratops , the NPP is narrow, exhibiting only slight anteroposterior expansion. The premaxilla of the holotype of Eotriceratops exhibits an extremely narrow NPP. In many specimens of Triceratops from relatively high in the HCF, this process is expanded into a wide, nearly square structure (Dataset S1). ) Midline peak on nasal process of the premaxilla: (code 0) absent; (code 1) present. The nasal process of MOR 3045 exhibits a pronounced dorsal peak anterior to its posterior margin (Fig. S2 E ). This process appears to be absent or greatly reduced in other specimens but is clearly present in juvenile specimens from U3 (MOR 1110 and MOR 2951). The degree to which this feature varies ontogenetically in specimens from the lower half of the formation is currently unknown. ) Prominence immediately anterior to or descending from the narial strut, directed into interpremaxillary fenestra: (code 0) absent; (code 1) present (Fig. S7 A ...Context 5
... pronounced notch; however, in some specimens, this notch is not present. ) Nasal-horn length: (code 0) short (length/width ratio < 1.85); (code 1) long (length/width ratio > 1.85). [(50) character 28 modified; (12) character 5 modified]. ) Dorsal surface of epinasal: (code 0) narrow to peaked; (code 1) broad. The posterior surface of the epinasal varies from being quite broad to nearly flat in some specimens, to being narrow and coming to a pronounced peak in others. The peaked condition is observed in the holotypes of Arrhinoceratops and Eotriceratops. ) Nasal: (code 0) short, arched; (code 1) elongate, straight. A short, arched nasal is observed in the holotype of T. horridus (YPM 1820) and several other specimens referred to this taxon. Specimens from U3 of the HCF exhibited a more elongate nasal morphology that lacks pronounced arching of the lateral margin. ) Anterior nasals and posterior portion of epinasal fused to form a protuberance posterior to epinasal: (code 0) present; (code 1) subtle or absent. Forster (12) noted a pronounced bump or boss posterior to the nasal horn in UCMP 113697. A similar structure is present in the holotype of Triceratops “ cal- icornis ” (USNM 4928) as noted by Ostrom and Wellnhofer (54). The structure appears to be formed by a combination of the anterior nasals and the posterior portion of the epinasal. Forster (12) suggested that this feature was due to the incomplete fusion of the epinasal to an underlying boss or horn core; disarticulated nasals reveal no underlying boss (13) but the anterior nasal can be somewhat thickened relative to the middle segment of this element. Presence of a homologous structure in mature individuals (MOR 1122) suggest that its presence is not a result of incomplete fusion although the degree to which this feature varies throughout ontogeny is currently unknown. Development of this feature may be tied to evolutionary elongation of the epinasal. ) Epinasal-nasal protuberance: (code 0) reduced or absent; (code 1) developed into pronounced boss. ) Anteromedial process on nasal: (code 0) present, pronounced; (code 1) reduced, constricted or absent (Fig. S3). Triceratops from the lower half of the HCF appear to exhibit a distinct process on the anteromedial surface of the nasal, medial to the rostroventral process (following the terminology of Fujiwara and Takakuwa) (55). In specimens from U3 in which this process is visible, it is greatly reduced. ) Posterior projection on epinasal: (code 0) present; (code 1) absent (Fig. S4). The posterior surface of some epinasals exhibits a small but pronounced posterior projection or shelf. The projection appears to be absent in observed specimens from U3. The projection may contribute to formation of the epinasal-nasal protuberance (see character 10). ) Nasal process of the premaxilla: (code 0) narrow; (code 1) expanded (Fig. S2). In some specimens of Triceratops , the NPP is narrow, exhibiting only slight anteroposterior expansion. The premaxilla of the holotype of Eotriceratops exhibits an extremely narrow NPP. In many specimens of Triceratops from relatively high in the HCF, this process is expanded into a wide, nearly square structure (Dataset S1). ) Midline peak on nasal process of the premaxilla: (code 0) absent; (code 1) present. The nasal process of MOR 3045 exhibits a pronounced dorsal peak anterior to its posterior margin (Fig. S2 E ). This process appears to be absent or greatly reduced in other specimens but is clearly present in juvenile specimens from U3 (MOR 1110 and MOR 2951). The degree to which this feature varies ontogenetically in specimens from the lower half of the formation is currently unknown. ) Prominence immediately anterior to or descending from the narial strut, directed into interpremaxillary fenestra: (code 0) absent; (code 1) present (Fig. S7 A ...Context 6
... Hell Creek Project (1999 – 2010), a multiinstitutional sur- vey of the fauna, flora, and geology of the Upper Cretaceous Hell Creek Formation (HCF), provides insights into the paleo- biology and evolution of the last nonavian dinosaurs (1). Triceratops (Ceratopsidae: Chasmosaurinae) is the most abundant dinosaur in the HCF; > 50 skulls, including previously unknown or rare growth stages, have been collected throughout the entire formation (spanning ∼ 1 – 2 million y) (2) over the course of the Hell Creek Project (1, 3 – 5). The combination of a stratigraphically controlled robust sample from the entire ∼ 90-m-thick HCF and identification of ontogenetic stages makes Triceratops a model organism for testing hypotheses proposed for the modes of dinosaur evolution (e.g., refs. 6 – 8). Since its initial discovery (9), as many as 16 species of Triceratops were named based on variations in cranial morphology (10, 11). Forster (12) recognized only two species, Triceratops horridus and Triceratops prorsus, based on cranial features including differences in relative length of the postorbital horn cores (long in T. horridus and shorter in T. prorsus ), morphology of the rostrum (elongate in T. horridus and shorter in T. prorsus ), and closure of the frontoparietal fontanelle (sensu Farke) (13) (open in T. horridus and closed in T. prorsus ). Marsh initially distinguished these two species by the morphology of the nasal horn (14); the type specimen of T. horridus possesses a short, blunt nasal horn whereas the nasal horn in T. prorsus is elongate. Whether or not these taxa were largely biogeographically separated or represented ontogenetic variants or sexual dimorphs within a single species has remained unresolved (8, 10, 12, 15 – 18). A record of the stratigraphic distribution of Triceratops from the Upper Cretaceous Lance Formation of Wyoming compiled by Lull (19, 20) suggested that these taxa overlap stratigraphically. However, this assessment was likely based on limited stratigraphic data (15) and “ the precise stratigraphic placement of these specimens can no longer be established ” (ref. 10, p. 155). As such, consideration of morphological variation in a detailed stratigraphic context is necessary to reassess systematic hypotheses. Stratigraphic placement of Triceratops specimens within the HCF reveals previously undocumented shifts in morphology. The HCF is divided into three stratigraphic units: the lower third (L3), middle third (M3), and upper third (U3) (1, 21). The stratigraphic separation of Triceratops morphospecies is apparent with specimens referable to T. prorsus (following Forster) (12) found in U3 and T. horridus recovered only lower in the HCF. Specimens from the upper part of M3 exhibit a combination of T. horridus and T. prorsus features (Fig. 1, SI Text , and Fig. S1). L3 Triceratops. Triceratops from the lowermost 15 – 30 m of the HCF (L3) possess either a small nasal horn (Fig. 2 A and Dataset S1) or a low nasal boss. The boss morphology appears in a large individual that histologically represents a mature specimen [ = “ Torosaurus ” ontogenetic morph (ref. 3; but see also refs. 22 – 24)] [Museum of the Rockies (MOR) specimen 1122] ( SI Text ). The nasal process of the premaxilla (NPP) in L3 Triceratops is narrow (Fig. 2 B and Fig. S2) and strongly posteriorly inclined; a pronounced anteromedial process is present on the nasal (Fig. S3). The frontoparietal fontanelle remains open until late in ontogeny (MOR 1122). Specimens from the lower unit of the HCF bear a range of postorbital horn-core lengths (ranging from ∼ 0.45 to at least 0.74 basal-skull length) (Fig. 2 D and Dataset S1). M3 Triceratops. The mean nasal-horn length increases through M3 (Figs. 1 E and F and 2 A ). The University of California Museum of Paleontology (UCMP) specimen 113697 (collected ∼ 6 m below the base of U3) possesses a nasal horn that is elongate (length/width: 2.12) (Dataset S1) but retains a broad posterior surface, giving the horn a subtriangular cross-section. Forster (12) noted that UCMP 113697 exhibits a small nasal boss posterior to the nasal horn. Disarticulated specimens (e.g., MOR 3027 and MOR 3045) reveal that this protuberance posterior to the epinasal appears to be formed by the combination of a posterior projection on the epinasal (Fig. S4) and the anteriormost nasal. A homologous morphology is observed in specimens from L3 and the lower half of M3 (MOR 1120, MOR 2982, and MOR 3010). UCMP 128561, from the upper half of M3, exhibits a low nasal boss (25, 26) ( SI Text ). The anteromedial process of the nasal is pronounced in Triceratops from M3, and the NPP is more vertically inclined in specimens from upper M3, producing a more convex rostrum morphology, which was previously found to characterize T. prorsus (12, 23). The frontoparietal fontanelle is open in late-stage subadults/young adults (UCMP 113697). U3 Triceratops. Specimens from U3 exhibit the features Forster (12) found to characterize T. prorsus . U3 Triceratops possess an elongate, relatively narrow nasal horn (average length/width > 2) (Fig. 2 A and Dataset S1). The NPP is more vertically inclined, producing a convex rostrum lacking the low, elongate profile noted in T. horridus [although the largest, and presumably oldest, known specimens (e.g., MOR 004 and MOR 1625) exhibit pro- portionally longer rostra] (Fig. 2 E and Dataset S1). The NPP is anteroposteriorly expanded, and the anteromedial process of the nasal is greatly reduced (Fig. S3) (27). The frontoparietal fontanelle becomes constricted and eventually closed in late-stage subadults/young adults (e.g., MOR 2923 and MOR 2979), ontogenetically earlier than in L3 and M3. The postorbital horn cores are short ( < 0.64 basal-skull length) (Fig. 2 D ). Further, U3 Triceratops seem to exhibit nasals that are more elongate than Triceratops from the lower half of the HCF (Fig. 2 F and Dataset S1). Shifts in Morphology over Time. Epinasals exhibit a directional morphologic trend; average length increases throughout the formation (Fig. 2 A and Dataset S1) (Spearman ’ s rank coefficient = 0.824, P = 4.15E − 07). A protuberance just posterior to the epinasal, observed in specimens from L3 and M3 (Fig. 1), is partic- ularly pronounced in UCMP 113697 from the uppermost M3 (Fig. 1 E ). U3 Triceratops either do not exhibit this feature or express only a subtle ridge in the homologous location. Concurrent with elongation of the epinasal was an expansion of the NPP (Fig. 2 B ) (Spearman ’ s rank coefficient = − 0.969, P = 3.74E − 06) and an increase in the angle between the NPP and the narial strut of the premaxilla (Fig. 2 C and Dataset S1) (Spearman ’ s rank coefficient = 0.802, P = .000186). Nasals also become more elongate relative to basal skull length (although only three specimens with complete nasals have thus far been recorded from the lower half of the formation) (Fig. 2 F and Dataset S1) (Spearman ’ s rank coefficient = 0.804, P = 0.00894). Postorbital horn-core length appears to be variable throughout L3 and M3 and is consistently short in U3 Triceratops (Fig. 2 D and Dataset S1) [Spearman ’ s rank coefficient is negative ( − 0.197) and not statistically significant ( P = 0.392)]. Large juvenile U3 Triceratops (e.g., MOR 1110) can possess more elongate postorbital horn cores (0.64 basal-skull length). Whereas U3 postorbital horn core length falls within the range of variation observed lower in the formation (Fig. 2 D ), elongate postorbital horn cores have thus far not been found in post-juvenile stage Triceratops from U3. Many large Triceratops (e.g., MOR 1122 and MOR 3000) (3) exhibit evidence of postorbital horn-core resorption, suggesting that maximum length is reached earlier in ontogeny. Maximum postorbital horn-core length may have been expressed later in development (or for a longer duration) in Triceratops from lower in the formation. Triceratops from the upper half of the HCF exhibit a more vertically inclined NPP (Fig. 2 C ), which contributes to a rostrum that appears shorter and more convex in lateral profile (a feature Forster noted in T. prorsus ) (12). However, we note that a Spearman ’ s rank correlation test found apparent reduction in rostrum length to be statistically insignificant (Spearman ’ s rank ...Context 7
... and how prominent are these patterns (30 – 32)? Small sample sizes for most nonavian dinosaur taxa complicate the investigation of evolutionary modes in this group. As such, it is unknown how prominent a role anagenesis (the transformation of lineages over time) (Fig. 4 A ) (33 – 37) played in their evolution or whether the majority of morphologies recorded in the fossil record were a product of cladogenesis (evolution via branching events) (Fig. 4 B – D ) (8, 32, 33, 37, 38). Horner et al. (6) presented evidence for anagenesis in several dinosaur clades within the Cretaceous Two Medicine Formation of Montana. It has been suggested that the ceratopsid sample size presented in that study was too small and that cladogenesis was a more conservative interpretation of the data (7). A combination of large sample size, ontogenetic resolution, and detailed stratigraphic data makes Triceratops an ideal taxon for testing hypotheses regarding evolutionary mode in a nonavian dinosaur. Restriction of the full T. prorsus morphology to U3 renders untenable hypotheses that T. horridus and T. prorsus represent sexual or ontogenetic variation within a single taxon. Triceratops from the upper part of M3 exhibit a combination of features found in L3 and U3 Triceratops . This pattern suggests that the evolution of Triceratops incorporated anagenesis. Strict consensus trees produced by cladistic analyses either recover upper M3 specimens in a polytomy with all HCF specimens, in a polytomy of HCF Triceratops from the upper half of the formation, or UCMP 113697 and MOR 3027 cluster together whereas MOR 3045 shares more features with U3 Triceratops (Fig. 3 and Fig. S5). We will consider four alternative hypotheses for the morphological pattern recorded in the HCF: i ) T. prorsus evolved elsewhere and migrated into the HCF, eventually replacing the incumbent HCF Triceratops population by the beginning of the deposition of U3. Upper M3 specimens represent early members (or close relatives of) this group that would come to dominate the ecosystem. ii ) Variation between MOR 3045, MOR 3027, and UCMP 113697 represents intraspecific (or intrapopulation) variation. As the HCF Triceratops lineage evolved, some individuals expressed more of the features that would eventually dominate the population. Over time, these traits were se- lected for and characterized U3 Triceratops. This is a purely anagenetic scenario. iii ) A bifurcation event is recorded in the HCF and occurred at some point before the deposition of U3, resulting in two lineages that differ primarily in the morphology of the epinasal and rostrum (consistent with Forster ’ s diagnoses for T. horridus and T. prorsus ). MOR 3045 represents an early member of a lineage that evolved into U3 Triceratops. This scenario incorporates anagenesis (38) and is presented in some trees produced by the stratocladistic analysis (Fig. S6). iv ) The evolution of Triceratops was characterized by a series of cladogenetic events that produced at least five taxa over the course of the deposition of the HCF (the L3 clade, the lower M3 clade, the MOR 3027 clade, the MOR 3045 clade, and the U3 clade). This strictly cladogenetic scenario suggests that no Triceratops found lower in the HCF underwent evolutionary transformation into forms found higher in the formation. A Biogeographic Signal? The Hell Creek Project ’ s stratigraphic record of Triceratops is primarily restricted to northeastern Montana. It has been hypothesized that T. horridus and T. prorsus were largely biogeographically separated, with T. prorsus generally restricted to the Hell Creek and Frenchman Formations and T. horridus commonly found in the more southern Lance, Laramie, and Denver Formations (15, 17). However, this suggested biogeographic segregation may represent an artifact of the stratigraphic record. Specimens that have thus far been described from neighboring coeval formations exhibit morphologies consistent with their stratigraphic position relative to the HCF (39, 40) ( SI Text ). Anagenesis and Cladogenesis. If the morphological trends noted in Triceratops were purely the result of cladogenetic branching (consistent with punctuated equilibrium) (32) (Fig. 4 C and D ), we would expect to find the full U3 morphology coexisting with Triceratops found lower in the formation, or alternatively, specimens exhibiting the L3 morphology in U3. Such specimens have yet to be discovered ( SI Text ). Specimens from the upper part of M3 exhibit transitional features relative to L3 and U3 Triceratops , a pattern consistent with anagenesis. Some cladistic analyses distinguish MOR 3045 from other upper M3 Triceratops based on variation in the length of the postorbital horn cores, width of the NPP, and the thickened regions of the parietal (Fig. 3, Fig. S5, and SI Text ). Triceratops collected from a multiindividual bonebed in U3 (MOR locality no. HC-430) (44) show variable morphology of the premaxillae and parietal between individuals (Fig. S2) (41). This finding suggests that the variation between upper M3 specimens may represent intrapopulational, not taxonomic, variation (10). Indi- viduals exhibiting more pronounced U3 character states may have become increasingly abundant in the HCF Triceratops population over time until, by the end of the Cretaceous, all Triceratops exhibited these character states (Fig. 4 A ). Alternatively, MOR 3045 may represent an early member of a U3 ( T. prorsus ) lineage, with MOR 3027 representing a separate lineage. Stratocladistic analyses suggest the possibility of two lineages in the HCF (Fig. 4 B and Fig. S6); however, this scenario would require the independent evolution of an enlarged epinasal-nasal protuberance. A purely cladogenetic interpretation of the HCF Triceratops dataset suggests the presence of at least five stratigraphically overlapping taxa in the formation (Fig. 4 C and D ). This scenario is possible, but we would argue that interpretations that incorporate populational transformation (anagenesis) are more conservative. Specimens from upper M3 exhibit a combination of primitive and derived characters, as well as more developed states of characters expressed in L3 Triceratops . Forster (12) noted that, whereas T. prorsus exhibited derived characters, no autapomor- phic characters were recognized in T. horridus . This finding is consistent with the hypothesis that the evolution of Triceratops incorporated anagenesis and illustrates the potential difficulties with defining species in evolving populations (6, 35). The HCF dataset underscores the importance of considering morphologies in a populational, rather than typological, context (42). The documented changes in Triceratops morphology occurred over a geologically short interval of time (1-2 million y) (2). High-resolution stratigraphy is necessary for recognizing fine- scale evolutionary trends. If cladogenesis is considered the primary mode of dinosaur evolution, a problematic inflation of dinosaur diversity occurs. Current evidence suggests that the evolution of Triceratops incorporated anagenesis as there is currently no evidence for biogeographic segregation of contemporaneous Triceratops morphospecies and there is evidence for the morphological transformation of Triceratops throughout the HCF. This dataset supports hypotheses that the evolution of other Cretaceous dinosaurs may have incorporated phyletic change (6, 43, 44) and suggests that many speciation events in the dinosaur record may represent bifurcation events within anagenetic lineages ...