A new species of tyrannosaurid from the upper Two Medicine Formation of Montana supports the presence of a Laramidian anagenetic (ancestor-descendant) lineage of Late Cretaceous tyrannosaurids. In concert with other anagenetic lineages of dinosaurs from the same time and place, this suggests that anagenesis could have been a widespread mechanism generating species diversity amongst dinosaurs, and perhaps beyond. We studied the excellent fossil record of the tyrannosaurid to test that hypothesis. Phylogenetic analysis places this new taxon as the sister species toDaspletosaurus torosus. However, given their close phylogenetic relationship, geographic proximity, and temporal succession, whereD. torosus (~76.7–75.2 Ma) precedes the younger new species (~75.1–74.4 Ma), we argue that the two forms most likely represent a single anagenetic lineage.Daspletosaurus was an important apex predator in the late Campanian dinosaur faunas of Laramidia; its absence from later units indicates it was extinct beforeTyrannosaurus rex dispersed into Laramidia from Asia. In addition to its evolutionary implications, the texture of the facial bones of the new taxon, and other derived tyrannosauroids, indicates a scaly integument with high tactile sensitivity. Most significantly, the lower jaw shows evidence for neurovasculature that is also seen in birds.

Tyrannosaurinae is a diverse clade of advanced theropods from the Late Cretaceous of Asia and the American West that culminated in the giantT. rex at the end of the Mesozoic^1,2,3,4. The clade has a high diversity in body size and skull shape, including medium-sized taxa with long and low skulls⁵, large taxa with short snouts², and a dwarf species from the Arctic Circle⁶. Tyrannosaurines are geographically widespread; fossils have been collected in China and Mongolia, and throughout western North America, from Alaska to Texas. The evolutionary success of Tyrannosaurinae is also reflected in its 14 million-year duration, which includes the geologically oldest species of tyrannosaurid⁴.

We report here the discovery of a new large tyrannosaurine (Figs 1–4) from the Upper Cretaceous of Montana. Phylogenetic analysis places this taxon as the sister species ofDaspletosaurus torosus (Fig. 2). The new species adds to the number of late Campanian tyrannosaurines and shows that this clade was a dominant component of the dinosaur faunas of the American West shortly after the emplacement of the Western Interior Seaway, in contrast to the depauperate, and geographically and temporally restrictedAlbertosaurus lineage that makes up the sister lineage of Tyrannosaurinae. In terms of its geological age and excellently preserved fossils, the new taxon is important regarding tyrannosaur evolution and appearance.

Skull and jaws of the holotype (MOR 590) ofDaspletosaurus horneri sp. nov.; (A) photograph and, (B) labeled line drawing of skull and jaws in left lateral view; (C) photograph and, (D) labeled line drawing of occiput and suspensorium in caudal view; (E) photograph and, (F) labeled line drawing of skull in dorsal view. Scale bars equal 10 cm. Abbreviations: MOR, Museum of the Rockies.

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(A) Phylogenetic relationships of tyrannosaurines calibrated to geological time. Full consensus trees in Extended Data. Synapomorphies of theDaspletosaurus lineage from: (B) maxilla of MOR 1130; (C) lacrimal of MOR 1130; (D) postorbital of CMN 11594; (E) vomer of MOR 590; (F) palatine of MOR 1130; and (G) frontoparietal complex of MOR 590. Abbreviations: AMNH FARB, American Museum of Natural History, Fossil Amphibians, Reptiles, and Birds; As, Asia CMN, Canadian Museum of Nature; K/Pg, Cretaceous-Paleogene; LA, Laramidia; MOR, Museum of the Rockies.

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Unambiguously optimized derived phylogenetic characters were recovered as synontomorphies at two of the five growth stages, which are labeled at the corresponding numbers. Scale bar equals 10 cm. Abbreviations: AMNH FARB, American Museum of Natural History, Fossil Amphibians, Reptiles, and Birds; MOR, Museum of the Rockies.

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Bone texture indicates large zones of large, flat scales and subordinate regions of armor-like skin and cornified epidermis; integumentary sense organs occur on the flat scales that cover the densest regions of neurovascular foramina. The region outside of the crocodylian-like skin is reconstructed with small scales after fossilized skin impressions of tyrannosaurids. This figure is not covered by the CC BY licence. Illustration © Dino Pulerà. All rights reserved, used with permission.

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Tyrannosaurs, the larger group of giant predatory dinosaurs of the Late Cretaceous from Asia and North America, are notable in terms of diversity and evolution thanks to many discoveries of new species over the past decade^{2,3,4,7,8,9,10}. With an excellent fossil record, tyrannosaurs stand as exemplar fossil organisms in studies of dinosaur biomechanics, development, anatomy, evolution, cognition, and paleoecology^3,7. Further, their well-resolved phylogeny and excellent stratigraphic record provides the rare opportunity to investigate the evolutionary processes (i.e., speciation modes) behind their numerical diversity and extreme morphologies^2,5,7,10,11.

Several extinct clades with stratigraphically continuous fossil records, including invertebrates¹², sticklebacks¹³, and mammals¹⁴ exhibit anagenesis, evolution within a single lineage. Among living species, anagenesis has occurred in cyprinid teleosts¹⁵ and it has produced genetic diversity among oceanic island plants^16,17. Anagenesis gained currency in studies of dinosaur evolution with Horneret al.’s¹ landmark study that found evidence for phyletic evolution in four lineages of dinosaurs, including tyrannosaurs, from the Late Cretaceous of the American West.

Renewed interest in anagenesis among dinosaur workers stems from the further discovery of stratigraphically stacked sequences of ornithischian dinosaurs, specifically hadrosaurids and ceratopsians^18,19 and coincides with the realization among paleontologists and neontologists that the branching patterns of phylogenies do not necessarily reflect the actual processes that produced organismal diversity^20,21,22,23. For example, anagenesis is a linear process that is obscured when the continuum of change is atomized into multiple subunits (species) and are arranged into a branching pattern on a phylogenetic tree^12,22.

Currently, it remains unclear if anagenesis is a frequent mode of speciation in dinosaur evolution. Studies of other organisms suggest that it is not²⁰. For example, cladogenesis (splitting or budding of an ancestor into daughter species) is considered to be the most frequent speciation mode among fossil invertebrates, and perhaps across metazoans in general^12,15,20.

For paleontologists, the best evidence for anagenesis requires dense stratigraphic sampling and precise radiometric dating, temporally successive specimens of close phylogenetic relationship, clear stratigraphic data for specimens, and a high sample size that includes growth series^{1,18,19,20,24,25}. Tyrannosaurs represent one of the few dinosaur clades that meet these criteria^7,26,27,28. Here we present a test of Horneret al.’s¹ case for anagenesis among Late Cretaceous North American tyrannosaurs that meet all of those criteria.

Tyrannosaurs in the flesh are ubiquitous across all media, from museum galleries to Hollywood blockbusters, arguably making them the most iconic dinosaurs in modern culture. As ambassadors of Natural History, it is ironic that the life appearance of the tyrannosaur face has not been rigorously studied, despite the availability of well-preserved fossils, published data on their closest living relatives (birds, crocodylians), and modern comparative methods^29,30. The question of facial integument in theropods (meat-eating dinosaurs) is critical to understanding the evolutionary transition from nonbeak to beak along the line to birds, since beaks are specialized epidermal structures³¹.

Tyrannosaurs are central to this question: they are advanced, bird-like theropods with large skulls covered in a variety of textures that correspond to identifiable, overlying soft tissues²⁹. We apply the information known about textures and their causal soft tissues to deduce the life appearance of the integumentary covering of tyrannosaurs²⁹; these results can then be placed into the framework of the evolutionary transition from nonavian theropods to birds. Theropoda Marsh, 1881

Tyrannosaurinae Matthew and Brown, 1922 (sensu Serenoet al., 2005)

Daspletosaurus Russell, 1970

Daspletosaurus. All species more closely related toDaspletosaurus torosus than toTyrannosaurus rex.

D. horneri sp. nov.

Horneri, Latinized form of Horner, in honor of Jack Horner, in recognition of his successful field program in the Two Medicine Formation that has recovered many new species of dinosaurs that are critical for our understanding of the palaeobiology of dinosaurs in Laramidia, support in the preparation and curation of these specimens, and to acknowledge that his mentoring efforts have launched many professional scientific careers.

MOR (Museum of the Rockies, Bozeman) 590, a complete skull, partial pectoral limb, and nearly complete hindlimb (Fig. 1, seeSupplementary Tables S1,S2,S3).

MOR 1130, an incomplete skull, partial axial series, and partial pelvic girdle and hindlimb. MOR 553S/7.19.0.97, a nearly complete dentary of a small juvenile, based on four features shared with the holotype and the other paratype: 17 dental alveoli, first three alveoli form a rostromedially extending arcade, laterally bowed dentary, rostroventral corner of bone is below the level of the septum between alveoli three and four.

AMNH FARB (American Museum of Natural History, Fossil Amphibians, Reptiles, and Birds, New York) 5477, a maxilla, partial postorbital, and parietal; MOR 3068, a partial mandibular ramus; MOR 553D.9.19.91, left ectopterygoid; MOR 553E.7.6.91.196, right ectopterygoid.

Glacier County (Co.), Lewis and Clark Co., and Teton Co., Montana, USA; Upper Cretaceous upper Two Medicine Formation.

The type and paratype specimens all come from the upper portion of the Two Medicine Formation^32,33 (TMF); MOR 590 occurs 65 m below a dated bentonite horizon (TM-4)⁷, and the MOR 553 specimens sit at least 10 m above this same bentonite. TM-4 occurs 480 m above the base of the ~545 m–thick TMF³², and recalibration of legacy standards on⁴⁰Ar/³⁹Ar ages from the TMF³² indicates that the TM-4 tuff is older than previously considered, yielding a recalibrated age of 75.03 Ma +/− 0.72 Ma³⁴. The fourth skeleton (MOR 1130) comes from within the disturbed belt on the eastern flank of the Rocky Mountains where folding and faulting make determining exact stratigraphic positions difficult. However, the MOR 1130 specimen sits 5.9 m above a newly dated bentonite, reported here to be 74.38 +/− 0.72 Ma (U-Pb zircon weighted mean age (1 σ; MSWD = 0.55); seeSupplementary Fig. S1, Discussion S1,Table S4; for bentonite locality information see ref.35), indicating that it is slightly younger than the other specimens.

Can be distinguished from all other derived tyrannosauroids, includingDaspletosaurus torosus, by the presence of: a wide dental arcade at the front of the snout, where the maxillary and dentary tooth rows extend distinctly rostromedially and the first interdental plate of the maxilla is narrow, which resembles those of the premaxilla where the tooth row is mediolaterally oriented; dentary distinctly bowed (convex) laterally; promaxillary sinus stopping between alveoli 3 and 4, as observed in medial view of the completely prepared pneumatic chamber; rostral end of the choana on the maxilla above alveolus 7; inflated dorsal surface of the lacrimal not reaching the medial edge of the bone; medial pneumatic recess of the lacrimal tall and narrow slot; concave upper half of orbital margin of the lacrimal; entire circumference of the pneumatic recess of the squamosal is undercut and clearly defined; sinuous rostral edge in dorsal view of the dorsotemporal fossa on the frontal; joint surface for the squamosal on the parietal covers the base of the caudolateral process; and the tympanic ridge extends onto the prootic.

Several autapomorphies were obtained by the cladistic analysis; autapomorphies were not included in the data matrix, but several characters were optimized on the terminal branch ofD. horneri. These include a pneumatic foramen penetrating the lateral surface of the quadratojugal, shallow notch between the basal tubera, short epipophyses of the anterior cervicals, and the humerus is ~34% the length of the femur (for further comparisons seeSupplementary Discussion S2 andSupplementary Fig. S2).

The so-called Two Medicine tyrannosaurine has been included in several phylogenetic analyses^{2,3,4,8,11,36}, with scorings based primarily on MOR 590. It has universally been recovered as a derived tyrannosaurine, but its specific relationships are unresolved, where it has been recovered as the sister species ofD. torosus^2,3,8,36 or closer toT. rex^4,36. Description of the taxon has been limited to brief summaries of salient features (e.g., form of lacrimal horn) that distinguish it fromD. torosus and to differentiateDaspletosaurus from other genera of tyrannosaurs^1,37, but an extensive description of the taxon has not been made.

TheD. horneri holoype is estimated to be ~9.0 m in total length and 2.2 m tall at the acetabulum (for additional measurements, seeSupplementary Tables S1, S2 andS3).D. horneri differs from its sister species in thatD. torosus has a rostral ramus of the lacrimal that is longer than the ventral ramus, indicating thatD. horneri has a taller skull. The antorbital fossa of the lacrimal is separated by a deep concavity from the ventral ramus of the bone inD. torosus, whereas these surfaces are confluent inD. horneri. InD. torosus, the coronoid region of the surangular faces equally dorsally and laterally, whereas it faces more laterally than dorsally inD. horneri.

Daspletosaurus is one of the best-supported tyrannosaurid clades, distinguished by a suite of unique, mostly cranial features (Fig. 2) that suggests a relatively long evolutionary history. In particular, the cornual processes (‘horns’) ofDaspletosaurus are enhanced: a new, secondary horn extends from the side of the large, triangular primary lacrimal horn that is expressed by most tyrannosaurids; and the postorbital horn, which nearly spans the rostrocaudal width of the postorbital bar, is the largest seen among tyrannosaurids. The primary cornual process of the lacrimal differs between the twoDaspletosaurus species, being taller inD. torosus (ratio height of process to maximum height of rostral ramus: 69%) than inD. horneri (ratio: 53%).

Phylogeny

The phylogenetic analysis (see Supplementary phylogenetic character list,Tables S5 andS6) recovered 18 most parsimonious trees, each having a tree length of 802 steps, a CI of 0.56, an HI of 0.44, and an RC of 0.45. The topology conforms to that of earlier works^3,11, but the strict consensus tree and 50% majority rule tree shows thatAviatyrannis and Proceratosauridae and the lineage leading to more derived tyrannosauroids form an unresolved trichotomy (Fig. 2A; seeSupplementary Fig. S3). Also, the tyrannosaurinesLythronax, Teratophoneus, andNanuqsaurus form an unresolved trichotomy.Alioramus andQianzhousaurus are recovered as sister species, and given that relationship we regard the genusQianzhousaurus as a junior synonym ofAlioramus (Fig. 2A). We follow the taxonomic practice in regarding sister species as congeneric, so this renaming does not constitute a phylogenetic rearrangement of alioramins. This convention is followed elsewhere in the tree (e.g.,Albertosaurus, Daspletosaurus, Tyrannosaurus). Our results recoverTimurlengia as more derived thanXiongguanlong and as the sister species of a new taxon from the Iren Dabasu Formation. The latter taxon (under study by TDC) is based on a partial individual (AMNH FARB 6556) that includes several teeth (premaxillary, lateral) and skull bones (lacrimal, jugal, pterygoid, ectopterygoid, quadratojugal) that was collected in 1923 under the auspices of the AMNH. The presence of D-shaped premaxillary teeth and the presence of a jugal pneumatic recess with a secondary fossa identifies it as a derived tyrannosauroid. The absence of hindlimb bones prevents comparison with the lectotype ofAlectrosaurus olseni, and so it was treated as a separate taxon in our analysis (for a complete list of unambiguously resolved synapomorphies seeSupplementary synapomorphy list).

Importantly,Daspletosaurus horneri is recovered as the sister species ofD. torosus; this relationship is supported by 11 unambiguously optimized synapomorphies (Fig. 2B–G), including the presence of a coarse subcutaneous surface of the maxilla, an accessory cornual process on the lacrimal, a partly concealed maxillary process of the lacrimal, a cornual process of the postorbital that closely approaches the laterotemporal fenestra, a rostral tip of the squamosal that stops caudal to the rostral margin of the laterotemporal fenestra, a ridge along the nasal process of the frontal, a deep ventral keel on the vomer, a caudal pneumatic recess of the palatine that is positioned caudal to the rostral margin of the dorsal process, a distinct mediolaterally oriented ridge on the dorsum of the laterosphenoid that extends toward the medial edge of the dorsotemporal fenestra, a ‘chin’ of the dentary (where the rostral and ventral margins of the dentary join) that is positioned below the third dentary tooth, and there are more than 13 maxillary teeth.

Historical biogeography

The pattern of historical biogeography indicated by our parsimony analysis is consistent with the hypothesis of Brusatte and Carr¹¹, where North American taxa are not divided into northern and southern subclades⁴. Our topology shows an Asian diversification intermediate-grade tyrannosauroids (Xiongguanlong baimoensis, Timurlengia euotica, Iren Dabasu taxon) during the mid- and early Late Cretaceous that preceded a dispersal event to North America, which was followed by subsequent and frequent exchange between the landmasses throughout the Late Cretaceous.

Ontogeny

The growth series ofD. horneri includes juveniles, subadults, and an adult (Fig. 3). The smallest specimen, a dentary, has a tooth row that is 221.5 mm long, in contrast to the 423.0 mm tooth row of the adult, which has a 947.0 mm long skull. The length of the dentary tooth row has been shown by Currie³⁸ that in comparison with skull length, it shows a weak negative allometry. Therefore, the original skull length of the small specimen was greater than 496.0 mm, slightly more than half the length of the adult skull.

The parsimony analysis of morphological features (see Supplementary ontogenetic character list, DataS1) resulted in a single most parsimonious growth series of 168 steps, with a CI of 0.93, an HI of 0.07, an RI of 0.93, and an RC of 0.91 (Fig. 3; seeSupplementary Fig. S4). The transition from a gracile juvenile to a robust adult inD. horneri is similar to that seen in other tyrannosauroids^8,26,28.

Soft tissues

The excellent quality of preservation of these specimens permits us to assess the type of soft tissue that covered the face (premaxilla, maxilla, nasal, lacrimal, jugal, postorbital, squamosal, dentary). InD. horneri, and in all derived tyrannosauroids, the subcutaneous texture is coarse and shows a hierarchy of textures (seeSupplementary Discussion S3). In order to identify the soft tissue that produced this complex surface, we compared the condition of tyrannosaurids with that of crocodylians (Alligator mississippiensis) and birds (Struthio camelus, Anser sp.,Anas sp.,Cygnus sp.,Meleagris gallopavo), and we followed several studies^29,31,39,40 to identify osteological correlates imprinted on the cortical surface of facial bones to deduce their causal soft tissues.

Although tyrannosaurids, crocodylians, and birds share neurovascular foramina that are densely clustered at the front of the jaws and form rows along the oral margin, the smooth texture of the snout in birds is sharply different from the hummocky texture of the facial bones of crocodylians and tyrannosaurids. The coarse surface of crocodylians is covered by many flat scales²⁹, whereas in birds the rhamphotheca (beak) covered the smooth surface of the snout and jaws. The coarse texture shared between tyrannosaurids and crocodylians indicates a primary covering of flat scales on the face of the nonavian dinosaurs (Fig. 4).

In archosaurs, a scaly integument appears to be correlated with the multiple rows of foramina seen in crocodylians and tyrannosaurids, whereas in birds the foramina deep to the beak are limited to the jaw tips, the caudal end of the maxilla, and in a row along the side of the lower jaw. A similar localization of foramina is seen in ornithischian dinosaurs, whose jaws and oral margins were sheathed by beaks ahead of the tooth row³⁹.

Unlike crocodylians, the alveolar row of foramina in the dentary of derived tyrannosauroids and birds occurs in a common groove that extends for much of the length of the bone. This groove is not seen in crocodylians, although caudodorsally extending sulci extend from the foramina. In birds the groove is covered by the rhamphotheca, and the ventral branches of the rictal vessels and the external branch of the mandibular nerve lie in the groove⁴⁰. The groove in tyrannosauroids is shallowly inset, unlike the sharply inset condition that is seen in birds. The presence of the groove in tyrannosauroids indicates that the ventral branches of the rictal vessels evolved prior to, and might have been prerequisites for, the later appearance of the beak (in terms of the stepwise vascular changes leading from nonbeak to beak), at least on the lower jaw. The caudal end of the groove fades out in birds, a condition that is also seen in mature tyrannosauroids⁴¹.

Variation in the coarse zone of the face in tyrannosaurids indicates a variety of epidermal types, in addition to flat scales. The rostral surface of the premaxilla, dorsum of the nasals, dorsolateral surface of the lacrimal, cornual process of the jugal, and the rostroventrolatral surface of the dentary, bear small bony papillae, which indicate regions of armor-like skin²⁹ (Fig. 4, seeSupplementary Discussion S3). Finally, the coarse and rim-like edges of the postorbital horn, and its smooth central region, indicate a cornified sheath-like covering on its surface and part of the postorbital bar (Fig. 4).

Anagenesis

A hypothesis of anagenesis amongst tyrannosaurids (D. torosus ->D. horneri ->T. rex) is defensible if: (1) the taxa are sister species or a phylogenetically successive series of species, (2) the species are stratigraphically sequential, (3) the phylogenetic relationships do not conflict with their stratigraphic sequence, and the taxa (4) are from the same landmass or adjacent landmasses that had connections that do not conflict with their chronological sequence.

Our new phylogeny (Fig. 2A) shows thatD. torosus andD. horneri are sister species, whereasT. rex is nested in a separate clade. This topology is different from the phylogenetic arrangement of previous workers¹, whereD. torosus is the sister species of a clade composed ofD. horneri andT. rex. In our phylogeny,T. rex is separated from theDaspletosaurus clade by two phylogenetically- and almost certainly stratigraphically-successive⁴ sister species,Zhuchengtyrannus magnus andT. bataar.

Chronostratigraphic and lithostratigraphic correlation between the TMF and Dinosaur Park Formation (DPF) suggests that the DPF correlates with the upper 220 m of the TMF^42,43,44,45. In-progress high-precision U-Pb dating of the four ash beds spanning the top of the Oldman Formation, the DPF and the lower part of the Bearpaw Formation (BPF) indicates an age range between 76.69 Ma–74.26 Ma (internal error <±30 ka) for this stratal package⁴⁶. Given that uppermost date of 74.26 Ma is from the lower BPF and these workers have identified a slowdown in sedimentation rates for the upper 22 meters of the DPF-BPF transition⁴⁶, the age of the top of the DPF is likely no younger than 74.5 Ma. BecauseD. torosus specimens are restricted to the lower two-thirds of the DPF (~76.7–75.2 Ma), andD. horneri specimens are limited to the uppermost part of the TMF⁴⁵ (~75.1–74.4 Ma) there appears to be little or no stratigraphic overlap betweenDaspletosaurus specimens from these two field areas. New high-precision CA-TIMS U-Pb dating is underway and promises to better resolve stratigraphic uncertainties.

Therefore,D. torosus andD. horneri meet the primary criteria for anagenesis: They are sister species, stratigraphically successive, and are from the Northern Rocky Mountain Region. In contrast, the divergence between theDaspletosaurus clade on the one hand, and theZ. magnus + Tyrannosaurus clade on the other, was the result of a cladogenetic (lineage-splitting) event, since they do not form a continuous series of stratigraphically sequential taxa. Therefore,T. rex was not a continuation of the anageneticDaspletosaurus lineage¹.

TheZ. magnus + Tyrannosaurus clade consists of a pair of sister species (T. bataar + T. rex) and a sister taxon that extends from the preceding node (Z. magnus). This topology is consistent with a hypothesis of anagenesis:Z. magnus lived no less than 73.5 Ma⁴⁷, andT. rex lived between 66.0 and ~67.2–67.4 Ma⁴⁸. The age of the Nemegt Formation, from whichT. bataar has been collected, is less than 75.0 Ma based on radiometric dating of the underlying Barun Goyot Formation⁴⁹. Therefore, ifT. bataar is intermediate in age betweenZ. magnus andT. rex, then the chronological sequence of these tyrannosaurs is also consistent with anagenesis. The time gap (~6.1–6.3 Myrs) that separatesZ. magnus andT. rex greatly exceeds that betweenD. torosus andD. horneri; therefore, the hypothesis of anagenesis fromZ. magnus toT. rex will be tested as new tyrannosaur specimens are collected from that interval in Asia and included in new phylogenetic analyses.

This is also the case for the two sister species ofAlbertosaurus, which are stratigraphically successive and from the same geographic region, in northern Laramidia^37,50. If the Asian sister speciesAlioramus remotus andA. sinensis are shown to be stratigraphically successive (the taxa are widely separated geographically, and neither is constrained by radiometric dates^5,10), then they meet the criteria as well, but in the absence of those data the decision between anagenesis and cladogenesis is equivocal.

Based on this approach, the evidence for anagenesis might be widespread among other dinosaur lineages with high-quality fossil records. If so, then anagenesis was an important contributor towards the generation of species diversity, in addition to cladogenesis, and in some instances cladogenesis might be an artifact of an incomplete fossil record.

Ontogenetic tooth count reduction

D. horneri shows another occurrence of growth related reduction in maxillary tooth count among tyrannosaurids, which starts in juveniles (AMNH FARB 5477) with 15 maxillary teeth, increases to 17 tooth positions in subadults (MOR 590), and then decreases to 15 in adults (MOR 1130). In contrast, the number of dentary teeth is constant, where 17 alveoli are seen in juveniles (MOR 553S/7.19.0.97), subadults (MOR 590) and adults (MOR 1130).

The pattern of tooth count increase followed by a decrease inD. horneri may result from individual variation. However, this general pattern is also seen in the maxilla ofD. torosus, where the least mature specimen (TMP 1994.143.0001) has a count of 13 teeth that increases in more mature specimens to 15 (AMNH FARB 5346) or 16 (MOR 395), which is followed by a decrease in the most mature specimens (CMN 8506) to a minimum of 14.

The phenomenon of growth related tooth count reduction is seen in the maxilla and dentary ofT. rex^26,28. The pattern of an initial increase to a later decrease is also seen in the recently published data forT. rex of Brownet al.⁵¹, where an increase in tooth count of the dentary (from 16 to 17) is seen in the two least mature specimens (CMNH 7541, BMRP 2002.4.1). Work in progress by one of us (TDC) finds that the smaller CMNH 7541 is the less mature specimen of the two. An increase is potentially also seen in the maxilla, where the tooth count for one specimen (BMRP 2002.4.1) is different between sides (left: 16, right: 15), but the authors only included the lower count in their data set⁵¹. Including the higher count would result in an increase from 15 to 16 teeth, followed by a decrease in number with increasing size, as seen in their data. If the tooth counts reflect ontogeny, and allowing for slightly different rates of tooth increase on each side of the jaw, it appears that an initial increase in tooth count followed by a decrease in number is typical of derived tyrannosaurines.

Ontogenetic facial texture reduction

There is an ontogenetic reduction in the coarseness of the facial texture from subadult (MOR 590) to adult (MOR 1130), especially of the nasal bones that form the top of the snout, where the texture is reduced. Examination of specimens ofT. rex reveals the same pattern, where the snout is coarse in relatively young adults (AMNH FARB 5027), whereas it is smoother in relatively old adults (LACM 23844)²⁸. This reduction in texture that is seen among tyrannosaurines is similar to the reduction in cephalic ornamentation that also occurs in other dinosaurs, including ceratopsids^52,53,54 and pachycephalosaurians⁵⁵. It is possible that ornament reduction in adults is an ancestral feature for dinosaurs. A complete list of synontomorphies (growth-related features) and an extended discussion of the growth series can be found in the Supplementary synontomorphy list and DiscussionS4.

Quadratojugal foramen

It has been claimed that the presence of a large pneumatic foramen in the lateral surface of the quadratojugal is unique to the contentious tyrannosaurid taxonNanotyrannus lancensis⁵⁶, the holotype of which has been revised to represent a juvenileT. rex^26,28. However, this feature is also seen in the adult specimen ofD. horneri, and in an isolated tyrannosaurid quadratojugal from the upper Campanian strata of southern Alberta (CMN 57080). Although our phylogenetic analysis shows that the quadratojugal foramen evolved independently inD. horneri andT. rex, the additional occurrence in the unidentified taxon from Alberta indicates that the foramen might be synapomorphic for derived tyrannosaurines.

Phylogenetic implications

The phylogenetic analysis placesD. horneri as the sister species ofD. torosus, indicating a monophyly of the known species withinDaspletosaurus, in contrast to a recent hypothesis that the clade is paraphyletic⁴. We attribute the difference in results to the absence of the lacrimal, frontal, and vomer characters from the data set of Loewenet al.⁴. Therefore, theDaspletosaurus lineage traces back to the interval between the emplacement of the WIS at 99.5 Ma, as represented by the Thermopolis Shale⁵⁷, and approximately 80 million years ago, the age of the oldest tyrannosaurines from the American West⁴.

Biogeographic implications

The stratigraphic distribution of specimens discussed above shows thatDaspletosaurus spp. inhabited northern Laramidia (what is now southern Alberta and northern Montana) for a minimum duration of ~2.3 Ma. This areal distribution makesDaspletosaurus one of the most widely distributed Late Cretaceous tyrannosaurid clades in Laramidia before the arrival ofT. rex; in contrast, the distribution of other taxa is marked by high endemism, where species are limited to local basins of deposition⁴. In Alberta,D. torosus was sympatric with another large tyrannosaurid,Albertosaurus libratus³⁷, but in Montana, at present, no sympatric tyrannosaurids are known.

Dispersal of tyrannosaurines from Laramidia to Asia must have occurred in that span (99.5 to ~80.0 Ma), to account for the presence in Asia of the relatively basalAlioramus and derivedTyrannosaurus (both from the Nemegt Formation, ~75.0–66.0 Ma⁴⁹), and the derivedZ. magnus (Wangshi Group, 73.5+ Ma⁴⁷). Also, there is no evidence for faunal exchange between the landmasses from 80 to 75.7 Ma, so the dispersal had to occur prior to this point. SinceDaspletosaurus is the sister species of theZhuchengtyrannus + Tyrannosaurus clade, both had to arise before the dispersal event. From these observations we predict that species of theDaspletosaurus lineage will be present in rocks several Myrs older than the oldest existing examples of individuals from that lineage (from the DPF, ~76.7 Ma).

Soft tissue interpretations

In tyrannosaurids, a scaly facial integument in association with multiple rows of neurovascular foramina on the snout and jaws serves as a reliable proxy for tactile sensitivity in these giant predatory dinosaurs. In crocodylians the craniomandibular foramina convey hundreds of afferent branches from the trigeminal nerve (N. V) in a density that transmits high resolution tactile sensations from the skin, making their snouts more sensitive than human fingertips⁵⁸. The density of foramina in crocodylians maps with the distribution of the integumentary sensory organs (ISOs) in the skin of the head, where they are densest at the rostral end of the jaws and along the oral margins adjacent to the teeth, and sparsest on the sides of the jaws and top of the snout. Given the nearly identical arrangement and density of foramina to crocodylians, we can now infer that tyrannosaurids possessed ISOs (Fig. 4) to transmit trigeminal innervation from the facial skin, as in seen in crocodylians and comparable mechanoreceptors of other terrestrial tetrapods (e.g., monotremes, moles, toads, frogs, snakes, ducks)⁵⁸.

If our soft–tissue inferences regarding the presence of flat facial scales and ISOs are correct, then behavioral inferences for tyrannosaurids can be drawn based on comparison with crocodylians⁵⁹. Tyrannosaurids had a highly sensitive facial tactile system that functioned in prey capture, and object identification and manipulation, given the skeletal similarities with crocodylians^58,59. In crocodylians the bony casements around the nerve branches protect them from injuries sustained during communal feeding while maintaining highly sensitive skin⁵⁸; given the similarity in foramen morphology, this protective function was present in tyrannosaurids (whose bony oral margins often show lesions), showing that this multipurpose cephalic tactile system was not limited to life in an aquatic environment.

Assuming that crocodylians are suitable models for dinosaur behavior, and that tyrannosaurids were primarily terrestrial, tactile stimulation, such as rubbing, was probably more important in tyrannosaurid agonistic behavior than detecting water borne vibrations⁵⁹. As in crocodylians, female tyrannosaurids would have relied upon ISOs on the snout for detecting the optimal temperature of a nest site, and for maintaining nest temperature and the nest materials; also, ISOs would have aided adult tyrannosaurids in harmlessly picking up eggs and nestlings and, in courtship, tyrannosaurids might have rubbed their sensitive faces together as a vital part of pre-copulatory play⁵⁹.

Character dataset

We includedD. horneri in an updated data matrix that is based on the most recent tyrannosauroid phylogeny¹¹, which analyzed 366 characters, and we contributed another 20 new characters to the data matrix, for a total of 386 (see Supplementary Phylogenetic character list andTables S5 andS6). We also includedTimurlengia euotica⁷ and an undescribed species from the Iren Dabasu Formation that is currently under study by one of us (TDC), for a total of 28 ingroup taxa. Unlike some other analyses⁴, ours does not includeBagaraatan ostromi orAlectrosaurus olseni, but we include the referred material ofTeratophoneus curriei. We take the view thatAlioramus altai is synonymous withA. remotus, which we coded together into a single taxonomic unit. We regardRaptorex kriegsteini as a juvenile tyrannosaurine, which we excluded from the analysis.

Parsimony analysis

We built the data matrix in MacClade 4 v.4.08⁶⁰; we analyzed the data in a branch-and-bound search using PAUP* v. 4.0b10⁶¹. Ordering of characters followed reference¹¹. As in the preceding analyses,Allosaurus sp., Maniraptora, Ornithomimosauria, andCompsognathus longipes were included as the outgroup taxa. The common components of the MPTs were summarized in a strict consensus and in a 50% majority rule consensus, which had the same topology (Fig. 2A); Bremer decay and bootstrap values we used to assess clade support (seeSupplementary Fig. S3).

Ontogeny

We reconstructed a hypothetical growth series forD. horneri, based on a cladistic analysis of 164 characters coded for 5 specimens (seeSupplementary Data S1). We built the data matrix in MacClade 4 v.4.08⁶⁰; we analyzed the data in a branch-and-bound search using PAUP* v. 4.0b10⁶¹ with the characters unordered and unweighted. An all-zero artificial embryo was included to optimize the characters on the topology.

Data archiving

All primary data, including the geochronological analysis, phylogenetic character list and character-taxon matrix, ontogenetic character list and character-specimen matrix, are available in thesupplementary information and Extended Data.

How to cite this article: Carr, T. D.et al. A new tyrannosaur with evidence for anagenesis and crocodile-like facial sensory system.Sci. Rep.7, 44942; doi: 10.1038/srep44942 (2017).

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T.D.C. thanks the following people for access to specimens under their care: D. Brinkman, J. Horner, P. Makovicky, M. Norell, X. Wu, and S. Brusatte for assistance with obtaining the bootstrap values of the phylogenetic analysis. T.D.C. was supported by a Faculty Research & Development Grant from Carthage College. D.J.V. and J.R.M. thank the Bahamas crews of 2000 and 2001. D.J.V. thanks E. Metz, E. Przybyszewski, and A. Takekawa for help in the field and B. Harmon and J. Jette for preparation of specimens. J.C.S. thanks L. M. Witmer for guidance as his advisor during his dissertation work. J.C.S. was supported by a Dissertation Improvement Grant. E.M.R. thanks P. C. Owusu Agyemang and R. Holm for assistance with heavy mineral separations and U-Pb LA-ICPMS analysis. We thank D. A. Eberth for discussion on Belly River Group geochronology. J.R.M. thanks Channel 4 production company for contributing funding for fieldwork on MOR 1130. All authors thank D. Pulerà for rendering the life reconstruction ofD. horneri, S. Williams for the photo of the quadratojugal of MOR 1130, S. Brusatte and an anonymous reviewer for their constructive comments, and R. McCrea for handling the manuscript.

Affiliations

1. Carthage College, 2001 Alford Park Drive, Kenosha, WI 53140, USA

   • Thomas D. Carr

2. Department of Earth Sciences, Montana State University, P.O. Box 173480, Bozeman, MT 59717-3480, USA

   • David J. Varricchio

3. Louisiana State University Health Sciences Centre - School of Medicine, 1901 Perdido Street, New Orleans, LA 70112, USA

   • Jayc C. Sedlmayr

4. Geosciences, College of Science and Engineering, James Cook University, Townsville, QLD 4811, Australia

   • Eric M. Roberts

5. Honors College, University of New Mexico, Albuquerque, NM 87131, USA

   • Jason R. Moore

Contributions

T.D.C. wrote the description of the new taxon, collected and analyzed the phylogenetic and ontogenetic data, and wrote the corresponding parts of the manuscript. D.J.V. collected specimens MOR 553 and 1130 and analyzed the stratigraphic data in the field, and wrote the corresponding methods and results. T.D.C and J.C.S. collected and analyzed the data on epidermal soft tissue and associated neurovasculature; T.D.C. wrote the results. E.M.R. analyzed the geochronological data and wrote the corresponding methods and results. J.R.M. obtained funding for 2001 fieldwork on MOR 1130, helped excavate the specimen in 2000 and 2001, and helped write the manuscript.

Corresponding author

Correspondence toThomas D. Carr.

Competing interests

The authors declare no competing financial interests.

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