A giant tyrannosaur from the Campanian–Maastrichtian of southern North America and the evolution of tyrannosaurid gigantism

Tyrannosaurid dinosaurs dominated as predators in the Late Cretaceous of Laurasia, culminating in the evolution of the giant Tyrannosaurus rex, both the last and largest tyrannosaurid. Where and when Tyrannosaurini (T. rex and kin) originated remains unclear. Competing hypotheses place tyrannosaurin origins in Asia, or western North America (Laramidia). We report a new tyrannosaurin, Tyrannosaurus mcraeensis, from the Campanian–Maastrichtian Hall Lake Formation of New Mexico, based on a fossil previously referred to T. rex. T. mcraeensis predates T. rex by ~ 6–7 million years, yet rivaled it in size. Phylogenetic analysis recovers T. mcraeensis as sister to T. rex and suggests Tyrannosaurini originated in southern Laramidia. Evolution of giant tyrannosaurs in southern North America, alongside giant ceratopsians, hadrosaurs, and titanosaurs suggests large-bodied dinosaurs evolved at low latitudes in North America.

analysis recovers NMMNH P-3698 as the closest known relative of T. rex, suggesting giant Tyrannosaurini evolved in southern Laramidia.
(Tyrannosaurini is here defined as the last common ancestor of Tarbosaurus baatar and Tyrannosaurus rex and all its descendants).

Etymology
The species name, mcraeensis, refers to the McRae Group of western New Mexico.

Horizon and locality
Uppermost Campanian or lower Maastrichtian of the Hall Lake Formation, McRae Group, NMMNH locality 343, near Kettle Top Butte, Sierra County, New Mexico 21 (Fig. 1A).The site lies 43 m above the base of the Hall Lake Formation.A tuff 33 m below the tyrannosaur site has a U/Pb age of 73.2 ± 0.7 Ma 22 (Fig. 1B).

Description and comparisons
The postorbital of Tyrannosaurus mcraeensis (Fig. 2A-C) is typical of tyrannosaurines 5,12 in bearing a massive cornual boss projecting above the postorbital dorsal margin.The cornual boss is C-shaped as in Tarbosaurus 12 but lacks the strong anteroventral expansion or undercut margin seen in Tarbosaurus and T. rex.The cornual boss lacks the prominent, anteriorly positioned apex above the orbit seen in T. rex, instead being more posteriorly positioned.The postorbital's dorsal margin is arched, as in T. rex 5 .In dorsal view the orbital margin and the body of the postorbital form a wide angle, indicating a posteriorly expanded skull as in Lythronax 14 , Tarbosaurus 12 , and Tyrannosaurus rex 5 .The frontal/prefrontal suture projects forward, whereas it is downturned in T. rex (Fig. 4A).The jugal process is anteroposteriorly expanded, with a convex jugal contact, as in T. rex 5 and T. bataar 12 .A large suborbital process projects forward to constrict the orbit as in Bistahieversor 23 , Teratophoneus 14 , and especially T. rex 5 and Tarbosaurus 12 .
The squamosal (Fig. 2D-F) recalls Tyrannosaurus rex 5 in being elongate in dorsal/ventral view.It is shorter in Tarbosaurus 12 , and especially Albertosaurinae 24 .It differs from the T. rex holotype, where the squamosal is straight (Fig. 4B) in having a strongly downturned end in lateral view; however some specimens of T. rex show this feature (SI1).The quadratojugal process is downturned relative to T. rex 5 or Tarbosaurus 12 and strongly curved.Ventrally, the squamosal bears a deep pneumatic recess.The recess' anterior margin is defined by a transverse bar as in Tarbosaurus; this bar is reduced to a low ridge in T. rex 12 .
The palatine (SI5) is broad, similar to Tarbosaurus bataar 12 but not to the degree seen in Tyrannosaurus rex; the palatine of Albertosaurinae is narrower 24 .This wide palatine contributes to the formation of a broad rostrum as in T. rex and Tarbosaurus.
The dentary (Fig. 3A-C) measures 645 mm from the tip back to the level of the coronoid process; the bone measures 894 mm along the long axis as preserved, however the posteroventral end is broken; it may have measured around 900 mm when complete.By comparison, corresponding measurements for the holotype of Tyrannosaurus rex are 589 and 855 mm; RSM P2523.8, one of if not the largest known T. rex specimens 25 , measures ~ 650 from the tip of the dentary to the coronoid process.Tyrannosaurus mcraeensis therefore overlaps T. rex in size (Fig. 5A), although the holotype is smaller than the largest known T. rex individuals.The dentary has 13 alveoli, a low tooth count uniquely shared with T. rex 5 which typically has 13 dentary alveoli, and rarely 14 or 15 26 alveoli.Zhuchengtyrannus has 15 teeth, Tarbosaurus has 14-15 12,13 ; Daspletosaurus horneri 10 and D. torosus have 17.The first alveolus is smaller than the second, as in other tyrannosaurins.The symphysis is deep, being about 125% the depth of the dentary at mid-length, as in T. rex.The symphysis' anteroventral margin rises up steeply, creating a squared-off chin, again as in T. rex.The dentary's occlusal margin rises up steeply at the back forming a strongly concave dorsal margin, as in other tyrannosaurines 5,[12][13][14] .Unusually, the dentary's posterior end is shallow and upturned; it is deep and typically has a downturned ventral margin in T. rex and other tyrannosaurids 5,14,24 .This condition is unique to T. mcraeensis but approached in Tarbosaurus 5,12 and Zhuchengtyrannus 13 .The angular process projects posteriorly, as in Tarbosaurus and Zhuchengtyrannus 13 but unlike T. rex and other tyrannosaurids, where it projects posteroventrally 5,14,24 .
In dorsal view the tip of the dentary bows outward so that the symphysis forms a broad "U".Similar bowing is present in Tyrannosaurus rex 5,14 and Tarbosaurus, associated with transverse expansion of the rostrum.The dentary tip is straight in Daspletosaurus, Lythronax 14 , Nanuqsaurus 27 and more basal taxa 28 .The dentary and toothrow curve outwards posteriorly, again suggesting transverse expansion of the skull's postorbital region, as in Lythronax 14 , Tarbosaurus, and T. rex 5,12 .
Medially, interdental plates are large and rectangular to triangular, as in other tyrannosaurins 5,13 ; they are smaller in Albertosaurinae 24 and Daspletosaurus 24 .The lingual bar covers the first two alveoli.It is deep anteriorly then narrows posteriorly to half its anterior depth, a condition otherwise seen only in Tyrannosaurus rex 5 .The symphysis is rugose and covered with bumps and grooves, as in other tyrannosaurines.It extends back to the third alveolus, as in Tarbosaurus 12 .In Zhuchengtyrannus 13 and some individuals of T. rex 5 it ends under the fourth alveolus.The symphysis lies above the dentary ventral margin, as in Tarbosaurus 12 and Zhuchengtyrannus 13 ; in T. rex the symphysis projects below the dentary's ventral margin 25 in some, but not all individuals.The bone's lateral surface bears pits and scars suggestive of intraspecific combat.
The triangular splenial (Fig. 3D) resembles other tyrannosaurids 5,12,24 .The tall dorsal process resembles T. rex 12 and Tarbosaurus 12 ; Daspletosaurus 24 has a low dorsal process.The apex is triangular, like Tarbosaurus; in T. rex the apex is usually quadrangular (Fig. 4e).The apex is anteriorly displaced compared to other tyrannosaurids.The ventral margin is straight, and the angular process projects posteriorly, versus posteroventrally in www.nature.com/scientificreports/Tarbosaurus 12 and Tyrannosaurus rex (Fig. 4E).The angular process is deep, as in Tarbosaurus; it is shallow in T. rex 5 .The anteroventral process, beneath the mylohyoid foramen, has a shelf overlapping the dentary, in T. rex it abuts the dentary.The anterior process of the angular (Fig. 3E) is longer and narrower than in Tyrannosaurus rex (Fig. 4F) and more similar to Lythronax and Tarbosaurus.It has a narrow ventral prearticular contact; T. rex has a broad anteroventral flange here.The ventral margin forms a sharp angle between the anterior and posterior processes.
The prearticular (Fig. 3F) is gently curved, versus strongly bent in Tyrannosaurus rex 5 (Fig. 4D) and other tyrannosaurids 12,24 .The articular is T-shaped in dorsal view, versus more triangular in T. rex.In posterior view, the retroarticular process is deep and subrectangular; that of T. rex is wider, and semicircular (SI).
Teeth (Fig. 3; SI) resemble Tyrannosaurus rex 5 in being large, robust, and labiolingually expanded.Tooth crowns have massive apices, as in Tarbosaurus 12 ; T. rex teeth have more pointed, spike-like apices 5 .The apex of the sixth dentary tooth is worn; T. rex tooth wear is often heavy as a result of biting bone 6,29,30 .The labiolingual width of anterior teeth approaches their mesiodistal diameter, as in T. rex; posterior teeth are robust, but more laterally compressed.Both carinae bear serrations.

Phylogenetic analysis
Phylogenetic analyses consistently recover Tyrannosaurus mcraeensis as sister to T. rex (Fig. 5) using either a parsimony-based or Bayesian tip-dated analysis (SI).The two share a reduced tooth count, deep dentary symphysis, posteriorly shallow lingual bar, and large size.T. mcraeensis is furthermore united with the Tarbosaurus + Tyrannosaurus clade by a postorbital with a broad ventral ramus, strongly convex posterior margin, and large suborbital flange, by the strongly concave dentary alveolar margin, and by the laterally bowed mandible.

Discussion
Systematics NMMNH P-3698 was referred to Tyrannosaurus rex 17,19,21 based on size and overall resemblance to T. rex, but this assignment has been questioned 20 .Newly collected material shows that T. mcraeensis differs from T. rex in the shape of the postorbital, squamosal, dentary, prearticular, angular, and articular.The characters that diagnose T. mcraeensis and differentiate it from T. rex are relatively subtle characters relating to the shape and articulation www.nature.com/scientificreports/ of the skull bones, but because T. rex is known from multiple individuals, it is possible to show that T. mcraeensis lies outside of the range of individual variation seen in T. rex (Fig. 6).
Tyrannosaurus rex exhibits a high degree of variation [31][32][33] and specimens assigned to the genus may or may not represent multiple species 31,33,34 .However in each of the diagnostic characters identified here, NMMNH P-3698 is unlike any other specimen referred to T. rex; furthermore each bone has at least one diagnostic character, it is therefore an outlier from all other specimens referred to T. rex, in every element.Neither can the differences between T. rex and T. mcraeensis be explained as ontogenetic, given that the animal matched T. rex in size.It is worth noting that these differences are subtle, but the differences between species are often relatively subtle.Characters diagnosing different species of Daspletosaurus 10,15 tend to be relatively subtle, as are those diagnosing different species of Alioramus 35 .

Age of NMMNH P-3698
Referral of NMMNH P-3698 to Tyrannosaurus rex was also based on the assumption that the Hall Lake Formation is late Maastrichtian aged; but no geological or paleontological evidence supports this assignment.In fact, one of the main arguments for a late Maastrichtian age was the incorrect assumption that Hall Lake dinosaurs could be referred to the late Maastrichtian taxa Torosaurus and Tyrannosaurus rex 19 .The ceratopsid previously referred to Torosaurus is now identified as a distinct genus, Sierraceratops 16 ; as shown here, NMMNH P-3698 is distinct from T. rex.
The dinosaur fauna suggests a latest Campanian or Maastrichtian age.Sierraceratops is similar to species known from the latest Campanian, including Coahuilaceratops magnacuerna 36 , and to Bravoceratops polyphemus from the Javelina Formation of Texas 37, which is probably either latest Campanian or early Maastrichtian.The existence of a titanosaurian sauropod in the Hall Lake Formation has been cited evidence of a late Maastrichtian or 'Lancian' age 19,38 .Titanosaurs appear suddenly in the latest Cretaceous of the American Southwest, suggesting a distinct biogeographic event resulting from their sudden dispersal into North America 39 ; sauropods are therefore a useful biostratigraphic constraint.However, titanosaurs range from just beneath the K-Pg boundary 40 to at least 69 ± 0.9 Ma, i.e. mid-Maastrichtian 40 .Sauropods are unknown from the De-Na-Zin Member of the Kirtland Formation of New Mexico 39 , the top of which is dated to 73.5 Ma 41 , or the Cerro Del Pueblo Formation of Mexico, which is latest Campanian, ~ 73.5-73 Ma 42 .Sauropods therefore appear to immigrate into North America between 73 and 69 Ma.The existence of titanosaurs in the assemblage, therefore, does not reject a latest Campanian or early Maastrichtian age, and given that the sauropod appears higher in section, NMMNH P-3698 could predate the arrival of titanosaurians in North America.Finally, a large hadrosaur femur resembles that of the Campanian-Maastrichtian 42 Edmontosaurus 43 and a large edmontosaurin from the latest Campanian Cerro Del Pueblo Formation 44 in terms of its large size and strongly inturned proximal femoral shaft.The presence of an edmontosaurin is consistent with an age range of latest Campanian to latest Maastrichtian.The dinosaur fauna as a whole is consistent with and suggests either a Campanian to Maastrichtian age.The ceratopsid Sierraceratops also tends to suggest a latest Campanian to early Maastrichtian age.Strikingly, no diagnostic late Maastrichtian dinosaur species are known.www.nature.com/scientificreports/Morphology also suggests Tyrannosaurus mcraeensis is older than T. rex, since it consistently lacks many derived characters characterizing T. rex.Tip-dated phylogenetic analysis recovers NMMNH P-3698 at 69 Ma, slightly younger than implied by the radiometric dates, but still much older than any known T. rex (Fig. 7).
Radiometric dates also point towards a latest Campanian or early Maastrichtian age.U/Pb dating 22 gives an age of 73.2 ± 0.7 Ma for a tuff 9 m above the base of the Hall Lake Formation, and a series of Late Campanian ages for the upper 70 m of the immediately underlying Jose Creek Formation, at 75.2 ± 1.3 Ma, 74.6 ± 0.6 Ma, 74.9 ± 0.7 Ma, and 75.0 ± 1.1 Ma.Although no radiometric dates are found above NMMNH P-3698, a titanosaur is found 108 m above the site, and can be no younger than 66 Ma, i.e. the K-Pg boundary.No hiatus, coal, or other evidence of the K-Pg boundary is visible in the exposed section, suggesting around 150 m of Cretaceous rock overlay the site.Depending on the estimated rate of sedimentation, Tyrannosaurus mcraeensis may therefore have lived between 72.7 and 70.9 Ma (SI), i.e., latest Campanian or earliest Maastrichtian, 5-7 million years before Tyrannosaurus rex.
Overall, three independent lines of evidence-(i) the dinosaur fauna, (ii) the morphology of NMMNH P-3698 itself, and (iii) the age constraints provided by underlying radiometric dates and overlying dinosaur bones suggest an age somewhat older than the latest Maastrichtian, and that the animal predates Tyrannosaurus rex.However, additional radiometric dates, palynostratigraphy, or vertebrate fossils are needed to provide more precise constraints on the age of NMMNH P-3698.
Tyrannosaurus mcraeensis shows several derived characters T. rex does not: an upturned dentary posteroventral margin, a weakly curved prearticular, and an anterior splenial apex (Fig. 4).These characters imply that T. mcraeensis was a side-branch in tyrannosaurin evolution, and would not have been directly ancestral to Tyrannosaurus rex.If so, then at least two giant tyrannosaurids existed concurrently in North America, with another species ultimately giving rise to Tyrannosaurus rex.
The presence of Tyrannosaurus mcraeensis in New Mexico and its phylogenetic position suggest that Tyrannosaurini 14 originated as part of this southern fauna.A southern origin of Tyrannosaurini is further supported by the presence of cf.Tyrannosaurus in the Javelina Formation of Texas 49,50 and T. rex in the latest Maastrichtian North Horn of Utah 7 .Following the appearance of tyrannosaurins in southern Laramidia during the Campanian, one lineage dispersed to Asia, giving rise to Tarbosaurus and Zhuchengtyrannus; another gave rise to Tyrannosaurus, eventually moving north to displace albertosaurines in the Late Maastrichtian.
In an alternative character-matrix 51 , Tyrannosaurus mcraeensis again emerges as sister to T. rex (SI).In this topology, Tarbosaurus and Zhuchengtyrannus are successive outgroups to the T. mcraeensis-T.rex clade.This topology is ambiguous about the origin of Tyrannosaurini, consistent with either two dispersals of Tyrannosaurinae into Asia, or dispersal into Asia, followed by back-dispersal into North America.The difference is due to the poorly known Zhuchengtyrannus acting as a wildcard taxon, clustering either with Tarbosaurus 14 or as sister to the T. rex-Tarbosaurus clade 9,10,15 .The out-of-Asia scenario is dependent on the placement of this uncertain taxon.Resolving these ambiguities requires a better understanding of Asian tyrannosaurs.Similarly, placement of Daspletosaurus spp.along the line leading to Tyrannosaurini 15 would tend to support a northern origin of the Tyrannosaurini.Further study of southern tyrannosaurs such as Bistahieversor and Lythronax can potentially resolve these issues, along with revisions of tyrannosaur phylogeny, but we argue that the appearance of T. rex-like dinosaurs in the Javelina Formation, which appear to be slightly older than T. rex itself, better fits the southern scenario 9,50 .
Tyrannosaurus mcraeensis shows that Tyrannosaurini achieved giant size near the end of the Campanian.It furthermore suggests that they did so in southern Laramidia (Fig. 5) but were initially restricted to southern Laramidia, and later dispersed north 7 .Chasmosaurinae show similar patterns, with giant Triceratopsini evolving in southern Laramidia in the Campanian, then moving into the northern Great Plains in the Maastrichtian 46 .Several other giant dinosaurs evolved in southern Laramidia, including large kritosaurin hadrosaurs 52 , the giant lambeosaurine Magnapaulia laticaudus 53 , and the titanosaurian Alamosaurus sanjuanensis 54 , but did not migrate north.Meanwhile, a tyrannosaurid from northernmost Laramidia, Nanuqsaurus hoglandi 27 , was smaller than tyrannosaurines from farther south.This, and the presence of giant ceratopsians and hadrosaurs in the Hall Lake Formation (SI) implies geographic patterns of body size evolution: large dinosaurs evolved in southern Laramidia.
Sea level changes have been hypothesized to drive tyrannosaurid diversification 14 , and among mammals, land area was found to be associated with body mass of top carnivores and herbivores 55 .However, the patterns raised here suggest that other processes are at work in driving tyrannosaurid size evolution.The evolution of Tyrannosaurus-sized tyrannosaurs appears to precede end-Maastrichtian marine regression by several million years; furthermore the giant tyrannosaurs appear to be initially restricted to a limted area of the relatively small Laramidian landmass.Gigantism therefore appears not to be driven by increases in land area, instead giant theropods evolved despite having relatively small geographic ranges.
Giant tyrannosaurins likely evolved to prey on the giant herbivores found in the south, although the reason for the evolution of large herbivorous dinosaurs-possibly including latitudinal variation in mean annual temperature, primary productivity, or seasonality-remains unknown.These patterns also suggest caution in relying on local dinosaur diversity patterns to study global dinosaur diversity changes preceding the K-Pg extinction.

Materials and methods
We added Tyrannosaurus mcraeensis to an existing character-taxon matrix 14 , adding 10 new characters as well as additional taxa (SI2).Phylogenetic analysis was implemented using cladistic methods and total-evidence estimation of phylogeny and divergence times using the fossilized clock model and birth-death priors under diversified sampling as described by recent authors 56 , with tip-dated estimates of fossil ages from all sampled taxa chosen using a "diversity" strategy to span internal branches.We optimized biogeographic history across the summary tree by classifying species into six areas: Europe, South America, Asia, Appalachia, Northern Laramidia, and Southern Laramidia, the latter two separated by present-day Utah and Colorado as the demarcating boundary.We tested a standard suite of biogeographic models in RASP 57 , selecting the DEC + J model as the best fit, and present the most-likely estimates for ancestral range (Fig. 5B).

Figure 7 .
Figure 7. Stratigraphy and radiometric dates of the basal Hall Lake Formation and top of the underlying Jose Creek Formation.