Differences between parsimony and Bayesian topologies

In comparing our parsimony and Bayesian phylogenies, the most striking finding is that the two methods produce extremely similar consensus trees. The overall structure of both trees is identical: a basal clade of proceratosaurids, an intermediate grade of small-to-mid-sized tyrannosauroids and a derived clade of very large apex predators. Most of the small details are identical as well: the fairly large Sinotyrannus and Yutyrannus group with proceratosaurids instead of the large-bodied tyrannosaurids; Dilong, Eotyrannus and Xiongguanlong are successively closer outgroups to Tyrannosauridae; Bistahieversor and Appalachiosaurus are non-tyrannosaurids; tyrannosaurids are divided into Albertosaurinae and Tyrannosaurinae subclades; and the long-snouted alioramins are basal tyrannosaurines. These results are encouraging, as they show that the major outline of tyrannosauroid phylogeny is recovered by multiple methods that differ substantially in their starting assumptions, at least when these methods are applied to the same dataset.

There are some differences between our parsimony and Bayesian topologies, however and these deserve further discussion. As outlined above, there are three main differences: the position of Dryptosaurus (non-tyrannosaurid in the parsimony tree, nesting with the alioramin tyrannosaurines in the Bayesian tree), the status of Daspletosaurus (the two species form a monophyletic cluster in the parsimony analysis but are a grade on the line to more derived tyrannosaurines in the Bayesian analysis) and resolution within Tyrannosaurinae (completely resolved in the parsimony analysis, one main polytomy including Lythronax and Teratophoneus in the Bayesian analysis). What is particularly interesting is that the basal position of Dryptosaurus and the monophyly of Daspletosaurus are supported by relatively high Bremer and jackknife values in the parsimony tree, but their alternative placements are supported by relatively high posterior probabilities in the Bayesian tree.

Understanding exactly why parsimony and Bayesian methods produce different results in this case is difficult, as the differences have to do with relatively minor aspects of the topology. However, we note that the most salient differences have to do with the relationships of the oldest and most basal tyrannosaurines. We hypothesize that the conflict reflects, in part, the ~20 million year gap between derived tyrannosaurids and their common ancestor that preceded the transgression of the Western Interior Seaway in North America. This gap reflects a large amount of missing data, in the form of tyrannosauroid taxa that must have been present but are not currently sampled (see further discussion of fossil record biases below). Perhaps the conflicting parts of the phylogeny correspond to clades of closely related species that have long ghost lineages with many missing taxa (e.g., Alioramini, basal Tyrannosaurinae). For example, Tyrannosaurinae almost certainly had a lengthy but unsampled early history in Asia and western North America. There is also potentially a long ghost lineage leading to Dryptosaurus, one of the few tyrannosauroids known from the latest Cretaceous of eastern North America28. Our hypothesis that ghost ranges and biased sampling may be causing conflict among parsimony and Bayesian results can be tested in the future, both as new discoveries fill these poorly sampled portions of tyrannosaur history and with Bayesian evolutionary models that can better take into account uneven sampling.

Rectifying differences in tyrannosauroid phylogenetic studies

One of the most vexing roadblocks in understanding tyrannosauroid evolution has been the discrepancy between our original 2010 phylogeny3 and the alternative study of Loewen et al.13, as these genealogies imply different biogeographic and evolutionary histories. Our integration of these two datasets is an attempt to bridge the gap and produce a novel phylogeny that can be used to study tyrannosauroid evolution.

After assimilating the two datasets we recover a phylogeny that is much more similar to our 2010 cladogram and considerably different from Loewen et al.’s topology. This is true of both our parsimony and Bayesian results. This is likely because we discarded several of Loewen et al.’s characters that we considered problematic. We argue that many of these are redundant with each other because they relate to overall skull proportions (see supplementary information). An over-abundance of these characters may explain why Loewen et al.13 found the long-snouted alioramins to nest outside of the deep-snouted tyrannosaurids and the deep-skulled Bistahieversor to group with derived tyrannosaurines that have a similar skull shape, whereas our phylogeny recovers different results in which major clades are not so cleanly diagnosed by similar skull proportions. If our topology is correct, Loewen et al.’s findings may result from something analogous to the long-noted ‘longirostrine problem’, which causes crocodylomorphs with similar skulls shapes to artefactually group together in phylogenetic analyses when in fact they are distantly related29,30.

Given that parsimony and Bayesian analyses of our dataset return similar results, but that our new phylogeny has key differences with the Loewen et al.13 study, it appears as if data selection (character choice and scorings) are more important drivers of topological differences than is methodology. Aside from the discovery of new specimens, we suggest that future authors pay close attention to character selection and scoring, present detailed rationale for why they have excluded certain published characters or changed scores and ideally work together to come to a joint understanding of the primary data that is input into TNT, Mr Bayes and other software to be used for phylogenetic analysis.

Consensus and conflict in tyrannosauroid phylogeny

Although there are some differences between our trees and the phylogeny of Loewen et al.13 and some differences between the parsimony and Bayesian analyses of our new dataset, we are generally optimistic about the state of consensus in tyrannosauroid phylogenetics. All of these varying analyses, using different character datasets and now different methods, agree on the broad framework of tyrannosauroid genealogy: there is a basal cluster of proceratosaurids, an intermediate grade of species like Dilong and Eotyrannus and a derived group of the largest tyrannosauroids from the latest Cretaceous. This clade of large, derived species is divided into clusters centered on Albertosaurus and Gorgosaurus (Albertosaurinae) and Tyrannosaurus and Daspletosaurus (Tyrannosaurinae). The largest Early Cretaceous tyrannosauroids like Sinotyrannus31 are primitive proceratosaurids, not close relatives of Tyrannosaurus or Albertosaurus. Seeing as these results are now commonly found in recent phylogenetic analyses, we consider them to be a well-supported hypothesis.

Tyrannosauroid body plan evolution

Our new phylogeny illustrates that the characteristic body plan of the colossal latest Cretaceous tyrannosaurids did not develop rapidly, but in a more piecemeal fashion. There is a general increase in body size across tyrannosauroid phylogeny (Figs 1 and 2), features that enabled ever-stronger bite forces evolved incrementally and cranial ornamentation gradually became more elaborate on the line to the very largest tyrannosauroids like T. rex (see expanded discussion in supplementary information).

The basal tyrannosauroids Yutyrannus and Sinotyrannus are early examples of fairly large body size in the group (~8–9 meters long and 1.5 tons in mass12,31), but these taxa are not closely related to the derived latest Cretaceous tyrannosaurids, as they are part of the early-flourishing proceratosaurid radiation and not on the direct line to T. rex and close relatives. Their body plan is also quite different from the characteristic colossal bauplan of the latest Cretaceous apex tyrannosaurids. The skulls of Yutyrannus and Sinotyrannus are shallower and less robust than T. rex and kin, with smaller jaw muscles and thinner teeth, and, at least in Yutyrannus, an elaborate midline cranial crest rather than the prescribed series of circum-orbital cranial ornaments in tyrannosaurids (although some of these ornamental features are present in Yutyrannus, their size, shape and position drastically differ from taxa like T. rex and Albertosaurus). The postcranial skeletons are also quite different, as most notably Yutyrannus has a large and three-fingered arm that does not resemble the withered two-fingered forearm of T. rex and close relatives. With its gaudy midline skull crest, huge external naris and proportionally long arms, Yutyrannus (and probably Sinotyrannus) resemble overgrown versions of Guanlong, not proto-tyrannosaurids.

The peculiar early Early Cretaceous Yutyrannus and Sinotyrannus indicate that tyrannosauroids were capable of evolving moderately large sizes during the middle portion of their evolutionary history. But colossal size (>10 metres in body length, >1.5 tons in mass) came much later, first appearing in the Campanian, ca. 80 million years ago, although this observation is probably clouded by sampling biases (see below). Many of the features so characteristic of the colossal end-Cretaceous taxa—such as a broad U-shaped snout, a ventrally convex maxilla and asymmetrical carinae on the maxillary teeth—make their first appearance in the late Early Cretaceous Xiongguanlong32, which we consider as the earliest taxon to exhibit something of a ‘tyrannosaurid-grade bauplan’ (see supplementary information). With that said, Xiongguanlong does not show any clear signs of developing gigantism, as its body mass is estimated at a modest 170 kg, an order of magnitude lower than tyrannosaurids33.

Tyrannosauroid biogeography

Our new phylogeny helps elucidate the biogeographic history of tyrannosauroids and implies a much different narrative than the topology of Loewen et al.13. They recover a series of tyrannosaurids (albertosaurines and basal tyrannosaurines) from northern Laramidia (western North America) on the line to a derived subclade of southern Laramidian taxa, which they interpret as support for a major biogeographic division between northern and southern faunas during the latest Cretaceous13,34. Both our parsimony and Bayesian phylogenies find no clear division between northern and southern species, which are interspersed with each other and with Asian taxa (Figs 1 and 2). In some cases we find close relationships between taxa that are widely separated latitudinally, such as Nanuqsaurus (Alaska) and Teratophoneus (Utah) in our parsimony analysis. Rather than depicting tyrannosaurids as provincial animals with a highly ordered geographic distribution, our topology suggests that they were dynamic organisms capable of recurrent faunal interchange.

The derived large-bodied tyrannosaurids inhabited both Asia and North America during the final ~20 million years of the Cretaceous. Loewen et al.13 argued for a single dispersal between western North America, which they considered the point of origin for Tyrannosauridae and Asia when global sea levels fell during the late Campanian. Our phylogeny implies more frequent interchange that is not so clearly linked to sea level changes. The placement of the Asian alioramins as basal tyrannosaurines indicates at least one other dispersal episode, prior to the middle Campanian (ca. 80 million years ago, based on the age of the more highly nested Lythronax). Additionally, we find Tyrannosaurus nested within a subclade of tyrannosaurines that otherwise includes two Asian taxa (Tarbosaurus and Zhuchengtyrannus). It is equally parsimonious that the two Asian lineages dispersed from North America independently or that this subgroup originated in Asia and Tyrannosaurus then immigrated to North America. In other words, it may be that T. rex was an invasive migrant species that spread across Laramidia. This may help explain why the latest Maastrichtian North American record is so unusual in yielding only a single large tyrannosaurid species, whereas sympatry of multiple tyrannosaurids is seen in the late Campanian of Alberta and Montana and the Maastrichtian of Asia.

Ultimately, these competing biogeographic scenarios could be tested by more explicit quantitative analysis, such as the likelihood-based techniques employed by Loewen et al.13. We argue, however, that despite the flurry of recent discoveries the tyrannosauroid fossil record is so incomplete (see below) that the results of these analyses may not be robust, as they can only incorporate known taxa and cannot easily compensate for sampling biases.

Fossil record biases and future directions

Tyrannosauroids are the subject of more research and popular interest than most, or perhaps all, other dinosaurs. However, their fossil record is frustratingly incomplete and patchy. Three main biases currently hamper our ability to understand long-term biogeographic and evolutionary patterns in tyrannosauroids. First, there is a gap of at least 20 million years and perhaps up to 45 million years, between the large-bodied latest Cretaceous clade and its sister taxon in which the first whispers of its body plan appear, the late Early Cretaceous Xiongguanlong. Filling this gap is critical to determining where Tyrannosauridae originated and how it dispersed in concert with the extreme sea level fluctuations of the middle Cretaceous.

Second, the diversity of large-bodied tyrannosauroids in the latest Cretaceous of Asia is clearly underestimated, as all but one taxon is Maastrichtian in age. There is high Campanian diversity in North America and long ghost lineages that extend to Asian taxa, suggesting that many tyrannosauroids probably lived in the Campanian of Asia as well, but have yet to be sampled. Finding these taxa will be critical in better understanding the number and nature of interchange events between North America and Asia and how these were affected by sea level change.

Third, we know very little about the tyrannosauroids that lived in Appalachia (eastern North America) during the terminal Cretaceous, as only two species have been recovered from this landmass, despite its large size. These taxa—Appalachiosaurus and Dryptosaurus—are both somewhat basal, non-tyrannosaurid tyrannosauroids17,28 (although our Bayesian analysis suggests that Dryptosaurus may be more derived and within Tyrannosauridae). Future discoveries are needed to assess whether tyrannosaurids proper lived in Appalachia, or whether this microcontinent was a refugium for more primitive tyrannosauroids while the super-sized, derived tyrannosaurids were thriving in Laramidia.

We hold that filling these gaps will be the next big step in tyrannosauroid research, as they may help rectify the differences between competing phylogenies of Tyrannosauroidea, make parsimony and Bayesian analyses more congruent with each other and lead to a breakthrough in our understanding of the biogeographic and evolutionary history of these most famous of dinosaurs.