Abstract Large-scale adaptive radiations might explain the runaway success of a minority of extant vertebrate clades. This hypothesis predicts, among other things, rapid rates of morphological evolution during the early history of major groups, as lineages invade disparate ecological niches. However, few studies of adaptive radiation have included deep time data, so the links between extant diversity and major extinct radiations are unclear. The intensively studied Mesozoic dinosaur record provides a model system for such investigation, representing an ecologically diverse group that dominated terrestrial ecosystems for 170 million years. Furthermore, with 10,000 species, extant dinosaurs (birds) are the most speciose living tetrapod clade. We assembled composite trees of 614–622 Mesozoic dinosaurs/birds, and a comprehensive body mass dataset using the scaling relationship of limb bone robustness. Maximum-likelihood modelling and the node height test reveal rapid evolutionary rates and a predominance of rapid shifts among size classes in early (Triassic) dinosaurs. This indicates an early burst niche-filling pattern and contrasts with previous studies that favoured gradualistic rates. Subsequently, rates declined in most lineages, which rarely exploited new ecological niches. However, feathered maniraptoran dinosaurs (including Mesozoic birds) sustained rapid evolution from at least the Middle Jurassic, suggesting that these taxa evaded the effects of niche saturation. This indicates that a long evolutionary history of continuing ecological innovation paved the way for a second great radiation of dinosaurs, in birds. We therefore demonstrate links between the predominantly extinct deep time adaptive radiation of non-avian dinosaurs and the phenomenal diversification of birds, via continuing rapid rates of evolution along the phylogenetic stem lineage. This raises the possibility that the uneven distribution of biodiversity results not just from large-scale extrapolation of the process of adaptive radiation in a few extant clades, but also from the maintenance of evolvability on vast time scales across the history of life, in key lineages.

Author Summary Animals display huge morphological and ecological diversity. One possible explanation of how this diversity evolved is the "niche filling" model of adaptive radiation—under which evolutionary rates are highest early in the evolution of a group, as lineages diversify to fill disparate ecological niches. We studied patterns of body size evolution in dinosaurs and birds to test this model, and to explore the links between modern day diversity and major extinct radiations. We found rapid evolutionary rates in early dinosaur evolution, beginning more than 200 million years ago, as dinosaur body sizes diversified rapidly to fill new ecological niches, including herbivory. High rates were maintained only on the evolutionary line leading to birds, which continued to produce new ecological diversity not seen in other dinosaurs. Small body size might have been key to maintaining evolutionary potential (evolvability) in birds, which broke the lower body size limit of about 1 kg seen in other dinosaurs. Our results suggest that the maintenance of evolvability in only some lineages explains the unbalanced distribution of morphological and ecological diversity seen among groups of animals, both extinct and extant. Important living groups such as birds might therefore result from sustained, rapid evolutionary rates over timescales of hundreds of millions of years.

Citation: Benson RBJ, Campione NE, Carrano MT, Mannion PD, Sullivan C, Upchurch P, et al. (2014) Rates of Dinosaur Body Mass Evolution Indicate 170 Million Years of Sustained Ecological Innovation on the Avian Stem Lineage. PLoS Biol 12(5): e1001853. https://doi.org/10.1371/journal.pbio.1001853 Academic Editor: Hélène Morlon, Ecole Normale Supérieure, France Received: October 16, 2013; Accepted: March 28, 2014; Published: May 6, 2014 This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Funding: Parts of this project were supported by a Leverhulme Research Grant (to Paul Upchurch) RPG-129. PDM is funded by an Imperial College Junior Research Fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Abbreviations: AICc, Akaike's information criterion for finite sample sizes; Ma, million years; mbl, minimum branch length

Discussion Niche-filling Patterns of Dinosaur Body Size Evolution Patterns of dinosaur body size evolution are consistent with the niche-filling model of adaptive radiation [1],[4],[6]. Early dinosaurs exhibit rapid background rates of body size evolution, and a predominance of temporally rapid, order-of-magnitude shifts between body size classes in the Triassic and Early Jurassic. These shifts reflect radiation into disparate ecological niches such as bulk herbivory in large-bodied sauropodomorphs (e.g., [60]) and thyreophoran ornithischians, herbivory using a complex masticating dentition in small-bodied heterodontosaurids (e.g., [61],[62]), and increasing diversity of macropredation in large theropods (Table 3). Subsequently, rates of body size evolution decreased, suggesting saturation of coarsely defined body size niches available to dinosaurs in terrestrial ecosystems, and increasingly limited exploration of novel body size space within clades. The early burst pattern of dinosaurian body size evolution is substantially weakened when Triassic data are excluded (Figure S1). This suggests that key innovations of Triassic dinosaurs (e.g., [63],[64]), and not the Triassic/Jurassic extinction of their competitors [37], drove the early radiation of dinosaur body sizes [34]. Indeed, phylogenetic patterns indicate that many basic ecomorphological divergences occurred well before the Triassic/Jurassic boundary. It is not clear which innovations allowed dinosaurs to radiate [34], or whether the pattern shown here was part of a larger archosaurian radiation [65]. However, the evolution of rapid growth rates may have been important [64], especially in Sauropodomorpha [66], and the erect stance of dinosaurs and some other archosaurs [34] might have been a prerequisite for body size diversification via increased efficiency/capacity for terrestrial weight support [63]. Maniraptoran theropods are an exception to the overall pattern of declining evolutionary rates through time: exhibiting numerous instances of exceptional body size shifts, maintaining rapid evolutionary rates, and generating high ecological diversity [67],[68], including flying taxa. Although a previous study found little evidence for directional trends of body size increase in herbivorous maniraptoran clades [69], this does not conflict with our observation that some body size shifts in maniraptorans (and other coelurosaurs) coincide with the appearance of craniodental, or other, evidence for herbivory (Table 3; e.g., [67],[68],[70]). Much of our knowledge of Late Jurassic and Early Cretaceous maniraptorans comes from a few well-sampled Chinese Lagerstätten, such as the Jehol biota. Without information from these exceptional deposits, we would have substantially less knowledge of divergence dates and ancestral body sizes among early maniraptorans. However, this is unlikely to bias comparisons between maniraptorans and other groups of dinosaurs for two reasons: (1) these deposits provide equally good information on the existence and affinities of small-bodied taxa in other clades, such as Ornithischia; and (2) exceptional information on early maniraptoran history should bias analyses towards finding an early burst pattern in maniraptorans. Inference of high early rates in Maniraptora would be more likely, due either to concentration of short branch durations at the base of the tree (especially using the “mbl” stratigraphic calibration method), or observation of additional body size diversity at the base of the tree that would remain undetected if sampling was poor. We cannot speculate as to the effects on our analyses of finding comparable Lagerstätten documenting early dinosaur history. However, there is currently little positive evidence that the general patterns of body size evolution documented here are artefactual. Many stratigraphically younger dinosaurs, especially non-maniraptorans, exhibit large body size and had slow macroevolutionary rates, possibly due to scaling of generation times (e.g., [71],[72]). Scaling effects are observed across Dinosauria, but show substantial scatter (non-significant; Figure 2C) within Ornithischia and Sauropodomorpha, consistent with previous suggestions that scaling effects should be weak in dinosaurs because of the life history effects of oviparity [73]. Small dinosaurs (10–50 kg) had the highest evolutionary rates, and rates attenuated only weakly, or not at all, at sizes below 10 kg (Figure S3). This might have been key to maniraptoran diversification from small-bodied ancestors, and also explains the origins of fundamentally new body plans and ecotypes from small-bodied ancestors later in ornithischian history (Iguanodontia, Ceratopsidae; Figure 1). Body Size, Ecological Diversity, and Cenozoic Survival Maniraptora includes Avialae, the only dinosaur clade to frequently break the lower body size limit around 1–3 kg seen in other dinosaurs. It is likely that more niches are available to birds (and mammals) around 100 g in mass [41],[74], so obtaining smaller body sizes might have contributed to the ecological radiation of Mesozoic birds (e.g., [27],[75]). If the K/Pg extinction event was ecologically selective, vigorous ecological diversification may have given maniraptoran lineages a greater chance of survival: Avialae was the only dinosaurian clade to survive, perhaps because of the small body sizes of its members. Although the fossil record of birds is inadequate to test hypotheses of K/Pg extinction selectivity, it is clear that smaller-sized squamates and mammals selectively survived this event [76],[77]. Therefore, our results suggest that rapid evolutionary rates within Maniraptora paved the way for a second great adaptive radiation of dinosaurs in the wake of the K/Pg extinction event: the diversification of neornithine birds [21]. Implications for Adaptive Radiation Theory Our findings complement recent studies of diversification rates in the avian crown group [3],[21], and suggest that birds, the most speciose class of tetrapods, arose from a long evolutionary history of continual ecological innovation. Our most striking finding is of sustained, rapid evolutionary rates on the line leading to birds (i.e., in maniraptorans) for more than 150 Ma, from the origin of dinosaurs until at least the end of the Mesozoic. Rates of evolution declined through time in most dinosaurs. However, this early burst pattern, which characterises the niche-filling model of adaptive radiation [6],[7], does not adequately describe evolution on the avian stem lineage. The recovered pattern of sustained evolutionary rates, and the repeated generation of novel ecotypes, suggests a key role for the maintenance of evolvability, the capacity for organisms to evolve, in the evolutionary success of this lineage. Evolvability might have also played a central role in the evolution of other major groups such as crustaceans [78] and actinopterygians [15], supporting its hypothesised importance in organismal evolution [79]. Rapid evolutionary rates observed during the early evolutionary history of Dinosauria, which decelerated through time in most subclades, indicate that much of the observed body size diversity of dinosaurs was generated by an early burst pattern of trait evolution. However, this pattern becomes difficult to detect when data from early dinosaurian history are not included in analyses (Figure S1), consistent with the observation that deep time data improve model inference in simulations [24]. The pruning of lineages by extinction might also overwrite the signals of ancient adaptive radiation in large neontological datasets. For example, Rabosky et al. [15] recovered slow evolutionary rates at the base of the actinopterygian tree, but the fossil record reveals substantial morphological and taxonomic diversity of extinct basal actinopterygian lineages [80],[81]. Although it has not yet been tested quantitatively, this diversity might have resulted from early rapid rates across Actinopterygii, as observed here across Dinosauria. If our results can be generalised, they suggest that the unbalanced distribution of morphological and ecological diversity among clades results from the maintenance of rapid evolutionary rates over vast timescales in key lineages. These highly evolvable lineages may be more likely to lead to successful modern groups such as birds, whereas other lineages show declining evolutionary rates through time. Declining evolutionary rates in dinosaurian lineages off the line leading to birds indicate large-scale niche saturation. This might signal failure to keep pace with a deteriorating (biotic) environment (the Red Queen hypothesis [82],[83]), with fewer broad-scale ecological opportunities than those favouring the early radiation of dinosaurs. There is strong evidence for Red Queen effects on diversification patterns in Cenozoic terrestrial mammals [22], and it is possible that a long-term failure to exploit new opportunities characterises the major extinct radiations of deep time (and depauperate modern clades), whether or not it directly caused their extinctions.

Acknowledgments We thank Graham Slater, Josef Uyeda, Rich FitzJohn, and Jeremy Beaulieu for discussion. We thank Ronan Allain, John Bird, Stephen Brusatte, Sérgio Cabreira, Jonah Choiniere, Serjoscha Evers, Maria Malabarba, Octavio Mateus, Jay Nair, Attila Õsi, Dennis Parsons, Diego Pol, Stephen Poropat, Toru Sekiya, Virginia Tidwell, Peggy Vincent, John Whitlock, and Thomas Williamson for sharing measurements.

Author Contributions The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: RBJB NEC DCE. Analyzed the data: RBJB. Contributed reagents/materials/analysis tools: RBJB NEC MTC PDM CS PU DCE. Wrote the paper: RBJB NEC MTC PDM CS PU DCE.