Some time round about 165 million years ago, the group of small, feathered dinosaurs that we call birds evolved from within the theropod radiation (theropods are the so-called ‘predatory dinosaurs’: the great group that includes animals like Tyrannosaurus and Velociraptor as well as the birds). As anyone reasonably familiar with recent palaeontological discoveries will know, we’re now aware of a large number of fossils that blur and smudge whatever distinction there might have been between ‘dinosaur’ and ‘bird’. Archaeopteryx may or may not be one of the oldest members of the bird lineage, but it’s evident that – when it was alive – it belonged to just one of several lineages of small, long-legged, fully feathered, omnivorous or predatory theropods, all of which possessed a mosaic of ‘bird-like’ and ‘unbird-like’ characters. [T-shirt design shown below available here.]

Indeed, if we look at theropod history across the whole of the Triassic, Jurassic and Cretaceous, we see a gradual, cumulative acquisition of bird-like features, ranging from wishbones and a pneumatised skeleton to complex feathers, a reduced, three-fingered hand, an enlarged sternum (breastbone) and tiny size.

This trend of increasing birdiness is well known and has often been commented on. Allosaurus is more bird-like than Coelophysis, Tyrannosaurus is more bird-like than Allosaurus, Ornithomimus is more bird-like than Tyrannosaurus, Velociraptor is more bird-like than Ornithomimus, and Archaeopteryx is more bird-like than Velociraptor. Incidentally, while this general trend might imply that theropods are a ‘bird factory’ (Holtz 2000) and not much else, remember that evolution is about divergence and diversification, with the umpteen lineages that split off along the way all having complex, intricate and independent histories of their own.

The fact that the non-bird theropods closest to birds are small has long been evident, but is there really a supportable trend of size reduction in theropods along the lineage that led to birds? This idea has been both supported (Sereno 1997, Padian et al. 2001, Turner et al. 2007, Novas et al. 2012, Dececchi & Larsson 2013) and contested (Hone et al. 2005, Sookias et al. 2012), but even those studies that supported this trend looked at just a few parameters, did not combine the data on trends with that on how quickly evolution was occurring, or did not analyse data on anatomy, stratigraphic age and body size simultaneously. Frankly, compiling and running analyses that incorporate all these different lines of data is a gargantuan task. But, with the University of Adelaide’s Mike Lee at the helm, this is exactly what a group of us have just done, and our results appear today in the journal Science (Lee et al. 2014a) (see also Benton 2014). In addition to Mike and myself, the team incorporates Andrea Cau and Gareth Dyke.

By applying Bayesian inference to two different datasets of theropod anatomy (Andrea Cau’s mega-matrix project - the most character-rich dataset yet compiled for theropods - and the so-called TWiG database combined by the AMNH-based Theropod Working Group), we produced results that simultaneously account for phylogenetic position, divergence date, evolutionary rates, body size and other factors as well (Lee et al. 2014a). I’m not going to pretend that I understand all of the underlying mathematics, but if you have a basic concept of what Bayesian inference is – that it involves inferring the probability of a relationship based on the addition of further data – then you can appreciate the methodology underpinning this study. We previously applied Bayesian methods to an analysis of the bird fossil record (Lee et al. 2014b).

The results? As revealed by the title of the paper (and the title of this article), what has emerged is a robust and well-supported model showing a prolonged, directional trend in size reduction in the theropod lineage leading to birds: a trend that is continuous across 50 million years of theropod history, and which shows the animals at successive nodes becoming ever-smaller as we get closer to birds in the phylogeny (Lee et al. 2014a).

The phylogeny we recovered is an essentially ‘standard’ one for large datasets, with major clades diverging in the following order: megalosauroids, allosauroids, tyrannosauroids, ornithomimosaurs, alvarezsauroids, oviraptorosaurs, dromaeosaurids, troodontids, birds (Lee et al. 2014a). Note that, even in those groups conventionally imagined as 'big' (like megalosauroids and allosauroids), the sizes estimated for ancestral species are 'only' in the 100-200 kg ballpark (Lee et al. 2014a), meaning that classic taxa like Megalosaurus and Allosaurus should not be considered typical of the ancestral body size for these groups. Elsewhere in the phylogeny, our depiction of troodontids as closer to birds than to dromaeosaurids is now pretty familiar; it means that Deinonychosauria is not monophyletic. The recognition of a maniraptoran clade that includes oviraptorosaurs, dromaeosaurids, troodontids and birds (and not therizinosaurs and alvarezsauroids) is also looking increasingly familiar; the clade concerned was recently named Pennaraptora by Foth et al. (2014).

Because our results allow us to map the appearance dates of lineages onto the phylogeny, we can see that evolutionary rates across part of the lineage leading to birds occurred much faster than expected compared to the rest of the tree – up to four times faster, in fact (Lee et al. 2014a). This seemingly explains why several groups of tetanuran theropods – allosauroids, tyrannosauroids, compsognathids and others – appear near-simultaneously in the fossil record: it seems that the time intervals between their originations really were very short. Why evolution was occurring so rapidly in these animals remains, of course, an unknown.

So, birds emerged as the ‘end products’ of a sustained, long-term period of miniaturisation. It should be said that the existence of this trend will not be surprising to the vast majority of dinosaur specialists, since the idea that birds and their non-bird maniraptoran relatives are relatively small compared to other coelurosaurs, and that coelurosaurs are generally small relative to other tetanurans, has often been noted. However, confirming this size reduction as part of a grander trend that involves non-coelurosaurs and even non-tetanurans is largely novel, and our results are the most comprehensive and statistically robust produced so far.

What impact might this long history of miniaturisation have had on the anatomy, biology and behaviour of the theropods that were ancestral to birds? In recent years it’s been noted that a number of unusual features are associated with those smaller-bodied theropods that are antecedent to birds in the phylogenetic tree: proportionally short snouts and big brains are present in many of the most bird-like maniraptorans, as are small teeth with reduced serrations. We suggest that these features – inherited by early birds and integral to the behaviours and ecological preferences they practised at the start of their history – were most likely a direct consequence of miniaturisation (Lee et al. 2014a).

Then there’s the fact that, as we get closer to birds in the phylogenetic tree, we see an increasingly elaborate plumage, a more bird-like system of body and hindlimb orientation linked to a shift in the centre of gravity, a stiffer, slimmer tail, and a number of behaviours that involve a degree of climbing (Birn-Jeffery et al. 2012) and gliding (Dyke et al. 2013). All of these features are linked in some way to the evolution of small size, but whether they evolved because size had decreased, or whether they drove the evolution of reduced size is just about impossible to say, especially when all were occurring in concert (Lee et al. 2014a).

The great stereotype about dinosaurs concerns their giant size. But the evolution of bigness was evidently not the case across the whole of the dinosaurian tree. In fact, it was the evolution of the very opposite trend that ultimately led dinosaurs in a wholly new direction, one that allowed their survival and, ultimately, their most successful evolutionary radiation.

Andrea's take on our project can be seen here at his Theropoda blog.

For previous Tet Zoo articles on the evolution and diversity of theropods (including birds), see...

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Benton, M. J. 2014 How birds became birds. Science 345, 508-509.

Birn-Jeffery, A. V., Miller, C. E., Naish, D., Rayfield, E. J., Hone, D. W. E. 2012. Pedal claw curvature in birds, lizards and Mesozoic dinosaurs – complicated categories and compensating for mass-specific and phylogenetic control. PLoS ONE 7(12): e50555. doi:10.1371/journal.pone.0050555

Dececchi, T. A. & Larsson, H. C. E. 2013. Body and limb size dissociation at the origin of birds: uncoupling allometric constraints across a macroevolutionary transition. Evolution 67, 2741-2752.

Dyke, G., de Kat, R., Palmer, C., van der Kindere, J., Naish, D. & Ganapathisubramani, B. 2013. Aerodynamic performance of the feathered dinosaur Microraptor and the evolution of feathered flight. Nature Communications 4, Article number: 2489 doi:10.1038/ncomms3489

Foth, C., Tischlinger, H. & Rauhut, O. W. M. 2014. New specimen of Archaeopteryx provides insights into the evolution of pennaceous feathers. Nature 511, 79-82.

Gatesy, S. M. 1990. Caudofemoral musculature and the evolution of theropod locomotion. Paleobiology 16, 170-186.

Holtz, T. R. 2000. Theropod paleobiology, more than just bird origins. Gaia 15, 1-3.

Hone, D. W. E., Keesey, T. M., Pisani, D. & Purvis, A. 2005. Macroevolutionary trends in the Dinosauria: Cope’s rule. Journal of Evolutionary Biology 18, 587-595.

Lee, M. S. Y., Cau, A., Naish, D. & Dyke, G. J. 2014a. Sustained miniaturization and anatomical innovation in the dinosaurian ancestors of birds. Science 345, 562-565.

- ., Cau, A., Naish, D. & Dyke, G. 2014b. Morphological clocks in paleontology, and a Mid-Cretaceous origin of crown Aves. Systematic Biology 63, 442-449.

Novas, F. E., Ezcurra. M. D., Agnolín, F. L., Pol, D. & Ortíz, R. 2012. New Patagonian Cretaceous theropod sheds light about the early radiation of Coelurosauria. Revista del Museo Argentino de Ciencias Naturales, nueva serie 14, 57-81.

Padian, K., de Ricqlès, A. J. & Horner, J. R. 2001. Dinosaurian growth rates and bird origins. Nature 412, 405-408.

Sereno, P. C. 1997. The origin and evolution of dinosaurs. Annual Review of Earth and Planetary Science 25, 435-489.

Sookias, R. B., Butler, R. J. & Benson, R. B. J. 2012. Rise of dinosaurs reveals major body size transitions are driven by passive processes of trait evolution. Proceedings of the Royal Society B 279, 2180-2187.

Turner, A. H., Pol, D., Clarke, J. A., Erickson, G. M. & Norell, M. A. 2007. A basal dromaeosaurid and size evolution preceding avian flight. Science 317, 1378-1381.