Science can be pretty exciting. Some days you wake up to new discoveries that offer the opportunity to test your favorite hypotheses and lines of reasoning. It seems some hard data is finally illuminating a most stimulating topic: The evolution from dinosaur arms to bird wings.
Regarding the dinosaur-bird transition, two very exciting ideas are currently floating around. One is that birds are paedomorphic, that is, that their adults evolved to resemble the juvenile morphology of their theropod ancestors (Thulborn 1986). This is a robust conclusion, well supported by recent studies on the evolution of cranial morphology (Bhullar et al 2012).
The other exciting idea stems from the recent description of a juvenile Deinonychus (a very bird-like dinosaur). While only fragments of the arms are preserved, it can be inferred that they were proportionally larger than the adult, and more suited for flapping-like movements (Parsons & Parsons 2015). This suggests that juveniles may have even had some flight capabilities that were lost in the larger (3m) adult . Needless to say, this fits neatly with the notion that paedomorphosis played an important role in the origin of birds and flight itself.
Materials of a juvenile Deinonychus. A proximal portion of the right ulna is available (hidden by superposition). From Parsons & Parsons 2015.
Of course, it would be desirable to count with better juvenile materials, such as a specimen with complete, directly measurable arm bones. Then again, other observations seem consistent, such as the fact the very long-armed Bambiraptor, a close relative of Deinonychus, is probably a juvenile.
Skeleton of Bambiraptor
However, for any theropod species, no research article has been published presenting an ontogenetic series with well-preserved arms, that would demonstrate they are proportionally larger in juveniles than adults. Even so, the idea of a negative allometry (or slower growth of the arm) has been around for a while. Perhaps the first to mention this possibility were Gould and Lewontin (evolutionary scientists that need no introduction) in their classic “spandrels” paper. They used the puny arms of Tyrannosaurus to criticize adaptationist thinking. Gould and Lewontin (1979) stated the following: [italics added by me].
“Fully half the explanatory information accompanying the full-scale Fibreglass Tyrannosaurus at Boston’s Museum of Science reads: ‘Front legs a puzzle : how Tyrannosaurus used its tiny front legs is a scientific puzzle ; they were too short even to reach the mouth. They may have been used to help the animal rise from a lying position.’ (We purposely choose an example based on public impact of science to show how widely habits of the adaptationist programme extend. We are not using glass beasts as straw men; similar arguments and relative emphases, framed in different words, appear regularly in the professional literature.) We don’t doubt that Tyrannosaurus used its diminutive front legs for something. If they had arisen de novo, we would encourage the search for some immediate adaptive reason. But they are, after all, the reduced product of conventionally functional homologues in ancestors (longer limbs of allosaurs, for example). As such, we do not need an explicitly adaptive explanation for the reduction itself. It is likely to be a developmental correlate of allometric fields for relative increase in head and hindlimb size. This non-adaptive hypothesis can be tested by conventional allometric methods (Gould (1974) in general; Lande (1978) on limb reduction) and seems to us both more interesting and fruitful than untestable speculations based on secondary utility in the best of possible worlds”
While possible allometric (unequal) development of the arms was mentioned for Tyrannosaurus, they did not discuss its possible relation with the evolution of carnivorous dinosaurs (theropods) in general, and birds in particular. The topic had laid abandoned for 20 years when, as an undergraduate, I noticed this trend, but not in development (ontogeny). Rather, I saw it in the evolutionary variation of theropod dinosaurs. If we compare different dinosaurs species, smaller species tend to show larger arm proportions. I plotted humerus vs. femur length (femur provides a good proxy for body size in general) and obtained pretty good values (R (r2)=0,87) demonstrating a negative allometric trend in the evolution of theropod arm size. I presented these results at two scientific meetings, and my very fist peer-reviewed article in the (now defunct) monthly news bulletin of the Museum of Natural History of Chile (Vargas 1999, link in the reference).
From Vargas 1999
As a hypothesis for explaining such an intriguing general trend among species, I proposed it to reflect common descent from an ancestor in which the arm grew slower than the body (negative allometry) . A prediction of this developmental hypothesis is that most theropods will show proportionally larger humeri at developmental stages earlier than those showing proportionally smaller humeri. However I also noted that development can evolve, and that some theropod lineages could have lost this pattern, specially ornithomimids, where large forms like Gallimimus bullatus show long arms. I also pointed out that a negative allometry was consistent with the proposal of paedamorphosis for the evolution of long arms at the origin of birds.
However, for many years, evidence from fossil ontogenies remained elusive. Indeed, some discouraging publications were available that described isometric growth (unchanging proportions) in Tyrannosaurids (Currie 2003), discarding Gould and Lewontin’s hypotheses. Similar results were proposed for the basal bird Archaeopteryx, assuming that specimens of different sizes reflect an ontogenetic series, rather than different species (Houck 1990). In any case, no negative allometry is found. Of course, these lineages could have secondarily lost it, but assuming all documented cases are exceptions does not look elegant for any hypothesis.
However, some suggestive evidence did become available from Allosaurus. In this case, an abundance of non-articulated skeletal elements of different ontogenetic stages were available from the Cleveland Lloyd dinosaur quarry, a jumble of bones with a notorious frequency of Allosaurus remains of all ages.
The Cleveland Lloyd Quarry
The age (in years) of a bone’s owner could be determined from growth rings in histological sections. These data showed that, yearly, the circumference of the humerus would increase slower than that of the femur, suggesting a negative allometry of the arm (Bybee et al. 2006). Then again, all bones are mixed; no isolated or articulated skeletons were available, which means humerus vs femur length could not be compared in any specific individual.
“ (..) regression analyses suggest that relative to the length of the femur, the lengths of the humerus, ulna, and tibia increase in length more slowly than isometry predicts” (from Bybee et al. 2006)
This discovery encouraged my lab to do some further analysis of evolutionary variation, which we presented at a scientific meeting (Yury-Yáñez et al. 2009), insisting on our developmental prediction. We emphasized how a negative allometry was present up to birds closest outgroups, to argue for the importance of paedomorphosis in wing evolution. A year afterwards, at another scientific meeting, an interesting discovery was announced: “A New subadult Tyrannosaurus rex and a reassesment of ontogenetic and phylogenetic changes in Tyrannosauroid forelimb proportions”. The abstract indicates the entire forelimb was relatively longer in juveniles (Williams et al. 2010). Unfortunately, no article about this specimen has yet been published.
In 2013, another research article used an extensive dataset to examine limb allometry in theropod evolution (Dececchi and Larsson 2013). They found the exact same negative allometry we found in non-avian theropods, with very similar numerical values (my slope= 0,68 their slope = 0,70). Importantly, they emphasized this trend was lost near the origin of birds, switching to a positive allometry (increasing arm proportions), which is consistent with the absence of negative allometry among Archaeopteryx specimens. Like us, they also noted the trend was lost in the evolution of ornithomimids. However, while a developmental prediction is implicit, this article did not explicitly state that the negative allometry should be found in the ontogeny of most non-avian theropods. They also made no mention of paedomorphosis at bird origins.
From Dececchi and Larsson 2013. Open squares are birds (Avialae), dots are non-avian dinosaurs. Notice both curves tend to intersect at small sizes.
In 2014, another informal datum became available: two “dueling dinosaurs” are being held by an auction house, the articulated fossils of a chasmosaurine ceratopsian locked in battle with a Nannotyranus. It has been argued that Nanotyrannus is actually a Tyrannosaurus juvenile. Importantly, the arms in this specimen were widely commented to be proportionally much larger than an adult Tyrannosaurus.
The dueling Nanotyrannus
And now, yet another spectacular but equally informal datum has come onstage: The discovery of a 3.8 m long, almost complete skeleton of a juvenile Allosaurus which is also set to be sold at an auction. Photographs of the specimen show arms that are very noticeably long, far more than the adult (who attained monster sizes, ranging 9-10 m) . Of course, it could be that the arms have been reconstructed, but why would this be done in such a different proportion from known Allosaurus specimens?
The new specimen of a juvenile Allosaurus, with slender, proportionally long arms
An adult Allosaurus, with stout, proportionally small arms
Of course, as yet there are no formal descriptions of this specimen, or of the dueling Nanotyrannus, so we may still have to wait some more. What is truly concerning is that, since the specimens may end up in private hands, it is unclear if they will ever become available for study by scientists. This is crucial step since it is necessary to confirm these are indeed indeed juvenile dinosaurs (through osteo-histological studies, for instance).
In all, it seems likely that in the near future, we may see published articles that confirm theropods with negative allometric arm growth. This would be a neat example of how the hypothetical-deductive method works in natural history, much as in any field. Differences with the “experimental” sciences are mostly of form, rather than essence. It is also a good example of how development drives evolution. The existence of the well-defined macroevolutionary trend defies explanation of humerus size variations as independent events of adaptation. A common ontogenetic pattern would provide the most straight-forward explanation.
The article by Parsons & Parsons 2015 has declared open season for discussing flight in juvenile non-avian theropods. Locomotory differences between juveniles and adults are a commonplace phenomenon (take for instance, humans) and can be very ancient in the lineage leading to birds. Crocodylians have notably longer, slender limbs as juveniles, and the sauropodomorph Massospondylus displayed marked negative allometry of forelimb growth (Reisz et al 2005). It is possible that, as large-headed hatchlings, many dinosaurs started out being more quadrupedal, before acquiring their derived bipedal locomotion. In forms closer to birds, pennaceous feathers were already present in the arms of basal maniraptora, and asymmetric flight feathers are found in close relatives of Deinonychus such as Microraptor. Mesozoic birds were born with fully formed remiges and are thought to have been immediately capable of flight, and may have also been the case for bird-like dinosaurs. The fact juveniles had larger arms, and that this ontogenetic trend can be traced back to the deep tetanuran roots of birds, should earn an important place for paedomorphosis in the classic discussion on the origin of birds and their flight capabilities.
Bhullar, B. A. S., Marugán-Lobón, J., Racimo, F., Bever, G. S., Rowe, T. B., Norell, M. A., & Abzhanov, A. (2012). Birds have paedomorphic dinosaur skulls.Nature, 487(7406), 223-226.
Bybee PJ, Lee AH, Lamm E. (2006) Sizing the Jurassic Theropod Dinosaur Allosaurus: Assessing Growth Strategy and Evolution of Ontogenetic Scaling of Limbs. Journal of Morphology 267:347–359 (2006)
Currie, P. J. (2003). Allometric growth in tyrannosaurids (Dinosauria: Theropoda) from the Upper Cretaceous of North America and Asia. Canadian Journal of Earth Sciences, 40(4), 651-665.
Gould, S. J., & Lewontin, R. C. (1979). The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proceedings of the Royal Society of London B: Biological Sciences, 205(1161), 581-598
Houck, M. A., Gauthier, J. A., & Strauss, R. E. (1990). Allometric scaling in the Earliest Archaeopteryx lithographica. Science, 247(4939), 195-198.
Parsons WL, Parsons KM (2015) Morphological Variations within the Ontogeny of Deinonychus antirrhopus (Theropoda, Dromaeosauridae). PLoS ONE 10(4): e0121476. doi:10.1371/journal.pone.0121476
Reisz, R. R., Scott, D., Sues, H. D., Evans, D. C., & Raath, M. A. (2005). Embryos of an Early Jurassic prosauropod dinosaur and their evolutionary significance. Science, 309(5735), 761-764.
Thulborn, R. A. (1985). Birds as neotenous dinosaurs. Records of the New Zealand Geological Survey, 9, 90-92.
Vargas A. (1999). The evolution of Arm Size in Theropod Dinosaurs: A Developmental Hypothesis. Noticiario Mensual del Museo Nacional de Historia Natural, Chile. 338:16-19. http://issuu.com/mnhn_cl/docs/nm-338
Williams, S. (2011, March). A new subadult Tyrannosaurus rex and a reassessment of ontogenetic and phylogenetic changes in Tyrannosauroid forelimb proportions. In Geological Society of America Abstracts with Programs(Vol. 43, No. 1, p. 120).
Yury-Yáñez R, Soto-Acuña S., and Vargas A.O. Negative allometry of forelimb size in non-ornithurine Paraves. Ameghiniana 46 (4): 55R