Fossil range: Late Jurassic (Oxfordian), 161-155 Ma
| Scientific classification
Limusaurus (meaning "mud lizard") is a genus of toothless herbivorous theropod dinosaur from the Jurassic (Oxfordian stage) Upper Shishugou Formation in the Junggar Basin of Xinjiang in western China.Limusaurus is also the first definitely known ceratosaur from Eastern Asia, including China. The discovery of Limusaurus also suggests that there may have been a land connection between Asia and several other continents allowing for faunal exchange even though the Turgai Sea was previously thought to prohibit such a movement.Limusaurus is also extremely important because previous ceratosaurs were all discovered to be carnivores, making this dinosaur the first herbivorous ceratosaur.
Limusaurus was a small, long-legged dinosaur with short, gracile forelimbs, tiny hands, a slender neck and tail, a short, deep skull, and a slender lower jaw with a down-curved tip. It was toothless, and beak tissue is preserved around its jaw margins.
The type, and only species, L. inextricabilis was described in a 2009 paper coauthored by X. Xu, J. M. Clark, J. Mo, J. Choiniere, C. A. Forster, G. M. Erickson, D. W. E. Hone, C. Sullivan, D. A. Eberth, S. Nesbitt, Q. Zhao, R. Hernandez, C.-K Jia, F.-L. Han, and Y. Guo in the journal Nature. It is known from two sub-adult specimens found in close connection; the holotype, (IVPP V 15923, is an almost complete articulated skeleton, and the other, IVPP V 15924, is a nearly completely articulated specimen only missing the skull. The second specimen is 15% larger than the holotype. A third referred specimen is IVPP V16134. All specimens were young adults when they died, as can be concluded from the extent of bone fusion; from growth lines it was inferred that IVPP V 15924 was in its sixth year when it died.
Limusaurus had a small slender body measuring about 1.7 meters in length. It is the first definite ceratosaur from eastern Asia to be discovered and one of the earliest. Its discovery shows that the Asian dinosaurian fauna was less endemic during the Middle/Late Jurassic period than previously thought and suggests a possible land connection between Asia and other continents during that period.
Limusaurus is a basal ceratosaur that shares many characteristics with coelophysoids and tetanurans. The features present in Limusaurus led to the conclusion that there is a close relationship between the clades Ceratosauria and Tetanurae.
Limusaurus shares several cranial features with other ceratosaurs and coelophysids but display some unique characteristics for the group, such as absence of teeth and the presence of a fully developed beak (rhamphotheca) which have been previously reported in non-avian theropods only among the cretaceous coelurosaurs. It had no teeth, and spaces for blood vessels and nerves in the bones of the jaws that suggest a beak was present. Limusaurus has a long neck, short forelimbs and elongated hindlimbs indicating strong cursorial (running) capabilities. The presence of gastroliths in the stomach of both specimens and the toothless beak indicate a herbivorous diet, making it the earliest and most basal theropod to become adapted to eating plants. The overall aspect of the animal is very similar to that of the Cretaceous ornithomimid theropods, as well as the Triassic non-dinosaurian archosaur Effigia, representing a remarkable case of convergent evolution among these three distinct groups of archosaurs.
Limusaurus was a very basal ceratosaur characterized by hands retaining four digits (I-IV), digit I being strongly reduced. It was traditionally thought that the hands of dinosaurs evolved into the wings of birds by the disappearance of the two outward digits (IV and V), in contradiction with developmental and ontologic studies on birds that showed that the retained digits are the three middle ones (II-III-IV). The hand structure of Limusaurus with its reduced digit I adds more weight to the digit II-III-IV identities for Tetanurae, among which are birds. Previous to the discovery of Limusaurus, theropods were assumed to have progressively evolved reduced digits on the ulnar side of the manus. This concept, known as Lateral Digit Reduction (LDR) is in contrast to Bilateral Digit Reduction (BDR), the reduction on digits on both sides of the hand commonly seen in all other tetrapod groups excluding dinosaurs. However, in Limusaurus, the first digit (Digit I) is strongly reduced, along with other ceratosaurs, suggesting that BDR occurred in their sister group the Tetanurae as well.
Previously, it was thought that digits I-III were retained in tetanurans as a homology with basal theropods, giving credence to the LDR hypothesis. However, the evidence of BDR in Limusaurus suggests that other non-avian theropods may also have exhibited BDR and the apparent digits I-III in tetanurans may actually be digits II-IV, a previous idea considered by Thulborn and Hamley, but largely ignored in the paleontological community.
Limusaurus, while having a reduced metacarpal I, the digit II metacarpal is both robust and twisted, like a ‘classic’ theropod digit I. These features may represent the beginnings of a change; it appears as if the specialized digit I is on the way to being lost and digit II is taking over and adopting the specializations that traditionally make out a digit I. There are also some other similarities in the digits between both basal and derived theropods which when but in the context of this proposed hypothesis do appear to support a II-IV identity of even derived theropod metacarpals.
However, digit IV is reduced significantly in Limusaurus and it is also being observed as reduced in other ceratosaurs and more basal taxa. In order for this hypothesis to be correct therefore, it does require that this digit is secondarily enlarged in later theropods to become a fully functioning digit again.
Furthermore, there are other theropods more derived than Limusaurus that have four functioning digits such as the basal tetanuran Xuanhanosaurus. Other derived theropods also show changes in phalanx number and structure of the digits in the manus. However, this is not necessarily a problem for the new hypothesis in some senses as this variation shows that the hands of theropods are to a degree plastic and can be modified and also some of these transitions are just as much an issue for the I-III hypothesis as they are for the II-IV hypothesis.
Limusaurus is associated with the following evidence:
- The reduction of digit I
- The modification of digit II to resemble that of a traditional digit I
- This corrects for the discrepancy between avian digits and the I-III hypothesis.
- A secondary reacquisition of digit IV as a functioning digit.
Analysis of the phylogenetic analysisEdit
Digit I in Limusaurus and Aucasaurus are highly reduced, with no phalanges. Yet Ceratosaurus shows an articular surface for phalanx I-1, showing the condition in Limusaurus may be derived within ceratosaurs as opposed to a basal ceratosauroid (ceratosaur+tetanurine) state. Furthermore, metacarpal II is medially twisted in Limusaurus, Dilophosaurus and some Coelophysis specimens, similar to metacarpal I in other saurischians. Unfortunately, this is not easily determinable from most figures, so the condition in basal tetanurines is unknown. While Xu et al. note metacarpal III lies ventral to metacarpal II in tetanurines, as metacarpal IV does to III in Limusaurus and coelophysoids, this is also true of metacarpal IV in tetanurines (e.g. Guanlong, as seen in its supplementary information; Tanycolagreus). Similarly, while metacarpal I does not overlap II in non-tetanurines, this is seemingly also true in Xuanhanosaurus and Acrocanthosaurus (overlap is present in "Szechuanoraptor", Megaraptor, Torvosaurus, Allosaurus and Guanlong however).
There is a dorsolateral flange on metacarpal II of Dilophosaurus and Limusaurus which is similar to one on metacarpal I of some tetanurines (e.g. "Szechuanoraptor", Allosaurus, Guanlong). But Xuanhanosaurus and Megaraptor also have such a flange on metacarpal II, but not I, like basal theropods. Both flanges seem to exist in Acrocanthosaurus, while none exist in Aucasaurus and Torvosaurus.
Xu et al. state metacarpal II is more robust than I in non-tetanurine theropods, homologizing it to the robust metacarpal I in tetanurines, but the situation is more complex. It is clearly the size of the base which is important, since even Coelophysis and Dilophosaurus have metacarpal I shafts more robust than those of II. Yet basal tetanurines (e.g. Xuanhanasaurus, "Szechuanoraptor", Torvosaurus, Megaraptor, Acrocanthosaurus, Allosaurus) have metacarpal II more robust than I, while Aucasaurus and Herrerasaurus have the opposite condition. This is true in Xu et al.'s tetanurine example of Guanlong as well, while even their example of Deinonychus has more proximal area and depth on metacarpal II, just less width.
Phalanx I-1 in tetanurines is said to be longer than phalanx I-1 in Herrerasaurus, Dilophosaurus and ceratosaurs, but phalanx I-1 is not preserved in any ceratosaur except for two questionably identified elements in Masiakasaurus. Furthermore, it is not as if any phalanx on digit II in Dilophosaurus or Herrerasaurus is notably more elongate than their phalanx I-1, and some basal tetanurines like Torvosaurus actually have an extremely short phalanx I-1.
Metacarpal II is longest in tetanurines, while III is longest in more basal theropods. Yet Limusaurus and Ceratosaurus resemble tetanurines in this (contrary Xu et al.'s statements and measurements about the former), and Dilophosaurus and Megapnosaurus are polymorphic (e.g. II longer in the paratype of Dilophosaurus, III longer in the holotype).
There is a proximal dorsolateral process on metacarpal III in coelophysoids and Limusaurus, similar to one on metacarpal II in some basal tetanurines like Guanlong. Yet Guanlong also has a process on metacarpal III, which partly covers metacarpal IV, even though the latter is not illustrated in Xu et al.'s paper. Acrocanthosaurus and Allosaurus also have a processes on metacarpal III, while "Szechuanoraptor" lacks processes on metacarpals II or III. This process on metacarpal III of tetanurines could be homologous to the process on III in basal theropods as easily as it could the process on II.
Finally, Xu et al. state metacarpal III in tetanurines is short, slender and proximally triangular like metacarpal IV in basal theropods. Of course, metacarpal IV in tetanurines is also short and slender (even moreso than III), with those of Xuanhanosaurus and "Szechuanoraptor" resembling metacarpal IV in basal theropods more than their metacarpal III does. This is a case where the more reduced metacarpal III in derived tetanurines like Guanlong and Deinonychus (illustrated by Xu et al.) resembles basal theropod metacarpal IV more than metacarpal III in basal tetanurines (e.g. Xuanhanosaurus, "Szechuanoraptor", Torvosaurus, carnosaurs) do, with the thicker shaft and robust distal articulation in the latter taxa. As for their triangular proximal outline, metacarpal IV in Dilophosaurus and Limusaurus are more round than triangular, but "Szechuanoraptor" shows basal tetanurines have triangular metacarpal IV too in any case.
Xu et al. ran a phylogenetic analysis which determined that when characters states are ordered, the resulting tree assuming tetanurines have digits II-III-IV-V is six steps longer than if they are assumed to have digits I-II-III-IV. The length of the unordered trees is equal, but leaving characters unordered potentially leads to ridiculous "intermediate synapomorphies" like coelophysoids and Herrerasaurus being diagnosed by having a single phalanx on digit IV (not more or less) or taxon being diagnosed by having an intermediate ratio, as opposed to relatives with low and high ratios. Furthermore, neither Xuanhanosaurus, "Szechuanoraptor" or Megaraptor were included in their matrix, though these taxa show high homoplasy if II-III-IV-V is assumed, as noted above.
Birds and dinosaursEdit
Digit I appears to have no phalanges and the metacarpal is heavily reduced, digits II and III each have 3, and the number on digit IV is unknown (i.e. the phalangeal formula is 0-3-3-?-X). It therefore appears that Limusaurus has gone the more ‘normal’ route of digit reduction losing V and then reducing I while keeping a reduced IV. Its position right at the base of ceratosaurs suggests that this is not a derived characteristic but one that may be primitive for the ceratosaurs and tetanurans as a whole inherited from a common ancestor. If that is the case then this would mean that the derived theropods we long though had digits I-III actually had digits II-IV, the same as birds.
Embryologists have often (though not always) argued that birds exhibit BDR, such that their tridactyl hands represent digits II, III and IV rather than the I, II and III thought universal among coelurosaurian theropods. Those who contend that birds cannot be theropods have latched on to this as an integral bit of their case. Alan Feduccia in particular has repeatedly said that bird hands and theropod hands are fundamentally different, and that this degree of difference bars theropods from avian ancestry.
The hypothesis that bird hands represent digits II-IV rests mostly on the fact that the primary axis of condensation (the first digit precursor to appear in the embryonic hand) corresponds to digit IV: because bird embryos grow two fingers medial to this axis, these two must be digits III and II. (incidentally, this is contested by some embryologists and is not universally accepted.)
The morphological evidence showing that birds really are theropod dinosaurs is overwhelmingly good, so if birds and other theropods really do have different digit patterns in the hand, something unusual must have occurred during evolution. One idea is that a frame shift occurred: that is, that the condensation axes that originally produced topographical digits II-IV became modified during later development, such that the digits that grew in these places came to resemble topographical digits I-III instead of II-IV. If the frame shift hypothesis is valid, then - somewhere in theropod evolution - the 'true' digit I was lost, and 'true' digit II became digit I. Some evidence from Hox genes provides support for the frame shift hypothesis, as the condensation axis for embryonic digit II receives a Hox signal normally associated with topographical digit I.
Because Limusaurus is basal to Tetanurae (the theropod clade that includes birds and all of the more bird-like theropods), then the digits I-III we see in all tridactyl tetanurans are, after all, topographical digits II-IV, and the frame shift occurred well prior to the origin of birds. If true, this would provide an explanation of the supposed discrepancy that exists between the embryological data and the inferences that palaeontologists have made from fossils.
While topographical digit II of Limusaurus only possesses two phalanges (topographical digit II normally has three, while topographical digit I normally has two), and while metacarpal II in Limusaurus does possess a few subtle features normally seen on metacarpal I (such as a dorsolateral flange), it may just as well be a reduced little hand where all the digits were becoming short and stumpy.
If Limusaurus is deeply nested within Ceratosauria, rather than down at its base, its peculiar hand morphology might - one could argue - be less significant in terms of big-picture implications. More work is needed to sort this out. Xu et al. (2009) analyse a lot of character data, and, while they do report finding Limusaurus to group with at least some noasaurids in at least some analyses (this is in the 101-page-long supplementary data, not in the published paper), they conclude that Limusaurus is close to Elaphrosaurus, and that both are outside of a clade that includes Ceratosaurus and abelisauroids (noasaurids + abelisaurids). This position is only very weakly supported (it hangs on one character).
- ^ New dinosaur gives bird wing clue. BBC News, June 17, 2009.
- ^ a b c d e Xu, X., Clark, J.M., Mo, J., Choiniere, J., Forster, C.A., Erickson, G.M., Hone, D.W.E., Sullivan, C., Eberth, D.A., Nesbitt, S., Zhao, Q., Hernandez, R., Jia, C.-K., Han, F.-L., and Guo, Y. (2009). "A Jurassic ceratosaur from China helps clarify avian digital homologies." Nature, 459(18): 940—944. doi:10.1038/nature08124
- ^ Thulborn, R. A. & Hamley, T. L. 1982. The reptilian relationships of Archaeopteryx. Aust. J. Zool. 30, 611-634
- ^ Burke, A. C. & Feduccia, A. 1997. Development patterns and the identification of homologies in the avian hand. Science 278, 666-668.
- ^ Feduccia, A. 1999. 1,2,3 = 2,3,4: accomodating the cladogram. Proceedings of the National Academy of Sciences 96, 4740-4742.
- ^ Feduccia, A. 2001. Digit homology of birds and dinosaurs: accomodating the cladogram. Trends in Ecology & Evolution 16, 285-286.
- ^ Feduccia, A. 2002. Birds are dinosaurs: simple answer to a complex problem. The Auk 119, 1187-1201.
- ^ Feduccia, A. 2003. Bird origins: problem solved, but the debate continues... Trends in Ecology and Evolution 18, 9-10.
- ^ Feduccia, A. & Nowicki, J. 2002. The hand of birds revealed by early ostrich embryos. Naturwissenschaften 89, 391-393.
- ^ Wagner, G. P. & Gauthier, J. A. 1999. 1,2,3 = 2,3,4: a solution to the problem of the homology of the digits in the avian hand. Proceedings of the National Academy of Sciences 96, 5111-5116.
- ^ Vargas, A. O. & Fallon, J. F. 2005. Birds have dinosaur wings: the molecular evidence. Journal of Experimental Zoology (Mol Dev Evol) 304B, 86-90.
- ^ Vargas, A. O. , Kohlsdorf, T., Fallon, J. F., VandenBrooks, J. & Wagner, G. P. 2008. The evolution of HoxD-11 expression in the bird wing: insights from Alligator mississippiensis. PLoS ONE 3(10): e3325 doi:10.1371/journal.pone.0003325