Reptile & Amphibian Forums

Traditionally turtles are considered anapsids. Recently some morphologists claim that turtles are really diapsids that have become secondarily anapsid. The solid skulls of the turtles are therefore, according to these morphologists, a reversal to the ancestral anapsid condition. In the past I have cited evidence from physiology to refute this claim. Specifically all known diapsids and their descendants (e.g. crocs, lizards, tuatara, snakes, birds) have irreversibly lost ureotelism, meaning that all of these diapsids cannot excrete nitrogenous waste as urea. All diapsids are uricotelic, meaning they excrete their nitrogenous waste primarily as uric acid. Turtles and mammals, however, retain the probably ancestral condition of ureotelism, and they excrete urea. All amniotes are capable of excreting uric acid. In humans, an excessive amount of uric acid can produce the painful condition known as gout. Hence turtles differ from all other diapsids in being ureotelic. It is certainly possible that turtles have undergone reversal in this character as well and returned to ureotelism because of the semi-aquatic habits of most turtles. But such a reversal seem unlikely since crocodilians, though semi-aquatic, has not undergone the same reversal to ureotelism. Crocs in fact still excrete uric acid, although they have also taken advantage of their aquatic habitats by excreting ammonia.

Physiology therefore argues strongly against turtles being diapsids. Dr. Michael Lee of the University of Queensland also claims that the characters used to unite the turtles and diapsids are convergences. Therefore it is surprising that a recently published paper by Rest et al. claims that turtles are diapsids using mtDNA data.

Rest, J.S., J.C. Ast, C.C. Austin, P.J. Waddell, E.A. Tibbets, J.M. Hay, D.P. Mindell. (2003). Molecular systematics of Reptilia and the tuatara mitochondrial genome. Molecular Phylogenetics and Evolution, 29:289-297

Rest et al.'s study is congruent with another claim by Dr. Lee: that snakes are closely related to varanoid lizards, therefore making it all the more surprising. Looking more carefully at their choice of outgroups, however, I believe I have found a potential problem in Rest et al.'s study. In their analysis of the relationship of snakes and lizards, Rest et al. correctly chose the tuatara as the outgroup since the tuatara is almost certainly not a member of the Squamata, to which snakes and lizards belong. Rest et al.'s choice of 2 mammals as the "outgroup" to their "Reptilia" is more problematic. They apparently are influenced by the current cladistic dogma that birds are "reptiles" but that mammals are not "reptiles" even though mammals of course are descendants of the synapsids (a group that is traditionally classified in Reptilia) but excluded from the cladists' "Reptilia" (sensu Gauthier). Monotremes, for example, retain many ancestral reptilian characters, including egg laying.

Rest et al. may also have erred by ASSUMING (again on the basis of cladistic dogma) that the ancestors of the mammals (namely the synapsids) are the first group to have branched off from the Amniota (the all inclusive group that includes birds, mammals and reptiles). Rest et al. therefore assumed that all amniotes other than the mammals and their ancestors form a holophyletic group. If, however, the turtles are in fact anapsids and if the anapsids giving rise to the turtles actually branched off earlier than the synapsids, then Rest et al. may have chosen a member of the ingroup as an outgroup. Evidence that shows they may have done just that is contained in their own paper. The two mammals they chose as "outgroup" form an unresolved polytomy with their "Reptilia." This is of course an anomaly because these two mammals should form a single lineage since all mammals evolved from a single therapsid, but the polytomy suggests that the marsupials and placental mammals evolved from different groups of synapsids!

Rest et al. would probably need to redo their analysis by including an amphibian and probably a fish as outgroups. Until then their data showing turtles as secondarily anapsid descendants of a diapsid reptile is problematic and not reliable. Their data in support of a close relationship between snakes and varanoid lizards, however, is much better because the correct outgroup (Sphenodon) was chosen.

Rest et al.,2003, Molecular systematics of primary reptilian lineages and the tuatara mitochondrial genome, Molecular Phylogenetics and Evolution 29 (2003) 289–297

you can find it here:
http://cis.arl.arizona.edu/PERT/people/Tibbetts/documents/Restetal_000.pdf

Cheers,
Wulf
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http://www.leiopython.de - the white-lipped python site -
http://www.herpers-digest.com - herp related eBooks search -

1. Ureotelism/uricotelism is a relatively conservative character, maybe not an absolutely infallible one. Are you so certain it couldn't have changed twice istead of once? (No need to answer that, surely)

2. Rest et al's assumption that mammals (Synapsida) represent an outgroup to other amniotes (Reptilia) is based not on any particular dogma but on analyses of large data sets by authors such as Gauthier et al. (several papers in 1988) and Laurin and Reisz (1995), references easy to find on the web.

3. The 'unresolved polytomy' at the base of the cladogram is not an anomaly. All standard phylogenetic analyses produce unrooted dendrograms, which are converted to cladograms (or phylogenetic hypotheses) by choosing the position of the root. There is no way that the analysis could identify common ancestry of the two furthest outgroup taxa (unless a different, arbitrary, method of placing the root was used), and hence it is correct that the figure doesn't show it.

4. Adding another, more distant outgroup (any non-amniote, such as an amphibian and/or fish) would let the mammalian group be resolved. And it would, as you say, further test the accepted view that Synapsida and Reptilia are sister groups. We would then be assuming (based on cladistic dogma, or whatever) that Amniota is monophyletic. I wonder where the fish-amphibian outgroup would attach to the cladogram in Rest et al's Fig. 3?

5. Of course, in theory the addition of new 'outgroup' taxa (or new characters) could also change the ingroup relationships. Bayesian analysis produces a lot of high numbers inspiring high confidence that this is the best result for the particular data matrix analysed, but addition of new (independent, e.g. nuclear, morphological etc.) data and new (e.g. fossil) taxa could still overturn the result, particularly at places where internal branches are much shorter than terminal ones.

6. Darwin would have been a cladist if he'd thought of it. T.H. Huxley came pretty close, he had a good eye for patterns of relationship (e.g. trumping Owen on Gorilla brains, and realising that birds were dinosaurs), while Darwin was looking for the process.

7. Many scientists behave badly, but Feduccia has always been wrong about bird origins and by now he must surely know it. The cladists were right again: birds are theropod dinosaurs.
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John D. Scanlon
Riversleigh Fossil Centre
Outback at Isa
Mount Isa, Queensland, Australia
riversleigh@outbackatisa.com.au

1. As I said, all known diapsids have irreversibly lost ureotelism. Diapsids are also uricotelic. But the ability to excrete urea is universal among amniotes (it probably evolved in the amniotic egg as a means to conserve water), so uricotelism is not the synapomorphy of the diapsids and their descendants (the birds). The lost of ureotelism is perhaps a lot like the lost of limbs in tetrapods: in neither case is there evidence that it can re-evolve once it is lost. Therefore the defining synapomorphy of the diapsids (besides the skull openings) is the irreversible lost of ureotelism. Turtles are probably not diapsids because they do not share this synapomorphy.

2. Many of Gauthier's ideas (that the synapsids split off first, that Reptilia should include birds, and that birds are descendants of a highly derived theropod) appear to have become cladistic dogma. Many cladists are defending these ideas using unparsimonious and/or scientifically untenable arguments, such as the idea that feathers may have evolved twice or that flight evolved from the ground up. Some of Gauthier's analyses have been criticized as being based on known symplesiomorphs and are therefore unreliable. Groups that are united on the basis of ancestral characters may be polyphyletic, as Gould pointed out in Wonderful Life.

3. Not so. The two mammalian lineages should form a single lineage. Take a look at Rodriguez-Robles et al.'s (2001, Mol. Phylogenetics and Evol. 18(2):227-237) cladogram, for example. The outgroup species they choose do not form an unresolved polytomy with the rubber boa at the base of the tree, unlike Rest et al.'s study.

4. Adding an amphibian would provide an unequivocal outgroup. It would result in a more robust phylogeny. Right now the choice of two mammals as outgroup may have resulted in the erroneous coding of some molecular synapomorphies as symplesiomorphs. Rest et al. would have eliminated the possibility that they had chosen a member of the ingroup as an outgroup by picking an amphibian (Lissamphibian) as an outgroup, even if they are confident that they did not owing to their belief that Gauthier's original analysis is unchallengeable scientific fact. They may have been tripped up by cladistic dogma.

5. Indeed, if the addition of an amphibian as outgroup changes the ingroup relationships, then turtles may not come out as descendants of a diapsid. If it does not change the topography of the cladogram, then it would lend support to the results. As it stands, the results appear unreliable. Either way, the results would be more reliable if an amphibian is picked as the outgroup.

6. Darwin emphatically rejected cladism when he i) championed character analysis (i.e ascertaining character goodness and homology) and ii) showed with an example how he would classify on the basis of not only branching order but morphological disparity. Darwin showed us how he would delimit taxa so that the resultant taxa may be paraphyletic if the descendants differ greatly from the parental taxa and how he would place the descendants in the same genus as the ancestor if little evolutionary change had taken place in a lineage. The cladists differ from Darwin and the Darwinians by ignoring morphological disparity in their classifications and by their intolerance of paraphyletic taxa.

7. Your declaration that Feduccia is "wrong" is little more than a re-assertion of current cladistic dogma, which has now been disproven by the discovery of Longisquama feathers. The likelihood that feathers evolved twice is even lower than the likelihood that limbs can reappear after it has been lost in a lineage. Feathers unequivocally evolved in the Triassic, well before the bird-like theropods evolved. Gauthier's cladogram requires not only that bird-like dinosaurs evolved not later than the Jurassic and then remain undetected in the fossil record until the late Cretaceous. But since the result of Gauthier's analysis has become cladistic dogma, the cladists will simply ignore the "mountain of evidence" that the opponents of the theropod origin of birds have accumulated in the past few decades. It takes an irrational person to believe that evolution is not a fact. It would take an equally irrational person to believe that birds evolved from a theropod, given the fact that many well preserved theropod skins show no evidence of feathers but the feathers of Longisquama display many of the unmistakable anatomical and developmental details of bird feathers.

Correction:

1. The ability to excrete uric acid is universal among amniotes. Uric acid excretion appears to have originated in the amniotic egg as a means to conserve water.