Morphology And Molecules Give Fundamentally Conflicting Results For Lizard Phylogeny

Hi Jonathan,
A timely topic and nice perspective. A couple of comments come to mind:
1. Your perspective ends with a pessimistic extrapolation to the whole fossil record, asking if “convergence is so pervasive, what faith can we have in placement of fossil taxa for which no molecular data are available?” I don’t think the discordance is quite that bad. When I recently wrote a similar sort of perspective on turtle origins (BMC Biology 10, no. 64), I mentioned, in contrast, how fortunate were are that the vast majority of studies do not find such strong contradictory signal. Usually there is an independent arbiter such as biogeography that will favor one or the other hypothesis, as in the molecular-supported hypothesis Afrotheria, where the six orders of mammals tie to Africa.

2. Your perspective doesn’t mention that there are morphological traits and biogeographic patterns that support the new molecular phylogeny and not the old morphological tree of squamates. Nicolas Vidal and I have been pointing this out in a series of papers (6-8?) starting in 2004 (slightly before the Townsend et al. paper). By 2005 we already had collected 10 nuclear genes and the phylogeny was getting well-supported, so we erected a new taxonomy of squamates (C. R. Biologies 328:1000-1008)–see http://www.hedgeslab.org for PDFs. See that one for those concordant morphological characters that we suggested. Biogeographically, anguimorph lizards and alethinophidians (typical snakes) each form monophyletic New World and Old World groups in our molecular trees, results contradicted by classical morphological trees. Similar to the Afrotheria case, I would argue that biogeography is the independent evidence suggesting that molecules are probably correct in those cases.

So my point here is that there is not rampant disagreement between molecules and morphology, and when it arises, we can usually and quickly determine which is likely to be correct. Even in the turtle origins case, a particularly prickly one, there has been disagreement among morphologists as to the correct tree (turtles basal or turtles with lepidosaurs), and consistency among molecular trees (turtles with archosaurs), that the odds are that the molecular tree is correct (although I’d prefer to see more taxa in the trees). The same can be said for aspects of the squamate tree, especially since some morphological characters support the molecular tree. Finally, the primary morphological traits supporting the classical squamate tree are associated with feeding (!), a trait system susceptible to convergence and not the first one I would go to for tracking phylogeny. The 44-gene study continues to support the new squamate tree so it really looks convincing at this point.

What if you mix Biogeography (plate tectonics) with ‘frequent’ (put that in an evolutionary/geological time scale) speciation through hybridisation. Just a first thought coming up…

While I think this post and the published Losos et al. piece cover an interesting issue, I find the suggestion “Gauthier et al. ( 2) argues persuasively that we should reconsider whether DNA is always inherently superior for inferring life’s history” quite false. Gauthier et al.’s dataset and analysis are impressive, but their rationale is almost nonexistent. They mention several issues which could cause a discordant signal between morphology and molecules (rooting incorrectly, rate heterogeniety, sampled taxa, etc.), but never show these are the case for squamates. The only squamate data they cite in this way are- “there are indications in both mitochondrial (e.g., Jiang et al. 2007) and nuclear genes (e.g., Hugall et al. 2007) that lizards in general, and snakes and iguanians (especially acrodontans) in particular, display conspicuously high rates of molecular evolution compared to other reptiles.” But they never explain why this would make iguanians clade with the slow evolving anguimorphs to the exclusion of snakes, let alone actually test their idea to form a persuasive argument. And indeed, Douglas and Arnason (2009; not cited by Gauthier et al.) ran models specifically to counter fast evolving sites and still didn’t recover Scleroglossa. This makes their conclusion “we anticipate that imposing the phenotypic tree on the genetic dataset will explain much more of these data than vice versa” more wishful thinking than an evidence-based statement.

All of this is particularly true given other questionable results of Gauthier et al.’s analysis like finding almost all legless taxa clade together as Krypteia, or finding mosasaurs weirdly basal outside Scleroglossa. Yet as noted in the paper, mosasaurs are attracted to snakes if you eliminate the probably convergent limbless fossorial taxa. And when only basal mosasaurs are used, they fall into a more plausible position, but when only derived mosasaurs are used, they stay weirdly basal, which I think is rather good proof the basal position is erroneous and due to the transformed
morphology of highly aquatic taxa. Furthermore, if only derived mosasaurs are
used AND the limbless Anniella and fossorial Sineoamphisbaena are excluded,
krypteians are nested with the fossorial legless skinks Feylinia and Acontias
instead. Surely that’s good evidence snakes are just going by the available legless
fossorial taxa. Gauthier et al. state “When all snake-like squamates (and mosasaurians) are removed from the analysis, and each well-supported fossorial clade is then added independently, Sineoamphisbaena hexatabularis groups with polyglyphanodontians (Figure 13; at least in the 50% majority rule consensus), Anniella pulchra and Pseudopus apodus group with anguids (Figure 14), Feylinia polylepis and Acontias percivali group with skinks (e.g., see Figure 1), and dibamids lie within scincoids on the xantusiid stem.” So most of the taxa go where ‘they’re supposed to’ when other fossorial limbless ones aren’t there to compete. Seems like pretty good evidence Gaithier et al.’s analysis, large as it is, is prone to find convergent taxa group together and thus does not show “the continuing power and importance of morphological and fossil investigation.”

This may be true of morphological analyses in general. Note Livezey and Zusi’s (2006) huge (2954 characters) bird analysis found traditional relationships disputed by molecules (though it lacked most fossils and had tons of coding errors), and Zack’s (2009) large placental analysis including fossils found traditional relationships instead of Afrotheria and such.

References- Douglas and Arnason, 2009. Examining the utility of categorical models and alleviating artifacts in phylogenetic reconstruction of the Squamata (Reptilia). Molecular Phylogenetics and Evolution. 52, 784-796.

Livezey and Zusi, 2006. Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy: I. – Methods and characters. Bulletin of Carnegie Museum of Natural History. 37, 1-544.

Zack, 2009. The phylogeny of eutherian mammals: A new analysis emphasizing dental and postcranial morphology of Paleogene taxa. PhD Thesis. Johns Hopkins University. 628 pp.