Noise and biases in genomic data may underlie radically different hypotheses for the position of Iguania within Squamata

Abstract

Squamate reptiles are a major component of vertebrate biodiversity whose crown-clade traces its origin to a narrow window of time in the Mesozoic during which the main subclades diverged in rapid succession. Deciphering phylogenetic relationships among these lineages has proven challenging given the conflicting signals provided by genomic and phenomic data. Most notably, the placement of Iguania has routinely differed between data sources, with morphological evidence supporting a sister relationship to the remaining squamates (Scleroglossa hypothesis) and molecular data favoring a highly nested position alongside snakes and anguimorphs (Toxicofera hypothesis). We provide novel insights by generating an expanded morphological dataset and exploring the presence of phylogenetic signal, noise, and biases in molecular data. Our analyses confirm the presence of strong conflicting signals for the position of Iguania between morphological and molecular datasets. However, we also find that molecular data behave highly erratically when inferring the deepest branches of the squamate tree, a consequence of limited phylogenetic signal to resolve this ancient radiation with confidence. This, in turn, seems to result from a rate of evolution that is too high for historical signals to survive to the present. Finally, we detect significant systematic biases, with iguanians and snakes sharing faster rates of molecular evolution and a similarly biased nucleotide composition. A combination of scant phylogenetic signal, high levels of noise, and the presence of systematic biases could result in the misplacement of Iguania. We regard this explanation to be at least as plausible as the complex scenario of convergence and reversals required for morphological data to be misleading. We further evaluate and discuss the utility of morphological data to resolve ancient radiations, as well as its impact in combined-evidence phylogenomic analyses, with results relevant for the assessment of evidence and conflict across the Tree of Life.

Development of the squamate naso-palatal complex: detailed 3D analysis of the vomeronasal organ and nasal cavity in the brown anole Anolis sagrei (Squamata: Iguania)

“…Nevertheless, members of the Iguania in contrast to the rest of the squamates (Scleroglossa) are characterized by a less developed VNO [ 37 ], lower tongue-flick rate [ 135 ] and lower abundance of vomeronasal and olfactory receptor cells [ 135 ]. The weakly or moderately developed chemosensory abilities in Iguania are difficult to explain, since the phylogenetic position of this group is still a matter of debate [ 50 ]. Such a Sphenodon -like condition may be considered either as plesiomorphy according to morphological studies placing the Iguania as sister to the other squamates (e.g.…”

“…The discordance between the morphological and molecular phylogeny of squamate reptiles and still unresolved phylogenetic position of Iguania [ 50 ] make the study of embryonic development even more important, and potentially useful for phylogenetic inference [ 51 ]. Moreover, there is a lack of substantial studies that consider development of the nasal cavity and VNO in relation to the superficial (soft-tissue) palate.…”

A Total-Evidence Dated Phylogeny of Echinoids and the Evolution of Body Size across Adaptive Landscape

“…Even though tree-independent methods have been criticized (Simmons and Gatesy 2016), TIGER produces rate estimates that have a strong log-linear relationship with those of a tree-based approach (Fig. S9 of SI File 4; see Mongiardino Koch and Gauthier 2018).…”

Phenotypic characters of static homology increase phylogenetic stability under direct optimization of otherwise dynamic homology characters

“…These results support the idea that phenotypic data improve the phylogenetic stability by providing extrinsic and hopefully reasonable constrains for the dynamic homology correspondences (Titus and Frost, 1996). Although some authors might argue that this behaviour illuminates the problems of DO rather than benefits of total‐evidence DO analysis (Simmons et al, 2010; Yoshizawa, 2010), it should be noted that phylogenetic sensitivity to input parameters is by no means restricted to DO approach and phenotypic data can be expected to have similar impact regardless of the analytical method applied (see Mongiardino Koch and Gauthier, 2018). Particularly interesting avenues would be simultaneous dynamic optimization of all character data (for a stimulating discussion on phenotypic data optimization see Vogt, 2018), and the development of more biologically realistic optimizations.…”