Using Genes as Characters and a Parsimony Analysis to Explore the Phylogenetic Position of Turtles

Abstract

The phylogenetic position of turtles within the vertebrate tree of life remains controversial. Conflicting conclusions from different studies are likely a consequence of systematic error in the tree construction process, rather than random error from small amounts of data. Using genomic data, we evaluate the phylogenetic position of turtles with both conventional concatenated data analysis and a “genes as characters” approach. Two datasets were constructed, one with seven species (human, opossum, zebra finch, chicken, green anole, Chinese pond turtle, and western clawed frog) and 4584 orthologous genes, and the second with four additional species (soft-shelled turtle, Nile crocodile, royal python, and tuatara) but only 1638 genes. Our concatenated data analysis strongly supported turtle as the sister-group to archosaurs (the archosaur hypothesis), similar to several recent genomic data based studies using similar methods. When using genes as characters and gene trees as character-state trees with equal weighting for each gene, however, our parsimony analysis suggested that turtles are possibly sister-group to diapsids, archosaurs, or lepidosaurs. None of these resolutions were strongly supported by bootstraps. Furthermore, our incongruence analysis clearly demonstrated that there is a large amount of inconsistency among genes and most of the conflict relates to the placement of turtles. We conclude that the uncertain placement of turtles is a reflection of the true state of nature. Concatenated data analysis of large and heterogeneous datasets likely suffers from systematic error and over-estimates of confidence as a consequence of a large number of characters. Using genes as characters offers an alternative for phylogenomic analysis. It has potential to reduce systematic error, such as data heterogeneity and long-branch attraction, and it can also avoid problems associated with computation time and model selection. Finally, treating genes as characters provides a convenient method for examining gene and genome evolution.

Toward consilience in reptile phylogeny: miRNAs support an archosaur, not lepidosaur, affinity for turtles

“…2), robustly support an archosaur, rather than a lepidosaur, affinity for turtles. Indeed, the latter analysis strongly supports a sister group relationship between crown turtles and crown archosaurs, as do most recent studies addressing amniote interrelationships using gene sequence data (Zardoya and Meyer 1998, Hedges and Poling 1999, Kumazawa and Nishida 1999, Iwabe et al 2005, Shen et al 2011, Tzika et al 2011, Chiari et al 2012, Crawford et al 2012, Fong et al 2012, Shaffer et al 2013, Wang et al 2013, Lu et al 2013). …”

“…Rieppel and deBraga 1996, deBraga and Rieppel 1997, Rieppel and Reisz 1999, Li et al 2008, Lyson et al 2012); and iii), turtles are the sister taxon to, or are nested within, Archosauria (birds and crocodylians; supported mainly by gene-sequence datasets e.g. Zardoya and Meyer 1998, Hedges and Poling 1999, Kumazawa and Nishida 1999, Iwabe et al 2005, Shen et al 2011, Tzika et al 2011, Chiari et al 2012, Crawford et al 2012, Fong et al 2012, Shaffer et al 2013, Wang et al 2013, Lu et al 2013). In the absence of a well-resolved phylogenetic hypothesis for Amniota, outstanding macroevolutionary questions, including those regarding the acquisition of the unique turtle body plan, cannot be adequately addressed.…”

A Middle Triassic stem-turtle and the evolution of the turtle body plan

“…Pappochelys provides new evidence that the plastron partly formed through serial fusion of gastralia 3,13 . Its skull has small upper and ventrally open lower temporal fenestrae, supporting the hypothesis of diapsid affinities of turtles 2,[7][8][9][10]14,15 .…”

“…The origin and early evolution of turtles have long been major contentious issues in vertebrate zoology [1][2][3][4][5][6][7][8][9][10][11] . This is due to conflicting character evidence from molecules and morphology and a lack of transitional fossils from the critical time interval.…”

Zebrin II Is Expressed in Sagittal Stripes in the Cerebellum of Dragon Lizards (<b><i>Ctenophorus </i></b>sp<b><i>.</i></b>)

“…In turtles and snakes, ZII stripes seem to have been lost, as all Purkinje cells are ZII+. Given that recent studies have placed the turtles as a sister group to the archosaurs [Crawford et al, 2012;Fong et al, 2012;Lu et al, 2013], the trait appears to have been lost twice. In a previous report [Aspden et al, 2015], we speculated that loss of ZII stripes in snakes and turtles could result from some simple changes.…”