Abstract
BackgroundThe morphological peculiarities of turtles have, for a long time, impeded their accurate placement in the phylogeny of amniotes. Molecular data used to address this major evolutionary question have so far been limited to a handful of markers and/or taxa. These studies have supported conflicting topologies, positioning turtles as either the sister group to all other reptiles, to lepidosaurs (tuatara, lizards and snakes), to archosaurs (birds and crocodiles), or to crocodilians. Genome-scale data have been shown to be useful in resolving other debated phylogenies, but no such adequate dataset is yet available for amniotes.ResultsIn this study, we used next-generation sequencing to obtain seven new transcriptomes from the blood, liver, or jaws of four turtles, a caiman, a lizard, and a lungfish. We used a phylogenomic dataset based on 248 nuclear genes (187,026 nucleotide sites) for 16 vertebrate taxa to resolve the origins of turtles. Maximum likelihood and Bayesian concatenation analyses and species tree approaches performed under the most realistic models of the nucleotide and amino acid substitution processes unambiguously support turtles as a sister group to birds and crocodiles. The use of more simplistic models of nucleotide substitution for both concatenation and species tree reconstruction methods leads to the artefactual grouping of turtles and crocodiles, most likely because of substitution saturation at third codon positions. Relaxed molecular clock methods estimate the divergence between turtles and archosaurs around 255 million years ago. The most recent common ancestor of living turtles, corresponding to the split between Pleurodira and Cryptodira, is estimated to have occurred around 157 million years ago, in the Upper Jurassic period. This is a more recent estimate than previously reported, and questions the interpretation of controversial Lower Jurassic fossils as being part of the extant turtles radiation.ConclusionsThese results provide a phylogenetic framework and timescale with which to interpret the evolution of the peculiar morphological, developmental, and molecular features of turtles within the amniotes.
Highlights
The morphological peculiarities of turtles have, for a long time, impeded their accurate placement in the phylogeny of amniotes
Phylogenetic results Our phylogenomic dataset provides strong support for the phylogenetic position of turtles as a sister group to Archosauria within Amniota based on concatenation analyses (Figure 1)
All of our Bayesian and maximum likelihood (ML) analyses of the concatenated amino-acid dataset recovered this topology with maximal ML bootstrap support (BP) and Bayesian posterior probabilities (PP) irrespective of the model used (BPML = 100; BPPARTG = 100; PPBAY = 1.0; PPCAT = 1.0) (Figure 1a; Table 1)
Summary
The morphological peculiarities of turtles have, for a long time, impeded their accurate placement in the phylogeny of amniotes. Molecular data used to address this major evolutionary question have so far been limited to a handful of markers and/or taxa These studies have supported conflicting topologies, positioning turtles as either the sister group to all other reptiles, to lepidosaurs (tuatara, lizards and snakes), to archosaurs (birds and crocodiles), or to crocodilians. Turtles have been described as having a conspicuously modified reptile body plan, and termed ‘hopeful monsters’, representing a successful phenotypic mutant with the potential to establish a new evolutionary lineage [2,3,4,5,6,7]. Harris et al [17] showed how the morphological characters used to assess the phylogenetic placement of the turtles within the tree of amniotes can lead to conflicting signals, and suggested, given these difficulties, that the answer to this long-standing controversy would most probably come from molecular data
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