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Phylogenomic analyses support the position of turtles as the sister group of birds and crocodiles (Archosauria).

Chiari Y, Cahais V, Galtier N, Delsuc F - BMC Biol. (2012)

Bottom Line: 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.These 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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institut des Sciences de l'Evolution, UMR5554-CNRS-IRD, Université Montpellier 2, Montpellier, France. yle@yleniachiari.it

ABSTRACT

Background: 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. Genome-scale data have been shown to be useful in resolving other debated phylogenies, but no such adequate dataset is yet available for amniotes.

Results: In 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.

Conclusions: These 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.

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Related in: MedlinePlus

Analyses of substitution saturation at each codon position. Maximum likelihood saturation plots [34] were compared (a) between the complete amino-acid and nucleotide datasets, and (b) between the codon positions of the complete nucleotide dataset. The observed pairwise distances between the 16 taxa were directly computed from sequence alignments, and the corresponding inferred pairwise tree distances calculated from branch lengths of the ML topology. The Y = × line marks the theoretical limit where the number of observed substitutions equals the number of inferred substitutions. The slope of the linear regression indicates the amount of substitution saturation; the smaller the slope, the greater the number of inferred multiple substitutions.
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Figure 2: Analyses of substitution saturation at each codon position. Maximum likelihood saturation plots [34] were compared (a) between the complete amino-acid and nucleotide datasets, and (b) between the codon positions of the complete nucleotide dataset. The observed pairwise distances between the 16 taxa were directly computed from sequence alignments, and the corresponding inferred pairwise tree distances calculated from branch lengths of the ML topology. The Y = × line marks the theoretical limit where the number of observed substitutions equals the number of inferred substitutions. The slope of the linear regression indicates the amount of substitution saturation; the smaller the slope, the greater the number of inferred multiple substitutions.

Mentions: Comparisons of ML-based saturation plots [34] between the amino-acid and the complete nucleotide datasets (Figure 2a) did not reveal clear evidence for global substitutional saturation of the complete nucleotide dataset relative to the amino-acid dataset, despite a slightly lower slope (0.36 versus 0.50, respectively). However, as expected in protein-coding genes conserved at this level of divergence, substitutional saturation was particularly pronounced at the third codon positions (Figure 2b). In cases in which the substitutional saturation of third codon positions was particularly high, excluding this third codon position partition from the dataset would be expected to result in less biased phylogenetic reconstructions. In agreement with this prediction, all ML and Bayesian reconstructions performed on the nucleotide dataset after exclusion of third codon positions provide unambiguous support (BPML = 100; PPBAY = 1.0; PPCAT = 1.0) for regrouping turtles and archosaurs (Table 1). Conversely, ML and Bayesian analyses of concatenated third codon positions using a single GTR + G model returned maximal support (BPML = 100; PPBAY = 1.0) for the topology clustering turtles with crocodilians (Table 1). Only the CAT-GTR + G4 mixture model seemed to be able to deal efficiently with the saturated third codon positions dataset by strongly supporting the turtles + archosaurs clade (PPCAT = 1.0). These analyses indicate that substitutional saturation at third codon positions is so strong in this phylogenomic dataset that it is able to impede phylogenetic reconstruction when inappropriate models of sequence evolution are used.


Phylogenomic analyses support the position of turtles as the sister group of birds and crocodiles (Archosauria).

Chiari Y, Cahais V, Galtier N, Delsuc F - BMC Biol. (2012)

Analyses of substitution saturation at each codon position. Maximum likelihood saturation plots [34] were compared (a) between the complete amino-acid and nucleotide datasets, and (b) between the codon positions of the complete nucleotide dataset. The observed pairwise distances between the 16 taxa were directly computed from sequence alignments, and the corresponding inferred pairwise tree distances calculated from branch lengths of the ML topology. The Y = × line marks the theoretical limit where the number of observed substitutions equals the number of inferred substitutions. The slope of the linear regression indicates the amount of substitution saturation; the smaller the slope, the greater the number of inferred multiple substitutions.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3473239&req=5

Figure 2: Analyses of substitution saturation at each codon position. Maximum likelihood saturation plots [34] were compared (a) between the complete amino-acid and nucleotide datasets, and (b) between the codon positions of the complete nucleotide dataset. The observed pairwise distances between the 16 taxa were directly computed from sequence alignments, and the corresponding inferred pairwise tree distances calculated from branch lengths of the ML topology. The Y = × line marks the theoretical limit where the number of observed substitutions equals the number of inferred substitutions. The slope of the linear regression indicates the amount of substitution saturation; the smaller the slope, the greater the number of inferred multiple substitutions.
Mentions: Comparisons of ML-based saturation plots [34] between the amino-acid and the complete nucleotide datasets (Figure 2a) did not reveal clear evidence for global substitutional saturation of the complete nucleotide dataset relative to the amino-acid dataset, despite a slightly lower slope (0.36 versus 0.50, respectively). However, as expected in protein-coding genes conserved at this level of divergence, substitutional saturation was particularly pronounced at the third codon positions (Figure 2b). In cases in which the substitutional saturation of third codon positions was particularly high, excluding this third codon position partition from the dataset would be expected to result in less biased phylogenetic reconstructions. In agreement with this prediction, all ML and Bayesian reconstructions performed on the nucleotide dataset after exclusion of third codon positions provide unambiguous support (BPML = 100; PPBAY = 1.0; PPCAT = 1.0) for regrouping turtles and archosaurs (Table 1). Conversely, ML and Bayesian analyses of concatenated third codon positions using a single GTR + G model returned maximal support (BPML = 100; PPBAY = 1.0) for the topology clustering turtles with crocodilians (Table 1). Only the CAT-GTR + G4 mixture model seemed to be able to deal efficiently with the saturated third codon positions dataset by strongly supporting the turtles + archosaurs clade (PPCAT = 1.0). These analyses indicate that substitutional saturation at third codon positions is so strong in this phylogenomic dataset that it is able to impede phylogenetic reconstruction when inappropriate models of sequence evolution are used.

Bottom Line: 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.These 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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institut des Sciences de l'Evolution, UMR5554-CNRS-IRD, Université Montpellier 2, Montpellier, France. yle@yleniachiari.it

ABSTRACT

Background: 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. Genome-scale data have been shown to be useful in resolving other debated phylogenies, but no such adequate dataset is yet available for amniotes.

Results: In 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.

Conclusions: These 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.

Show MeSH
Related in: MedlinePlus