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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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Bayesian relaxed molecular clock time scale. Chronogram obtained from the analysis of the nucleotide dataset using the CAT-GTR + G mixture model. Numbers in circles at nodes refer to lines of Table 3, and squared boxes represent 95% credibility intervals. Numbers between brackets represent the six calibration constraints implemented as soft bounds. Absolute ages of the geological periods follow Gradstein and Hogg [91].
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Figure 4: Bayesian relaxed molecular clock time scale. Chronogram obtained from the analysis of the nucleotide dataset using the CAT-GTR + G mixture model. Numbers in circles at nodes refer to lines of Table 3, and squared boxes represent 95% credibility intervals. Numbers between brackets represent the six calibration constraints implemented as soft bounds. Absolute ages of the geological periods follow Gradstein and Hogg [91].

Mentions: Detailed results from the molecular dating analyses performed under auto-correlated models of molecular clock relaxation are presented in Table 3. Divergence date estimates varied depending on the methods and datasets used, but were nevertheless consistent between the two programs we used (MCMCTree and PhyloBayes). We generally found more consistency with published estimates for the results obtained with PhyloBayes under the CAT-GTR + G site-heterogeneous mixture model (Table 3) than for the results obtained with the site-homogeneous LG + G / WAG + G and GTR + G models. Our analyses based on the CAT-GTR + G model placed the divergence between turtles and archosaurs around the Permian-Triassic boundary at a mean of 255 Mya (range 274 to 233 Mya), the separation of crocodilians and birds in the Upper Triassic with a mean of 219 Mya (249 to 186 Mya), and the most recent common ancestor (MRCA) of living turtles (corresponding to the separation between Pleurodira and Cryptodira) in the Upper Jurassic with a mean of 157 Mya (207 to 104 Mya) depending on whether amino acids or nucleotides are considered (Table 3). The chronogram obtained from the analysis of the nucleotide dataset using the CAT-GTR + G model is shown in Figure 4.


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)

Bayesian relaxed molecular clock time scale. Chronogram obtained from the analysis of the nucleotide dataset using the CAT-GTR + G mixture model. Numbers in circles at nodes refer to lines of Table 3, and squared boxes represent 95% credibility intervals. Numbers between brackets represent the six calibration constraints implemented as soft bounds. Absolute ages of the geological periods follow Gradstein and Hogg [91].
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Bayesian relaxed molecular clock time scale. Chronogram obtained from the analysis of the nucleotide dataset using the CAT-GTR + G mixture model. Numbers in circles at nodes refer to lines of Table 3, and squared boxes represent 95% credibility intervals. Numbers between brackets represent the six calibration constraints implemented as soft bounds. Absolute ages of the geological periods follow Gradstein and Hogg [91].
Mentions: Detailed results from the molecular dating analyses performed under auto-correlated models of molecular clock relaxation are presented in Table 3. Divergence date estimates varied depending on the methods and datasets used, but were nevertheless consistent between the two programs we used (MCMCTree and PhyloBayes). We generally found more consistency with published estimates for the results obtained with PhyloBayes under the CAT-GTR + G site-heterogeneous mixture model (Table 3) than for the results obtained with the site-homogeneous LG + G / WAG + G and GTR + G models. Our analyses based on the CAT-GTR + G model placed the divergence between turtles and archosaurs around the Permian-Triassic boundary at a mean of 255 Mya (range 274 to 233 Mya), the separation of crocodilians and birds in the Upper Triassic with a mean of 219 Mya (249 to 186 Mya), and the most recent common ancestor (MRCA) of living turtles (corresponding to the separation between Pleurodira and Cryptodira) in the Upper Jurassic with a mean of 157 Mya (207 to 104 Mya) depending on whether amino acids or nucleotides are considered (Table 3). The chronogram obtained from the analysis of the nucleotide dataset using the CAT-GTR + G model is shown in Figure 4.

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