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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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Phylogenetic relationships of amniotes as inferred from analyses of the 248-gene dataset. (a) Bayesian consensus topology obtained from analyses of the amino-acid dataset (62,342 sites) under the CAT-GTR + G4 mixture model. (b) Bayesian consensus topology obtained from analyses of the complete nucleotide dataset (187,026 sites) under the CAT-GTR + G4 mixture model. The nodal values indicate the clade Bayesian posterior probability (PP). Statistical support values obtained with different methods, models and data partitions detailed in Table 1 are reported in boxes for turtles plus archosaurs. Note the relative incongruence between the two trees concerning the position of Python. All pictures are from Wikimedia Commons, except for Chelonoidis from Y. Chiari. Please note also that the taxonomy of Galapagos turtles being currently revised, the appropriate species name for the Chelonoidis specimen included here might be Chelonoidis sp.
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Figure 1: Phylogenetic relationships of amniotes as inferred from analyses of the 248-gene dataset. (a) Bayesian consensus topology obtained from analyses of the amino-acid dataset (62,342 sites) under the CAT-GTR + G4 mixture model. (b) Bayesian consensus topology obtained from analyses of the complete nucleotide dataset (187,026 sites) under the CAT-GTR + G4 mixture model. The nodal values indicate the clade Bayesian posterior probability (PP). Statistical support values obtained with different methods, models and data partitions detailed in Table 1 are reported in boxes for turtles plus archosaurs. Note the relative incongruence between the two trees concerning the position of Python. All pictures are from Wikimedia Commons, except for Chelonoidis from Y. Chiari. Please note also that the taxonomy of Galapagos turtles being currently revised, the appropriate species name for the Chelonoidis specimen included here might be Chelonoidis sp.

Mentions: 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 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). The same result was obtained from analyses of the complete nucleotide dataset with ML and Bayesian analyses when a mixed model partitioned by codon was applied (BPPARTC = 100; PPPARTC = 1.0), and in Bayesian analyses conducted under the site-heterogeneous CAT-GTR + G4 mixture model (PPCAT = 1.0) (Figure 1b; Table 1). Conversely, ML and Bayesian phylogenetic reconstructions from the complete nucleotide dataset using a single site-homogeneous GTR + G model for the whole concatenation (BPML = 76; PPBAY = 1.0), and a mixed model partitioned by gene (BPPARTG = 54) tended to support an alternative topology grouping turtles with crocodilians (Table 1).


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)

Phylogenetic relationships of amniotes as inferred from analyses of the 248-gene dataset. (a) Bayesian consensus topology obtained from analyses of the amino-acid dataset (62,342 sites) under the CAT-GTR + G4 mixture model. (b) Bayesian consensus topology obtained from analyses of the complete nucleotide dataset (187,026 sites) under the CAT-GTR + G4 mixture model. The nodal values indicate the clade Bayesian posterior probability (PP). Statistical support values obtained with different methods, models and data partitions detailed in Table 1 are reported in boxes for turtles plus archosaurs. Note the relative incongruence between the two trees concerning the position of Python. All pictures are from Wikimedia Commons, except for Chelonoidis from Y. Chiari. Please note also that the taxonomy of Galapagos turtles being currently revised, the appropriate species name for the Chelonoidis specimen included here might be Chelonoidis sp.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Phylogenetic relationships of amniotes as inferred from analyses of the 248-gene dataset. (a) Bayesian consensus topology obtained from analyses of the amino-acid dataset (62,342 sites) under the CAT-GTR + G4 mixture model. (b) Bayesian consensus topology obtained from analyses of the complete nucleotide dataset (187,026 sites) under the CAT-GTR + G4 mixture model. The nodal values indicate the clade Bayesian posterior probability (PP). Statistical support values obtained with different methods, models and data partitions detailed in Table 1 are reported in boxes for turtles plus archosaurs. Note the relative incongruence between the two trees concerning the position of Python. All pictures are from Wikimedia Commons, except for Chelonoidis from Y. Chiari. Please note also that the taxonomy of Galapagos turtles being currently revised, the appropriate species name for the Chelonoidis specimen included here might be Chelonoidis sp.
Mentions: 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 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). The same result was obtained from analyses of the complete nucleotide dataset with ML and Bayesian analyses when a mixed model partitioned by codon was applied (BPPARTC = 100; PPPARTC = 1.0), and in Bayesian analyses conducted under the site-heterogeneous CAT-GTR + G4 mixture model (PPCAT = 1.0) (Figure 1b; Table 1). Conversely, ML and Bayesian phylogenetic reconstructions from the complete nucleotide dataset using a single site-homogeneous GTR + G model for the whole concatenation (BPML = 76; PPBAY = 1.0), and a mixed model partitioned by gene (BPPARTG = 54) tended to support an alternative topology grouping turtles with crocodilians (Table 1).

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