Limits...
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.

Show MeSH
Species trees inferred from the 248 individual maximum likelihood (ML) gene trees using a pseudo-ML approach. Maximum pseudo-likelihood for estimating species trees (MP-EST) bootstrap consensus species tree obtained for (a) the amino-acid and (b) the nucleotide dataset. (a) This consensus tree was computed from the species trees estimated by the MP-EST method for 100 bootstrap datasets of the 248 ML gene trees inferred under the LG + G8 model. (b) This consensus tree was computed from the species trees estimated by the MP-EST method for 100 bootstrap datasets of the 248 ML gene trees inferred under the GTR + G8 model. Values at nodes indicate bootstrap percentages obtained with 100 replicates. Note the strong incongruence between the two species trees concerning the position of turtles.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3473239&req=5

Figure 3: Species trees inferred from the 248 individual maximum likelihood (ML) gene trees using a pseudo-ML approach. Maximum pseudo-likelihood for estimating species trees (MP-EST) bootstrap consensus species tree obtained for (a) the amino-acid and (b) the nucleotide dataset. (a) This consensus tree was computed from the species trees estimated by the MP-EST method for 100 bootstrap datasets of the 248 ML gene trees inferred under the LG + G8 model. (b) This consensus tree was computed from the species trees estimated by the MP-EST method for 100 bootstrap datasets of the 248 ML gene trees inferred under the GTR + G8 model. Values at nodes indicate bootstrap percentages obtained with 100 replicates. Note the strong incongruence between the two species trees concerning the position of turtles.

Mentions: Finally, given the fact that the internal branch lengths connecting the main reptiles lineages seemed to be relatively short in trees obtained from concatenated analyses (Figure 1), we also explored the potential influence of the underlying gene-tree heterogeneity created by deep coalescence events, which might lead to statistical inconsistency of concatenation-based methods in the anomaly zone [35,36]. The results obtained using the maximum pseudo-likelihood for estimating species trees (MP-EST) approach showed high consistency with the results of our concatenation-based analyses (Figure 3). Indeed, the species tree reconstructed from the amino-acid ML gene trees unambiguously supported (BP = 100) the grouping of turtles and archosaurs (Figure 3a), whereas the species tree based on nucleotide ML gene trees supported (BP = 87) a conflicting turtles plus crocodilians clade (Figure 3b), as previously shown in concatenation-based analyses using suboptimal models of sequence evolution. In fact, only six amino-acid and three nucleotide ML gene trees were fully compatible with their corresponding species trees. These figures illustrate the large extent of gene-tree heterogeneity in this dataset, which probably reflects the large effect of stochastic error on individual gene-tree inference. We interpret these congruent results between concatenation and species tree inference as good evidence that the source of the statistical inconsistency resulting in the grouping of turtles with crocodiles does not come from potential discordances between gene trees and the species tree, but rather from the influence of substitutional saturation of third codon positions in individual gene-tree inference.


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)

Species trees inferred from the 248 individual maximum likelihood (ML) gene trees using a pseudo-ML approach. Maximum pseudo-likelihood for estimating species trees (MP-EST) bootstrap consensus species tree obtained for (a) the amino-acid and (b) the nucleotide dataset. (a) This consensus tree was computed from the species trees estimated by the MP-EST method for 100 bootstrap datasets of the 248 ML gene trees inferred under the LG + G8 model. (b) This consensus tree was computed from the species trees estimated by the MP-EST method for 100 bootstrap datasets of the 248 ML gene trees inferred under the GTR + G8 model. Values at nodes indicate bootstrap percentages obtained with 100 replicates. Note the strong incongruence between the two species trees concerning the position of turtles.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Species trees inferred from the 248 individual maximum likelihood (ML) gene trees using a pseudo-ML approach. Maximum pseudo-likelihood for estimating species trees (MP-EST) bootstrap consensus species tree obtained for (a) the amino-acid and (b) the nucleotide dataset. (a) This consensus tree was computed from the species trees estimated by the MP-EST method for 100 bootstrap datasets of the 248 ML gene trees inferred under the LG + G8 model. (b) This consensus tree was computed from the species trees estimated by the MP-EST method for 100 bootstrap datasets of the 248 ML gene trees inferred under the GTR + G8 model. Values at nodes indicate bootstrap percentages obtained with 100 replicates. Note the strong incongruence between the two species trees concerning the position of turtles.
Mentions: Finally, given the fact that the internal branch lengths connecting the main reptiles lineages seemed to be relatively short in trees obtained from concatenated analyses (Figure 1), we also explored the potential influence of the underlying gene-tree heterogeneity created by deep coalescence events, which might lead to statistical inconsistency of concatenation-based methods in the anomaly zone [35,36]. The results obtained using the maximum pseudo-likelihood for estimating species trees (MP-EST) approach showed high consistency with the results of our concatenation-based analyses (Figure 3). Indeed, the species tree reconstructed from the amino-acid ML gene trees unambiguously supported (BP = 100) the grouping of turtles and archosaurs (Figure 3a), whereas the species tree based on nucleotide ML gene trees supported (BP = 87) a conflicting turtles plus crocodilians clade (Figure 3b), as previously shown in concatenation-based analyses using suboptimal models of sequence evolution. In fact, only six amino-acid and three nucleotide ML gene trees were fully compatible with their corresponding species trees. These figures illustrate the large extent of gene-tree heterogeneity in this dataset, which probably reflects the large effect of stochastic error on individual gene-tree inference. We interpret these congruent results between concatenation and species tree inference as good evidence that the source of the statistical inconsistency resulting in the grouping of turtles with crocodiles does not come from potential discordances between gene trees and the species tree, but rather from the influence of substitutional saturation of third codon positions in individual gene-tree inference.

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