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. 2013 Apr 12;8(4):e59439.
doi: 10.1371/journal.pone.0059439. Print 2013.

Phylogenetic analysis of Thecosomata Blainville, 1824 (holoplanktonic opisthobranchia) using morphological and molecular data

Emmanuel Corse  1 , Jeannine Rampal, Corinne Cuoc, Nicolas Pech, Yvan Perez, André Gilles
Affiliations

Phylogenetic analysis of Thecosomata Blainville, 1824 (holoplanktonic opisthobranchia) using morphological and molecular data

Emmanuel Corse et al. PLoS One. .

Abstract

Thecosomata is a marine zooplankton group, which played an important role in the carbonate cycle in oceans due to their shell composition. So far, there is important discrepancy between the previous morphological-based taxonomies, and subsequently the evolutionary history of Thecosomata. In this study, the remarkable planktonic sampling of TARA Oceans expedition associated with a set of various other missions allowed us to assess the phylogenetic relationships of Thecosomata using morphological and molecular data (28 S and COI genes). The two gene trees showed incongruities (e.g. Hyalocylis, Cavolinia), and high congruence between morphological and 28S trees (e.g. monophyly of Euthecosomata). The monophyly of straight shell species led us to reviving the Orthoconcha, and the split of Limacinidae led us to the revival of Embolus inflata replacing Limacina inflata. The results also jeopardized the Euthecosomata families that are based on plesiomorphic character state as in the case for Creseidae which was not a monophyletic group. Divergence times were also estimated, and suggested that the evolutionary history of Thecosomata was characterized by four major diversifying events. By bringing the knowledge of palaeontology, we propose a new evolutionary scenario for which macro-evolution implying morphological innovations were rhythmed by climatic changes and associated species turn-over that spread from the Eocene to Miocene, and were shaped principally by predation and shell buoyancy.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Different phylogenetic hypothesis of Euthecosomata.
A) The left topology is deduced from Rampal studies which considered two straight shell species groups: Creseidae (Creseis, Hyalocylis, Styliola) and Cavoliniidae composed of two sub families, the Cavoliniinae (Cavolinia Clio and Diacria) and the Cuvierininae (Cuvierina) B) The right topology is deduced from the works of Spoel , and Bé & Gilmer which group all the straight shell species in Cavoliniidae, which is composed of three sub-families Clionae (Clio, Creseis, Hyalocylis, Styliola), Cuvierininae (Cuvierina) and Cavoliniinae (Cavolinia, Diacria). Family and sub-family taxa are indicated by symbols: diamond for Limacinidae; down triangle for Cavoliniidae; square for Creseidae; up triangle for Clionae; hexagon for Cavoliniinae; round for Cuvierininae.
Figure 2
Figure 2. Cladistical analysis of morphological data.
Majority rule consensus tree of 74,840 equally parsimonious tree (CI = 0.816; RI = 0.854). Majority rule consensus values and bootsrap values are respectively shown above internal branches (only values ≥50% are shown). Only synapomorphies presenting a consistency index  = 1 are shown on the branches. Black bars represent the synapomorphy characterized by the corresponding morphological character number and the character state change respectively above and below. Characters coding is presented in Table S1.
Figure 3
Figure 3. Phylogenetic analysis of Thecosomata based on COI data.
We display the topology of the Bayesian tree issued from the COI gene complete data set with “noisy” site (657 base pair) and for each clade, the posterior probability (pp) is indicated, followed by the maximum likelihood bootstrap values (bv). Non supported group (pp<0.5; bv<70%) are indicated by stars. Topological incongruences between Bayesian tree and Maximum likelihood tree are indicated by hyphens. Evolutionary rate is indicated by scale bar.
Figure 4
Figure 4. Phylogenetic analysis of Thecosomata based on partial COI data set.
We display the topology of the Bayesian tree issued from the COI gene data set without “noisy” site ( 607 base pair). For each clade, the maximum likelihood bootstrap values (bv) and the a-Bayes value (av) are indicated. Non supported group (av<0.5; bv<70%) are indicated by stars. Topological incongruences between a-Bayes tree and bootstrap tree are indicated by hyphens. Evolutionary rate is indicated by scale bar.
Figure 5
Figure 5. Phylogenetic analysis of Thecosomata based on 28S molecular data.
We display the topology of the Bayesian tree issued from the 28S gene complete data set with “noisy” sites (1013 base pair). For each clade, the posterior probability (pp) is indicated, followed by the maximum likelihood bootstrap values (bv). Non supported group (pp<0.5; bv<70%) are indicated by stars. The dotted line corresponds to the topological position of L.inflata obtained when the corresponding sequence is added into the data set. Topological incongruences between Bayesian tree and Maximum likelihood tree are indicated by hyphens.
Figure 6
Figure 6. Phylogenetic analysis of Thecosomata based on partial 28S gene data set.
We display the topology of the Bayesian tree issued from 28S gene data set without “noisy” site (888 base pair). For each clade, the maximum likelihood bootstrap values (bv) and the a-Bayes value (av) are indicated. Non supported group (av<0.5; bv<70%) are indicated by stars. Topological incongruences between a-Bayes tree and bootstrap tree are indicated by hyphens. Evolutionary rate is indicated by scale bar.
Figure 7
Figure 7. Evolutionary scenario of Thecosomata.
On the right is denoted a series of fossil records. The names of the four drawn fossils are indicated by asterisks. Colors grouped fossils and living species together according to their closed morphology. The dotted lines characterize the unresolved branching:. Five paleoclimatic events mentioned in the text are also indicated and correspond to Late Paleocene Thermal Maximum (LPTM), Early Eocene Climatic Optimum (EECO), Oi-1 Glaciation (Oi-1), Late Oligocene warming (LOw) and Middle Miocene disruption (MMd) that corresponded to the Langhian/Serravalian boundary. Paleontological estimates correspond to the oldest fossils record from different studies: for Thilea; and for Vaginella Daudin, 1800 Cheilocuspidata Hodgkinson, 1992, Loxobidens Hodgkinson, 1992 and for Euchilotheca Fisher, 1882. See Table 3 for the others fossil references. The older Styliola and Hyalocylis-like fossil was represented by horizontal line on the branch.
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