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Comptes Rendus

Evolution/Évolution
The phylogenetic position of the ‘living fossils’ Neoglyphea and Laurentaeglyphea (Decapoda: Glypheidea)
Comptes Rendus. Biologies, Volume 333 (2010) no. 10, pp. 755-759.

Abstracts

The Glypheidea is a group of lobster-like decapods that appeared in the Triassic and that was thought to be extinct until 1975, when a specimen of the species Neoglyphea inopinata was caught off the Philippines. More recently, in 2005, a specimen of another glypheid species, Laurentaeglyphea neocaledonica, was discovered near New Caledonia. Here, we construct a decapod molecular data set including the two extant glypheid species sequenced from eight nuclear and mitochondrial genes. Our study strongly shows that the two extant genera of glypheids cluster together, and further confirms the status of Glypheidea as a separate infraorder. Moreover the reptantian decapods are divided into two major groups, one including Brachyura, Anomura, and Axiidea, and the other including Astacidea, Polychelida, Achelata, and Glypheidea. Although commonly nicknamed ‘Jurassic shrimps’ and considered as ‘living fossils’, glypheids are therefore a derived decapod lineage.

Les glyphéides sont des décapodes apparus au Trias que l’on pensait éteints jusqu’en 1975, date à laquelle un spécimen de l’espèce Neoglyphea inopinata a été découvert aux Philippines. En 2005, un spécimen d’une autre espèce, Laurentaeglyphea neocaledonica, a été collecté près de la Nouvelle Calédonie. Nous présentons ici un jeu de données moléculaires des décapodes, incluant les deux espèces de glyphéides vivantes et basé sur huit gènes nucléaires et mitochondriaux. Notre étude montre que les deux glyphéides actuelles forment un groupe monophylétique et confirme le statut de sous-ordre pour les Glypheidea. Les Reptantia apparaissent divisés en deux groupes principaux : le premier comprend les Brachyura, Anomura et Axiidea et le second inclut les Astacidea, Polychelida, Achelata et Glypheidea. Bien que surnommées « crevettes du Jurassique » et considérées comme des « fossiles vivants », les glyphéides constituent donc une lignée dérivée de décapodes.

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DOI: 10.1016/j.crvi.2010.08.007
Keywords: Phylogenetics, Reptantia, Achelata, Astacidea New Caledonia
Mot clés : Phylogénie, Reptantia, Achelata, Astacidea, Nouvelle Calédonie

Marie-Catherine Boisselier-Dubayle 1; Céline Bonillo 2; Corinne Cruaud 3; Arnaud Couloux 3; Bertrand Richer de Forges 4; Nicolas Vidal 1

1 UMR 7138, systématique, évolution, adaptation, Muséum national d’histoire naturelle, 43, rue Cuvier, 75005 Paris, France
2 UMS 2700, service de systématique moléculaire, Muséum national d’histoire naturelle, 43, rue Cuvier, 75005 Paris, France
3 Genoscope, centre national de sequençage, 2, rue Gaston-Crémieux, CP5706, 91057 Evry cedex, France
4 Kiwa Consulting, 5, rue Félix Franchette, 98800 Nouméa, New Caledonia
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     author = {Marie-Catherine Boisselier-Dubayle and C\'eline Bonillo and Corinne Cruaud and Arnaud Couloux and Bertrand Richer de Forges and Nicolas Vidal},
     title = {The phylogenetic position of the {\textquoteleft}living fossils{\textquoteright} {\protect\emph{Neoglyphea}} and {\protect\emph{Laurentaeglyphea}} {(Decapoda:} {Glypheidea)}},
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Marie-Catherine Boisselier-Dubayle; Céline Bonillo; Corinne Cruaud; Arnaud Couloux; Bertrand Richer de Forges; Nicolas Vidal. The phylogenetic position of the ‘living fossils’ Neoglyphea and Laurentaeglyphea (Decapoda: Glypheidea). Comptes Rendus. Biologies, Volume 333 (2010) no. 10, pp. 755-759. doi : 10.1016/j.crvi.2010.08.007. https://comptes-rendus.academie-sciences.fr/biologies/articles/10.1016/j.crvi.2010.08.007/

Version originale du texte intégral

1 Introduction

Crustaceans are the fourth most species-rich group of animals on the planet, following insects, chelicerates, and molluscs. Foremost among the crustaceans in number and morphological diversity are the decapods. With nearly 15,000 extant species, they include the well-known crabs (Brachyura), hermit crabs and their relatives (Anomura), shrimps (Dendrobranchiata, Caridea, and Stenopodidea), lobsters (Astacidea, Gebiidea, and Axiidea), and other lesser known groups: Achelata, Polychelida and Glypheidea [1–3].

The Glypheidae Winckler 1883 are a group of lobster-like decapods that first appeared in the Lower Triassic, flourished during the Jurassic, became less abundant in the Cretaceous, and apparently disappeared before the end of the Eocene [4]. Glypheids were therefore thought to be an extinct group until 1975, when a male specimen of the species Neoglyphea inopinata, caught off the Philippines at a depth of 185 meters in 1908 and kept in the collections of the Smithsonian Institution, was described [4]. Subsequent expeditions in 1976, 1980, and 1985, captured additional specimens at the same site, and another specimen was trawled in the Timor Sea. This discovery stimulated new research on the group, and subsequently the glypheid lobsters were recognized as a separate infraorder [5]. More recently, in October 2005, during the EBISCO cruise (MNHN-IRD), a single female specimen of another glypheid species was discovered on a seamount in the Coral Sea, near New Caledonia, at a depth of 400 meters. Nicknamed ‘Jurassic shrimp’, it received some attention from the media [6]. This specimen has been named Laurentaeglyphea neocaledonica in 2006 [7,8].

Although several markers are now available that can resolve deep and shallow relationships within the Decapod Tree of Life [9,10], only four rRNA gene fragments (12S, 16S, 18S and 28S rRNA) have been sequenced from Neoglyphea inopinata. Consequently, the exact phylogenetic position of the Glypheidea is still unresolved [9]. Here, we sequenced four additional protein-coding genes, both mitochondrial and nuclear (cytochrome oxydase I, histone H3, phosphoenolpyruvate carboxykinase and sodium-potassium ATPase α-subunit) from the two extant glypheid species in order to investigate their relationships among decapods.

2 Material and methods

We constructed an expanded decapod molecular data set, which included representatives from Dendrobranchiata, Stenopodidea, Caridea, Brachyura, Anomura, Axiidea, Astacidea, Polychelida, Achelata, and the two extant glypheid species Neoglyphea inopinata and Laurentaeglyphea neocaledonica. The genes sampled are three mitochondrial genes: cytochrome oxydase I (COI), 12S and 16S rRNA, and five nuclear genes: histone H3, 18S and 28S rRNA, phosphoenolpyruvate carboxykinase (PEPCK) and sodium-potassium ATPase α-subunit (NaK).

2.1 Data collection

Table 1 lists the taxa used in the study. All the specimens sequenced for the study are housed in the crustacean collection at the Muséum national d’histoire naturelle in Paris and preserved in 80% ethanol.

Table 1

List of taxa and markers used in this study.

COI 12S 16S H3 18S 28S PEPCK NaK
Dendrobranchiata Penaeoidea Aristeus ssp. ----- HQ211500 HQ241511 HQ241556 HQ241523 HQ241534 EU427212 EU427143
Penaeus ssp. AY781297 EF584003 AF192088 ---- AF186250 AF124597 EU427213 EU427144
Pleocyemata Caridea Crangonoidea Glyphocrangon ssp. HQ241546 HQ241502 HQ241513 HQ241558 HQ241525 HQ241537 EU427242 EU427173
Pandaloidea Heterocarpus ssp. HQ241547 HQ241503 HQ241514 HQ241559 HQ241526 HQ241537 EU427243 EU427174
Plesionika ssp. HQ241552 HQ241507 HQ241519 HQ241564 HQ241530 HQ241541 EU427249 EU427180
Stenopodidea Stenopus ssp. AF125441 ----- DQ079734 DQ079701 DQ079769 DQ079812 EU427247 EU427178
Axiidea Callianassoidea Callianassidae AF436025 ----- DQ079777 DQ079664 DQ079741 DQ079777 EU427236 EU427167
Achelata Palinuroidea Panulirus ssp. AF339470 ----- AF337976 DQ079697 DQ079765 DQ079808 EU427230 EU427161
Puerulus angulatus HQ241554 HQ241509 HQ241521 HQ241566 HQ241532 HQ241543 EU427233 EU427164
Anomura Galatheoidea Munida ssp. HQ241548 HQ241504 HQ241515 HQ241560 HQ241527 HQ241538 EU427188 EU427119
Lomosoidea Lomis hirta AY595672 AY595547 AF436052 DQ079680 AF436013 AY596101 EU427187 EU427118
Paguroidea Coenobita ssp. HQ241545 HQ241501 HQ241512 HQ241557 HQ241524 HQ241535 EU427184 EU427115
Astacidea Nephropoidea Homarus ssp. AF370853 DQ298427 AF370876 DQ079675 AF235971 AY859581 EU427219 EU427150
Nephropsis ssp. HQ241551 HQ241506 HQ241518 HQ241563 HQ241529 HQ241540 EU427221 EU427152
Thaumastocheles ssp. HQ241555 HQ241510 HQ241522 HQ241567 HQ241533 HQ241544 EU427223 EU427154
Brachyura Cancridea Cancer ssp. AF060771 ----- DQ079708 DQ079668 DQ079743 DQ079781 EU427196 EU427127
Portunoidea Portunidae AY616443 AY919085 AJ130811 DQ079669 DQ079744 DQ079782 EU427205 EU427136
Glypheidea Neoglyphea inopinata HQ241549 DQ298431 HQ241516 HQ241561 AY583968 AY583986
Laurentaeglyphea neocaledonica HQ241550 HQ241505 HQ241517 HQ241562 HQ241528 HQ241539 HQ241499 HQ241568
Polychelida Eryonoidea Polycheles ssp. HQ241553 HQ241508 HQ241520 HQ241565 HQ241531 HQ241542 EU427234 EU427165

DNA extraction was performed using the QIAamp DNA Micro Kit commercialized by Qiagen. Amplification and sequencing were performed using the following sets of primers: L1490 and H2198 for COI [11]; 16Sar and 16Sbr for 16S rRNA [12]; H3F1 and H3R1 or H3F2 and H3R2 for Histone H3 [13]; 12S1 and 12S3 [14] or 12SF and 12SR [15] for 12S rRNA; 1F-5R, 3F-18Sbi and 18Sa2.0-9R [16,17] for 18S rDNA; 28SC’1 [18] and 28SC2 or 28SD2 [19] for 28S rDNA; PEPCK for, PEPCK for2, PEPCK rev and PEPCK rev3 [20] for PEPCK; NaK for-b and NaK rev [20] for NaK.

PCR products were sequenced using the BigDyeTerminator V3.1 kit (Applied biosystem) and the ABI3730XL sequencer. Both strands of the PCR products were sequenced. The two strands obtained for each sequence were combined using the BioEdit Sequence Alignment Editor program [21].

The 70 sequences generated for this work have been deposited in GenBank under accession numbers HQ241499-HQ241568.

Nucleotide sequences were aligned by eye. Alignment was straightforward for the protein-coding genes, COI, H3, NaK and PEPCK, resulting in datasets of 666, 330, 534, and 570 base pairs (bp), respectively. Variable regions of the 16S, 18S and 28S genes were difficult to align reliably and were removed from the alignments. The final aligned sequences consisted of 438 bp for 16S, 1869 bp for 18S, 358 bp for 28S, and 364 bp for 12S. The few remaining gaps were treated as missing data in all further analyses. Alignments can be obtained from Marie-Catherine Boisselier.

2.2 Phylogenetic analyses

We performed both separate and combined analyses. We built phylogenies using Maximum Likelihood (ML) and Bayesian methods of inference. ML analyses were performed with RAxML 7.0.4 [22,23], and Bayesian analyses were performed with MrBayes 3.1 [24]. We used eight data partitions in the combined analyses, corresponding to the eight genes here sampled.

Bayesian analyses were performed by running 5,000,000 generations in four chains, saving the current tree every 100 generations, with the model inferred by Modeltest using the AIC criterion [25] applied to each partition (GTR). The last 48,000 trees were used to construct a 50% majority rule consensus tree. For the ML analysis, we used the same eight partitions and performed 1000 bootstrap replicates.

3 Results and discussion

As all recent molecular studies found Dendrobranchiata, Stenopodidea and Caridea to be the most basal decapod infraorders, we used them as outgroups [1,9,10,20,26,27]. The remaining decapods (Reptantia) are divided into two major groups supported by ML BP and Bayesian PP values of 100%, one including Brachyura, Anomura, and Axiidea, and the other including Astacidea, Polychelida, Achelata, and Glypheidea (Fig. 1).

Fig. 1

Bayesian tree obtained from the combined data set (COI, 12S and 16S rRNA, 18S and 28S rRNA, H3, PEPCK and NaK; 5129 bp). Nodes with values are supported by Bayesian posterior probabilities values and ML bootstrap values above 95%.

The phylogenetic position of the Glypheidea has long been debated [5,28–33] and our study is the first molecular one to strongly support the inclusion of Glypheidea within one of the two major reptantian clades.

Our study also strongly shows that the two extant genera of glypheids cluster together. It further confirms the status of Glypheidea as a separate infraorder [5,34], in disagreement with several authors who considered glypheoids as Astacidea [33,35,36].

Among the major clade identified here that includes Astacidea, Polychelida, Achelata, and Glypheidea, the position of the latter is however unresolved. In the ML analysis, Glypheidea is placed as sister-group to Achelata (BP value < 50%, a result also obtained with weak support by Bracken et al. [9]) while the Bayesian analysis places Glypheidea as the sister-group to Achelata plus Polychelida (both forming the ancient Palinura infraorder) with a PP value of 72%.

Glypheids somewhat resemble crayfish or lobsters and are hypothesized to have an astacidean-like habitus (lifestyle) as well as a growth close to that observed for Nephrops norvegicus [34]. They also appear to be close to the Astacidea through their thoracic and abdominal structures, by their mouthparts and gills, and by the presence of gonopods [7]. The presence of a diaeresis on the uropodal exopod, with a spinose and distinct margin is another common feature and a horizontal position of the first pereiopod has been inferred to be a synapomorphy of the Astacura (Glypheoidea plus Astacidea) [32]. On the basis of nodal robustness, our results do not exclude a sister relationship of glypheids with astacideans [5].

Conflict of statement

No conflict of interest for any of the authors.

Acknowledgements

We thank A. Crosnier, R. Cleva and J. Brisset for their help in collection management. This work was supported by the “Consortium national de recherche en génomique”, and the “Service de systématique moléculaire” of the Muséum national d’histoire naturelle (CNRS UMS 2700). It is part of the agreement No. 2005/67 between the Genoscope and the Muséum national d’histoire naturelle on the project “Macrophylogeny of life” directed by Guillaume Lecointre.


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