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EST based phylogenomics of Syndermata questions monophyly of Eurotatoria.

Witek A, Herlyn H, Meyer A, Boell L, Bucher G, Hankeln T - BMC Evol. Biol. (2008)

Bottom Line: Here we present our results from a phylogenomic approach studying i) the phylogenetic position of Syndermata within Spiralia, ii) the monophyletic origin of monogononts and bdelloids and iii) the phylogenetic relations of the latter two taxa to acanthocephalans.Our findings suggest that the phylogenetic position of Syndermata within Spiralia is close to Platyhelminthes, that Eurotatoria are not monophyletic and that bdelloids are more closely related to acanthocephalans than monogononts.Mapping morphological character evolution onto molecular phylogeny suggests the (partial or complete) reduction of the corona and the emergence of a retractable anterior end (rostrum, proboscis) before the separation of Acanthocephala.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Molecular Genetics, Johannes Gutenberg-University Mainz, J. J.-Becherweg 32, D-55099 Mainz, Germany. witeka@uni-mainz.de

ABSTRACT

Background: The metazoan taxon Syndermata comprising Rotifera (in the classical sense of Monogononta+Bdelloidea+Seisonidea) and Acanthocephala has raised several hypotheses connected to the phylogeny of these animal groups and the included subtaxa. While the monophyletic origin of Syndermata and Acanthocephala is well established based on morphological and molecular data, the phylogenetic position of Syndermata within Spiralia, the monophyletic origin of Monogononta, Bdelloidea, and Seisonidea and the acanthocephalan sister group are still a matter of debate. The comparison of the alternative hypotheses suggests that testing the phylogenetic validity of Eurotatoria (Monogononta+Bdelloidea) is the key to unravel the phylogenetic relations within Syndermata. The syndermatan phylogeny in turn is a prerequisite for reconstructing the evolution of the acanthocephalan endoparasitism.

Results: Here we present our results from a phylogenomic approach studying i) the phylogenetic position of Syndermata within Spiralia, ii) the monophyletic origin of monogononts and bdelloids and iii) the phylogenetic relations of the latter two taxa to acanthocephalans. For this analysis we have generated EST libraries of Pomphorhynchus laevis, Echinorhynchus truttae (Acanthocephala) and Brachionus plicatilis (Monogononta). By extending these data with database entries of B. plicatilis, Philodina roseola (Bdelloidea) and 25 additional metazoan species, we conducted phylogenetic reconstructions based on 79 ribosomal proteins using maximum likelihood and bayesian approaches. Our findings suggest that the phylogenetic position of Syndermata within Spiralia is close to Platyhelminthes, that Eurotatoria are not monophyletic and that bdelloids are more closely related to acanthocephalans than monogononts.

Conclusion: Mapping morphological character evolution onto molecular phylogeny suggests the (partial or complete) reduction of the corona and the emergence of a retractable anterior end (rostrum, proboscis) before the separation of Acanthocephala. In particular, the evolution of a rostrum might have been a key event leading to the later evolution of the acanthocephalan endoparasitism, given the enormous relevance of the proboscis for anchoring of the adults to the definitive hosts' intestinal wall.

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Competing phylogenetic hypotheses amongst Syndermata. Cladograms reflecting the competing hypotheses on the phylogenetic relations among Monogononta, Bdelloidea, Acanthocephala and Seisonidea. A Lemniscea hypothesis [23]. B Eurotatoria+Pararotatoria hypothesis [5,9,12]. C Rotifera+Acanthocephala [8,26]. D Eurotatoria+Acanthocephala [28]. E Hemirotifera [29].
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Figure 1: Competing phylogenetic hypotheses amongst Syndermata. Cladograms reflecting the competing hypotheses on the phylogenetic relations among Monogononta, Bdelloidea, Acanthocephala and Seisonidea. A Lemniscea hypothesis [23]. B Eurotatoria+Pararotatoria hypothesis [5,9,12]. C Rotifera+Acanthocephala [8,26]. D Eurotatoria+Acanthocephala [28]. E Hemirotifera [29].

Mentions: The animal taxon Rotifera comprises free-living and commensalic microscopic species of aquatic habitats that are traditionally grouped into the three subtaxa Bdelloidea, Monogononta and Seisonidea [1-3]. Bdelloids (about 460 species) inhabit freshwater, are capable of anhydrobiosis and reproduce strictly by parthenogenesis. Monogononts (about 1,570 species) live in limnic, brackish and marine waters and have a lifecycle with alternating phases of parthenogenetic and sexual reproduction. Thirdly, at least two of the hitherto three described species belonging to Seisonidea are epibionts on marine crustaceans of the genus Nebalia [3,4]. Though Bdelloidea, Monogononta and Seisonidea are subsumed as Rotifera or Rotatoria, the eponymous rotatory organ or corona, a seemingly rotating assembly of cilia at the anterior end of the animal, is absent in Seisonidea. For this and other reasons Bdelloidea and Monogononta are often regarded as sistergroups of a taxon named Eurotatoria [2,5,6]. In contrast to Bdelloidea, Monogononta and Seisonidea, the Acanthocephala are obligatory endoparasites with a complicated lifecycle. Their definite hosts are vertebrates, while their intermediate hosts are insects, chilopods and crustaceans (e.g., Meyer [7]). Along with the endoparasitic life cycle, the acanthocephalan subtaxa share a plethora of derived morphological characters (e.g., [8-11]) so that the monophyly of Acanthocephala as a whole has never been debated. Moreover, the grouping of Acanthocephala, Bdelloidea, Monogononta and Seisonidea into the taxon Syndermata is widely accepted due to special features in epidermal and sperm ultrastructure (e.g., syncytial epidermis, spermatozoon with anteriorly inserted cilium; see [5,8,9,12,13]), as well as congruent results from molecular approaches [14-20]. It is further undisputed that Syndermata are part of a more comprehensive monophylum called Gnathifera [9,21,22]. On the other hand, the phylogenetic position of Syndermata beyond Gnathifera as well as the relationships among the syndermatan subtaxa Acanthocephala, Bdelloidea, Monogononta and Seisonidea are still unresolved. So far, five competing hypotheses on the internal phylogeny of Syndermata have been suggested (Fig. 1A–E). The Lemniscea hypothesis goes back to Lorenzen [23] and favors a sister group relationship of bdelloids and acanthocephalans, with the Monogononta and Seisonidea placed basally to the Lemniscea (Fig. 1A). Morphological evidence for such grouping has been inferred from two lateral intrusions in the neck region and a retractable anterior body section in Acanthocephala and Bdelloidea [23]. The Lemniscea hypothesis received additional support from 16S rRNA, 18S rRNA, 28S rRNA, cytochrome c oxidase subunit 1 (cox 1) and histone H3 data [14-17,19]. The second hypothesis suggests a sistergroup relationship of Monogononta and Bdelloidea (Eurotatoria) and of Seisonidea and Acanthocephala (Pararotatoria) and is herein called Eurotatoria+Pararotatoria hypothesis (Fig. 1B). Besides presumed eurotatorian apomorphies such as the already mentioned corona, the Eurotatoria+Pararotatoria hypothesis is based on ultrastructural peculiarities that have been interpreted as synapomorphies of Seisonidea and Acanthocepahala (spermatozoa with "dense bodies" and epidermis with special filaments [5,9,12]). Additional support for the monophyly of Pararotatoria came from partial 18S rRNA data [24] as well as from a combined dataset of 18S rRNA sequences, heat shock gene sequences (hsp82), and morphological characters [25]. The third hypothesis reflects the classical view of monophyletic Rotifera (Monogononta+Bdelloidea+Seisonidea) and Eurotatoria (Monogononta+Bdelloidea) and proposes Acanthocephala as the sistergroup of Rotifera ("classical Rotifera+Acanthocephala hypothesis", see Fig. 1C). This classical concept has been formulated based on specific features of toe morphology, sensory and masticatory apparatus in Rotifera and Eurotatoria, respectively [13,26], and was supported by 18S rRNA data [27]. The fourth hypothesis has been proposed on the basis of hsp82 sequences, and groups Acanthocephala and Eurotatoria with exclusion of Seisonidea [28] ("Eurotatoria+Acanthocephala", see Fig. 1D). Underlying the fourth hypothesis, the absence of acrosomal structures might represent a synapomorphy of Eurotatoria and Acanthocephala [21]. According to the fifth hypothesis, Bdelloidea, Seisonidea, and Acanthocephala form a monophylum for which the name Hemirotifera has been proposed (Fig. 1E). The Hemirotifera hypothesis has been inferred from a combined dataset of molecular (18S rRNA, 28S rRNA, histone H3, cox 1) and morphological characters [29]. This survey of competing hypotheses demonstrates that the question of phylogenetic relationships within Syndermata and therewith of the evolution of the acanthocephalan endoparasitism is closely connected to the more basal question of monophyly of Eurotatoria.


EST based phylogenomics of Syndermata questions monophyly of Eurotatoria.

Witek A, Herlyn H, Meyer A, Boell L, Bucher G, Hankeln T - BMC Evol. Biol. (2008)

Competing phylogenetic hypotheses amongst Syndermata. Cladograms reflecting the competing hypotheses on the phylogenetic relations among Monogononta, Bdelloidea, Acanthocephala and Seisonidea. A Lemniscea hypothesis [23]. B Eurotatoria+Pararotatoria hypothesis [5,9,12]. C Rotifera+Acanthocephala [8,26]. D Eurotatoria+Acanthocephala [28]. E Hemirotifera [29].
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2654452&req=5

Figure 1: Competing phylogenetic hypotheses amongst Syndermata. Cladograms reflecting the competing hypotheses on the phylogenetic relations among Monogononta, Bdelloidea, Acanthocephala and Seisonidea. A Lemniscea hypothesis [23]. B Eurotatoria+Pararotatoria hypothesis [5,9,12]. C Rotifera+Acanthocephala [8,26]. D Eurotatoria+Acanthocephala [28]. E Hemirotifera [29].
Mentions: The animal taxon Rotifera comprises free-living and commensalic microscopic species of aquatic habitats that are traditionally grouped into the three subtaxa Bdelloidea, Monogononta and Seisonidea [1-3]. Bdelloids (about 460 species) inhabit freshwater, are capable of anhydrobiosis and reproduce strictly by parthenogenesis. Monogononts (about 1,570 species) live in limnic, brackish and marine waters and have a lifecycle with alternating phases of parthenogenetic and sexual reproduction. Thirdly, at least two of the hitherto three described species belonging to Seisonidea are epibionts on marine crustaceans of the genus Nebalia [3,4]. Though Bdelloidea, Monogononta and Seisonidea are subsumed as Rotifera or Rotatoria, the eponymous rotatory organ or corona, a seemingly rotating assembly of cilia at the anterior end of the animal, is absent in Seisonidea. For this and other reasons Bdelloidea and Monogononta are often regarded as sistergroups of a taxon named Eurotatoria [2,5,6]. In contrast to Bdelloidea, Monogononta and Seisonidea, the Acanthocephala are obligatory endoparasites with a complicated lifecycle. Their definite hosts are vertebrates, while their intermediate hosts are insects, chilopods and crustaceans (e.g., Meyer [7]). Along with the endoparasitic life cycle, the acanthocephalan subtaxa share a plethora of derived morphological characters (e.g., [8-11]) so that the monophyly of Acanthocephala as a whole has never been debated. Moreover, the grouping of Acanthocephala, Bdelloidea, Monogononta and Seisonidea into the taxon Syndermata is widely accepted due to special features in epidermal and sperm ultrastructure (e.g., syncytial epidermis, spermatozoon with anteriorly inserted cilium; see [5,8,9,12,13]), as well as congruent results from molecular approaches [14-20]. It is further undisputed that Syndermata are part of a more comprehensive monophylum called Gnathifera [9,21,22]. On the other hand, the phylogenetic position of Syndermata beyond Gnathifera as well as the relationships among the syndermatan subtaxa Acanthocephala, Bdelloidea, Monogononta and Seisonidea are still unresolved. So far, five competing hypotheses on the internal phylogeny of Syndermata have been suggested (Fig. 1A–E). The Lemniscea hypothesis goes back to Lorenzen [23] and favors a sister group relationship of bdelloids and acanthocephalans, with the Monogononta and Seisonidea placed basally to the Lemniscea (Fig. 1A). Morphological evidence for such grouping has been inferred from two lateral intrusions in the neck region and a retractable anterior body section in Acanthocephala and Bdelloidea [23]. The Lemniscea hypothesis received additional support from 16S rRNA, 18S rRNA, 28S rRNA, cytochrome c oxidase subunit 1 (cox 1) and histone H3 data [14-17,19]. The second hypothesis suggests a sistergroup relationship of Monogononta and Bdelloidea (Eurotatoria) and of Seisonidea and Acanthocephala (Pararotatoria) and is herein called Eurotatoria+Pararotatoria hypothesis (Fig. 1B). Besides presumed eurotatorian apomorphies such as the already mentioned corona, the Eurotatoria+Pararotatoria hypothesis is based on ultrastructural peculiarities that have been interpreted as synapomorphies of Seisonidea and Acanthocepahala (spermatozoa with "dense bodies" and epidermis with special filaments [5,9,12]). Additional support for the monophyly of Pararotatoria came from partial 18S rRNA data [24] as well as from a combined dataset of 18S rRNA sequences, heat shock gene sequences (hsp82), and morphological characters [25]. The third hypothesis reflects the classical view of monophyletic Rotifera (Monogononta+Bdelloidea+Seisonidea) and Eurotatoria (Monogononta+Bdelloidea) and proposes Acanthocephala as the sistergroup of Rotifera ("classical Rotifera+Acanthocephala hypothesis", see Fig. 1C). This classical concept has been formulated based on specific features of toe morphology, sensory and masticatory apparatus in Rotifera and Eurotatoria, respectively [13,26], and was supported by 18S rRNA data [27]. The fourth hypothesis has been proposed on the basis of hsp82 sequences, and groups Acanthocephala and Eurotatoria with exclusion of Seisonidea [28] ("Eurotatoria+Acanthocephala", see Fig. 1D). Underlying the fourth hypothesis, the absence of acrosomal structures might represent a synapomorphy of Eurotatoria and Acanthocephala [21]. According to the fifth hypothesis, Bdelloidea, Seisonidea, and Acanthocephala form a monophylum for which the name Hemirotifera has been proposed (Fig. 1E). The Hemirotifera hypothesis has been inferred from a combined dataset of molecular (18S rRNA, 28S rRNA, histone H3, cox 1) and morphological characters [29]. This survey of competing hypotheses demonstrates that the question of phylogenetic relationships within Syndermata and therewith of the evolution of the acanthocephalan endoparasitism is closely connected to the more basal question of monophyly of Eurotatoria.

Bottom Line: Here we present our results from a phylogenomic approach studying i) the phylogenetic position of Syndermata within Spiralia, ii) the monophyletic origin of monogononts and bdelloids and iii) the phylogenetic relations of the latter two taxa to acanthocephalans.Our findings suggest that the phylogenetic position of Syndermata within Spiralia is close to Platyhelminthes, that Eurotatoria are not monophyletic and that bdelloids are more closely related to acanthocephalans than monogononts.Mapping morphological character evolution onto molecular phylogeny suggests the (partial or complete) reduction of the corona and the emergence of a retractable anterior end (rostrum, proboscis) before the separation of Acanthocephala.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Molecular Genetics, Johannes Gutenberg-University Mainz, J. J.-Becherweg 32, D-55099 Mainz, Germany. witeka@uni-mainz.de

ABSTRACT

Background: The metazoan taxon Syndermata comprising Rotifera (in the classical sense of Monogononta+Bdelloidea+Seisonidea) and Acanthocephala has raised several hypotheses connected to the phylogeny of these animal groups and the included subtaxa. While the monophyletic origin of Syndermata and Acanthocephala is well established based on morphological and molecular data, the phylogenetic position of Syndermata within Spiralia, the monophyletic origin of Monogononta, Bdelloidea, and Seisonidea and the acanthocephalan sister group are still a matter of debate. The comparison of the alternative hypotheses suggests that testing the phylogenetic validity of Eurotatoria (Monogononta+Bdelloidea) is the key to unravel the phylogenetic relations within Syndermata. The syndermatan phylogeny in turn is a prerequisite for reconstructing the evolution of the acanthocephalan endoparasitism.

Results: Here we present our results from a phylogenomic approach studying i) the phylogenetic position of Syndermata within Spiralia, ii) the monophyletic origin of monogononts and bdelloids and iii) the phylogenetic relations of the latter two taxa to acanthocephalans. For this analysis we have generated EST libraries of Pomphorhynchus laevis, Echinorhynchus truttae (Acanthocephala) and Brachionus plicatilis (Monogononta). By extending these data with database entries of B. plicatilis, Philodina roseola (Bdelloidea) and 25 additional metazoan species, we conducted phylogenetic reconstructions based on 79 ribosomal proteins using maximum likelihood and bayesian approaches. Our findings suggest that the phylogenetic position of Syndermata within Spiralia is close to Platyhelminthes, that Eurotatoria are not monophyletic and that bdelloids are more closely related to acanthocephalans than monogononts.

Conclusion: Mapping morphological character evolution onto molecular phylogeny suggests the (partial or complete) reduction of the corona and the emergence of a retractable anterior end (rostrum, proboscis) before the separation of Acanthocephala. In particular, the evolution of a rostrum might have been a key event leading to the later evolution of the acanthocephalan endoparasitism, given the enormous relevance of the proboscis for anchoring of the adults to the definitive hosts' intestinal wall.

Show MeSH
Related in: MedlinePlus