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Adoption of conserved developmental genes in development and origin of the medusa body plan.

Kraus JE, Fredman D, Wang W, Khalturin K, Technau U - Evodevo (2015)

Bottom Line: It is therefore unclear whether medusa formation has evolved independently in different medusozoans.Our data represent the first comparative gene expression analysis of developing medusae in two representatives of Scyphozoa and Hydrozoa.We propose that the evolution of a new life stage may be facilitated by the adoption of existing developmental genes.

View Article: PubMed Central - PubMed

Affiliation: Department for Molecular Evolution and Development, Centre for Organismal Systems Biology, University of Vienna, Althanstraße 14, Wien, Vienna 1090 Austria.

ABSTRACT

Background: The metagenesis of sessile polyps into pelagic medusae in cnidarians represents one of the most ancient complex life cycles in animals. Interestingly, scyphozoans and hydrozoans generate medusae by apparently fundamentally different processes. It is therefore unclear whether medusa formation has evolved independently in different medusozoans. To this end, a thorough understanding of the correspondence of polyp and medusa is required.

Results: We monitored the expression patterns of conserved developmental genes in developing medusae of Clytia hemisphaerica (Hydrozoa) and Aurelia aurita (Scyphozoa) and found that developing medusae and polyps share similarities in their morphology and developmental gene expression. Unexpectedly, however, polyp tentacle marker genes were consistently expressed in the developing medusa bell, suggesting that the bell of medusae corresponds to modified and fused polyp tentacle anlagen.

Conclusions: Our data represent the first comparative gene expression analysis of developing medusae in two representatives of Scyphozoa and Hydrozoa. The results challenge prevailing views about polyp medusa body plan homology. We propose that the evolution of a new life stage may be facilitated by the adoption of existing developmental genes.

No MeSH data available.


Related in: MedlinePlus

Principles underlying medusa formation in cnidarians. a Phylogenetic relationship of the cnidarian taxa (blue box) [14, 55, 56]. Anthozoans only form polyps, whereas medusozoan taxa show life cycles with polyps and medusae. Staurozoans, cubozoans and scyphozoans form their medusae by different forms of apical metamorphosis of polyps (pink box) [55]. Hydrozoans form their medusae through lateral budding on polyps (green box). b Polydisc strobilation in Aurelia aurita. c Lateral budding of young medusae in Clytia hemisphaerica from a specialized polyp form within the polyp colony
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Fig1: Principles underlying medusa formation in cnidarians. a Phylogenetic relationship of the cnidarian taxa (blue box) [14, 55, 56]. Anthozoans only form polyps, whereas medusozoan taxa show life cycles with polyps and medusae. Staurozoans, cubozoans and scyphozoans form their medusae by different forms of apical metamorphosis of polyps (pink box) [55]. Hydrozoans form their medusae through lateral budding on polyps (green box). b Polydisc strobilation in Aurelia aurita. c Lateral budding of young medusae in Clytia hemisphaerica from a specialized polyp form within the polyp colony

Mentions: Complex life cycles involve a succession of life stages with drastically divergent body forms, behaviours and ecological habitat [1]. The emergence of complex life cycles is driven by the exploitation of different ecological niches and seasonally available resources [1]. The wide distribution of complex life cycles shows that such phenomena constitute an evolutionary advantage in virtually all eukaryotic phyla. Cnidaria, the sister group of the Bilateria, represent the oldest of all animal lineages with a complex life cycle. Cubozoa, Scyphozoa and Hydrozoa generally show a triphasic life cycle with a succession of a larva, a sessile polyp form and a pelagic, sexually active medusa stage (Fig. 1a). A polyp-like form has been suggested by many authors as the ancestral cnidarian adult body plan, and the medusa life stage a later inserted secondary derivative [2–8], although other scenarios have also been proposed (e.g. [9, 10]). The generation of medusae occurs in fundamentally different ways in different medusozoan taxa. A process called strobilation, where medusae form by apical metamorphosis of the polyp body followed by horizontal fission, is found in scyphozoans. Also in cubozoans, medusae are generated by apical metamorphosis from polyps [11] (Fig. 1b). While most authors interpret the cubozoan medusa formation as a complete metamorphosis from polyp to medusa [11, 12], others understand it as a modified form of strobilation [13]. Staurozoans are unusual as they form ‘stalked medusae’ by apical metamorphosis of the polyp but do not subsequently undergo fission [14, 15]. In contrast to the three other medusozoan taxa, medusae of hydrozoans (‘hydromedusae’) are generally formed in a lateral budding process from polyps. Uniquely, this process involves the generation of a third tissue layer in between endo- and ectoderm, the so-called entocodon, previously proposed as a potential homologous layer to the bilaterian mesoderm [9, 10] (Fig. 1c).Fig. 1


Adoption of conserved developmental genes in development and origin of the medusa body plan.

Kraus JE, Fredman D, Wang W, Khalturin K, Technau U - Evodevo (2015)

Principles underlying medusa formation in cnidarians. a Phylogenetic relationship of the cnidarian taxa (blue box) [14, 55, 56]. Anthozoans only form polyps, whereas medusozoan taxa show life cycles with polyps and medusae. Staurozoans, cubozoans and scyphozoans form their medusae by different forms of apical metamorphosis of polyps (pink box) [55]. Hydrozoans form their medusae through lateral budding on polyps (green box). b Polydisc strobilation in Aurelia aurita. c Lateral budding of young medusae in Clytia hemisphaerica from a specialized polyp form within the polyp colony
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4464714&req=5

Fig1: Principles underlying medusa formation in cnidarians. a Phylogenetic relationship of the cnidarian taxa (blue box) [14, 55, 56]. Anthozoans only form polyps, whereas medusozoan taxa show life cycles with polyps and medusae. Staurozoans, cubozoans and scyphozoans form their medusae by different forms of apical metamorphosis of polyps (pink box) [55]. Hydrozoans form their medusae through lateral budding on polyps (green box). b Polydisc strobilation in Aurelia aurita. c Lateral budding of young medusae in Clytia hemisphaerica from a specialized polyp form within the polyp colony
Mentions: Complex life cycles involve a succession of life stages with drastically divergent body forms, behaviours and ecological habitat [1]. The emergence of complex life cycles is driven by the exploitation of different ecological niches and seasonally available resources [1]. The wide distribution of complex life cycles shows that such phenomena constitute an evolutionary advantage in virtually all eukaryotic phyla. Cnidaria, the sister group of the Bilateria, represent the oldest of all animal lineages with a complex life cycle. Cubozoa, Scyphozoa and Hydrozoa generally show a triphasic life cycle with a succession of a larva, a sessile polyp form and a pelagic, sexually active medusa stage (Fig. 1a). A polyp-like form has been suggested by many authors as the ancestral cnidarian adult body plan, and the medusa life stage a later inserted secondary derivative [2–8], although other scenarios have also been proposed (e.g. [9, 10]). The generation of medusae occurs in fundamentally different ways in different medusozoan taxa. A process called strobilation, where medusae form by apical metamorphosis of the polyp body followed by horizontal fission, is found in scyphozoans. Also in cubozoans, medusae are generated by apical metamorphosis from polyps [11] (Fig. 1b). While most authors interpret the cubozoan medusa formation as a complete metamorphosis from polyp to medusa [11, 12], others understand it as a modified form of strobilation [13]. Staurozoans are unusual as they form ‘stalked medusae’ by apical metamorphosis of the polyp but do not subsequently undergo fission [14, 15]. In contrast to the three other medusozoan taxa, medusae of hydrozoans (‘hydromedusae’) are generally formed in a lateral budding process from polyps. Uniquely, this process involves the generation of a third tissue layer in between endo- and ectoderm, the so-called entocodon, previously proposed as a potential homologous layer to the bilaterian mesoderm [9, 10] (Fig. 1c).Fig. 1

Bottom Line: It is therefore unclear whether medusa formation has evolved independently in different medusozoans.Our data represent the first comparative gene expression analysis of developing medusae in two representatives of Scyphozoa and Hydrozoa.We propose that the evolution of a new life stage may be facilitated by the adoption of existing developmental genes.

View Article: PubMed Central - PubMed

Affiliation: Department for Molecular Evolution and Development, Centre for Organismal Systems Biology, University of Vienna, Althanstraße 14, Wien, Vienna 1090 Austria.

ABSTRACT

Background: The metagenesis of sessile polyps into pelagic medusae in cnidarians represents one of the most ancient complex life cycles in animals. Interestingly, scyphozoans and hydrozoans generate medusae by apparently fundamentally different processes. It is therefore unclear whether medusa formation has evolved independently in different medusozoans. To this end, a thorough understanding of the correspondence of polyp and medusa is required.

Results: We monitored the expression patterns of conserved developmental genes in developing medusae of Clytia hemisphaerica (Hydrozoa) and Aurelia aurita (Scyphozoa) and found that developing medusae and polyps share similarities in their morphology and developmental gene expression. Unexpectedly, however, polyp tentacle marker genes were consistently expressed in the developing medusa bell, suggesting that the bell of medusae corresponds to modified and fused polyp tentacle anlagen.

Conclusions: Our data represent the first comparative gene expression analysis of developing medusae in two representatives of Scyphozoa and Hydrozoa. The results challenge prevailing views about polyp medusa body plan homology. We propose that the evolution of a new life stage may be facilitated by the adoption of existing developmental genes.

No MeSH data available.


Related in: MedlinePlus