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The developmental basis for the recurrent evolution of deuterostomy and protostomy

Abstract

The mouth opening of bilaterian animals develops either separate from (deuterostomy) or connected to (protostomy) the embryonic blastopore, the site of endomesoderm internalization. Although this distinction preluded the classification of bilaterian animals in Deuterostomia and Protostomia, and has influenced major scenarios of bilaterian evolution, the developmental basis for the appearance of these different embryonic patterns remains unclear. To identify the underlying mechanisms, we compared the development of two brachiopod species that show deuterostomy (Novocrania anomala) and protostomy (Terebratalia transversa), respectively. We show that the differential activity of Wnt signalling, together with the timing and location of mesoderm formation, correlate with the differential behaviour and fate of the blastopore. We further assess these principles in the spiral-cleaving group Annelida, and propose that the developmental relationships of mouth and blastoporal openings are secondary by-products of variations in axial and mesoderm development. This challenges the previous evolutionary emphasis on extant blastoporal behaviours to explain the origin and diversification of bilaterian animals.

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Figure 1: Fate of the blastopore and the evolution of Bilateria.
Figure 2: Gene expression during N. anomala and T. transversa embryogenesis.
Figure 3: Lateral drawings showing simplified expression domains of the analysed markers shown in Fig. 2.
Figure 4: Effect of Azk on brachiopod embryos at the blastula stage.
Figure 5: Dorsoventral development and effect of DMH1 in brachiopod embryos.
Figure 6: Gene expression during development of O. fusiformis.
Figure 7: The developmental basis of different blastoporal fates in N. anomala and T. transversa.

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Acknowledgements

We thank H. Hausen and O. Voecking for sharing the RNAseq data of O. fusiformis and expertise with the spawnings, B. C. Vellutini for help with collections and drug treatments, and G. S. Richards, F. Rentzsch, M. Iglesias and the members of the Hejnol laboratory for their comments on the manuscript. We also thank the staff at Friday Harbor Laboratories, Espeland Marine Biological Station and Station Biologique de Roscoff for assistance with animal collections. The study was funded by the core budget of the Sars Centre and supported by The European Research Council Community’s Framework Program Horizon 2020 (2014–2020) ERC grant agreement 648861 and an L. Meltzers Høyskolefond grant to A.H. J.M.M.-D. was supported by Marie Curie fellowship IEF 329024.

Author information

Authors and Affiliations

Authors

Contributions

J.M.M.-D. and A.H. conceived the project. J.M.M.-D., Y.J.P. and A.H. performed animal collections and cloned genes, J.M.M.-D conducted the experiments, and J.M.M.-D. and A.H. performed the four-dimensional recordings. Y.J.P. carried out the EdU analysis in T. transversa. J.M.M.-D. and A.H. analysed the data and wrote the manuscript, and Y.J.P. and M.Q.M. edited the paper. All authors discussed and commented on the data.

Corresponding authors

Correspondence to José M. Martín-Durán or Andreas Hejnol.

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The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary figures 1–12; Supplementary Tables 1–9; Supplementary References and legends for Supplementary Videos (PDF 4910 kb)

Supplementary Animation

Animated summary of the main findings of the manuscript regarding brachiopod gastrulation. (HTML 204 kb)

Supplementary Video 1

Description: Time-lapse recording of an embryo of N. anomala from the 5 early blastula stage to gastrulation, viewed from the animal hemisphere. (MP4 2036 kb)

Supplementary Video 2

Time-lapse recording of N. anomala from the early gastrula stage to the onset of axial elongation (shift of the blastopore to a ventral-posterior position), viewed from the vegetal pole. (MP4 12442 kb)

Supplementary Video 3

Time-lapse recording of N. anomala during early axial elongation, viewed from the ventral side. (MP4 2468 kb)

Supplementary Video 4

Time-lapse recording of N. anomala during axial elongation and blastopore closure, viewed from the ventral side. (MP4 10529 kb)

Supplementary Video 5

Time-lapse recording of N. anomala during late axial elongation and early larva differentiation (apical lobe-mantle lobe boundary formation; closure of the blastopore), viewed from the ventral side. (MP4 3006 kb)

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Martín-Durán, J., Passamaneck, Y., Martindale, M. et al. The developmental basis for the recurrent evolution of deuterostomy and protostomy. Nat Ecol Evol 1, 0005 (2017). https://doi.org/10.1038/s41559-016-0005

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