Embryonic chirality and the evolution of spiralian left–right asymmetries

The group Spiralia includes species with one of the most significant cases of left–right asymmetries in animals: the coiling of the shell of gastropod molluscs (snails). In this animal group, an early event of embryonic chirality controlled by cytoskeleton dynamics and the subsequent differential ac...

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Published in:Philosophical transactions of the Royal Society of London. Series B. Biological sciences 2016-12, Vol.371 (1710), p.20150411-20150411
Main Authors: Martín-Durán, José M., Vellutini, Bruno C., Hejnol, Andreas
Format: Article
Language:English
Subjects:
Animals
Annelida
Anomala
Biological Evolution
Body Patterning
Brachiopoda
Evolution
Gastropoda
Gene Expression Regulation, Developmental
Invertebrates - embryology
Invertebrates - genetics
Left–right Axis
Lineus
Membranipora membranacea
Mollusca
Nodal
Nodal Protein - genetics
Owenia fusiformis
Pitx
Spiralia
Transcription Factors - genetics
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Summary:The group Spiralia includes species with one of the most significant cases of left–right asymmetries in animals: the coiling of the shell of gastropod molluscs (snails). In this animal group, an early event of embryonic chirality controlled by cytoskeleton dynamics and the subsequent differential activation of the genes nodal and Pitx determine the left–right axis of snails, and thus the direction of coiling of the shell. Despite progressive advances in our understanding of left–right axis specification in molluscs, little is known about left–right development in other spiralian taxa. Here, we identify and characterize the expression of nodal and Pitx orthologues in three different spiralian animals—the brachiopod Novocrania anomala, the annelid Owenia fusiformis and the nemertean Lineus ruber—and demonstrate embryonic chirality in the biradial-cleaving spiralian embryo of the bryozoan Membranipora membranacea. We show asymmetric expression of nodal and Pitx in the brachiopod and annelid, respectively, and symmetric expression of Pitx in the nemertean. Our findings indicate that early embryonic chirality is widespread and independent of the cleavage programme in the Spiralia. Additionally, our study illuminates the evolution of nodal and Pitx signalling by demonstrating embryonic asymmetric expression in lineages without obvious adult left–right asymmetries. This article is part of the themed issue ‘Provocative questions in left–right asymmetry’.
ISSN:0962-8436
1471-2970
DOI:10.1098/rstb.2015.0411