Embryonic chirality and the evolution of spiralian left–right asymmetries

Abstract

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’.

Cerberus–Nodal–Lefty–Pitx signaling cascade controls left – right asymmetry in amphioxus

“…Pitx and Nodal are also involved in LR specification in molluscs (5) and may be asymmetrically expressed in some other lophotrochozoans (7,8), leading to speculation that the role of Nodal signaling in LR development was acquired early in animal evolution. However, the roles of Cer and Lefty may be more recent innovations.…”

“…Notably, asymmetric expression of Nodal and Pitx in gastropod mollusc embryos plays a role in the development of LR asymmetry, including the coiling of the shell (5,6). Asymmetric expression of Nodal and/or Pitx has also been reported in some other lophotrochozoans, including Pitx in a brachiopod and an annelid and Nodal in a brachiopod (7,8). These data can be interpreted to suggest an ancestral role for Nodal and Pitx in regulating bilaterian LR asymmetry, however the picture is complicated by data from other lineages.…”

“…These data can be interpreted to suggest an ancestral role for Nodal and Pitx in regulating bilaterian LR asymmetry, however the picture is complicated by data from other lineages. First, in ecdysozoan lineages, Nodal appears to have been lost (7,9), whereas Pitx is generally symmetrically expressed (8) and, where studied, does not function in LR asymmetry (10,11). Second, some lophotrochozoans do not show asymmetric Pitx expression (8,12,13).…”

“…First, in ecdysozoan lineages, Nodal appears to have been lost (7, 9), whereas Pitx is generally symmetrically expressed (8) and, where studied, does not function in LR asymmetry (10, 11). Second, some lophotrochozoans do not show asymmetric Pitx expression (8,12,13). Third, functional studies on protostome Nodal signaling are currently restricted to molluscs (5), so it is unclear whether the regulatory connection between Nodal and Pitx is conserved even in those species that show asymmetric expression.…”

Chirality provides a direct fitness advantage and facilitates intermixing in cellular aggregates

“…they break left-right symmetry. While the mechanism of chiral symmetry breaking have been elucidated in some systems [4][5][6][7][8][9][10], the functional role of chirality remains largely unexplored [10][11][12][13].…”