Integrative biology of an embryonic respiratory behaviour in pond snails:the `embryo stir-bar hypothesis'

Abstract

SummaryEmbryos of freshwater snails undergo direct development from single cell to juvenile inside egg masses that are deposited on vegetation and other substratum in pond, lake and stream habitats. Helisoma trivolvis, a member of the Planorbidae family of basommatophoran snails, has served as a model for studying the developmental and physiological roles for neurotransmitters during embryogenesis. Early studies revealed that H. trivolvis embryos from stage E15 to E30, the period between gastrulation and the trochophore-juvenile transition, display a cilia-driven behaviour consisting of slow basal rotation and transient periods of rapid rotation. The discovery of a bilateral pair of early serotonergic neurons, named ENC1, which project an apical process to the embryo surface and basal neurites to ciliated cells, prompted the hypothesis that each ENC1 is a dual-function sensory and motor neuron mediating a physiological embryonic response. This article reviews our past and present studies and addresses questions concerning this hypothesis, including the following. (1) What environmental signal regulates ENC1 activity and rotational behaviour? (2) Does ENC1 function as both a primary sensory and motor neuron underlying the rotational behaviour? (3) What are the sensory transduction mechanisms? (4) How does ENC1 regulate ciliary beating? (5) Do other basommatophoran species have similar neural-ciliary pathways and behavioural responses? (6) How is the behaviour manifest in the dynamic natural environment? In this review, we introduce the 'embryo stir-bar hypothesis', which proposes that embryonic rotation is a hypoxiasensitive respiratory behaviour responsible for mixing the egg capsule fluid, thereby enhancing delivery of environmental oxygen to the embryo.

Development of cardiovascular function in the marine gastropodLittorina obtusata(Linnaeus)

“…We also incorporate a measure of rotational behaviour during larval development as this behaviour is thought to play a role in O 2 uptake by larvae, providing circulation by mixing fluids within the egg capsule (Goldberg et al, 2008;Byrne et al, 2009). We used information of these patterns to test the hypothesis that larval heart function is intimately related to the production of a functional velum and that the development of these structures would coincide, with a subsequent reduction in larval heart activity as the velum degenerates and as circulatory function is assumed by the true heart.…”

Parent–offspring similarity in the timing of developmental events: an origin of heterochrony?

“…Early crawling in embryonic physids could perhaps therefore lead to improved crawling function in adults in line with scenario (i) described by Richardson et al [9]. Moreover, embryonic Lymnaea stagnalis, a species from the same family as R. balthica, is known to exhibit increased spinning frequency in response to hypoxia [31], which has been suggested to improve mixing of capsular fluid, providing an adaptation to the embryo for surviving hypoxic environments [32]. Here, we see a parallel with scenario (ii) outlined by Richardson et al [9].…”

Fluid dynamics in developmental biology: Moving fluids that shape ontogeny

“…Oxygen must reach the embryo by crossing the extraembryonic liquid surrounding it, and in the absence of flow the oxygen will diffuse across, but if the diffusive flux is insufficient, the ciliary movement will stir the liquid, which will increase the oxygen transport to the embryo. The rotation of the embryo as a whole is then a consequence of this behavior coupled with the alignment of ciliary beat directions on the embryo surface (Hunter and Vogel, 1986;Goldberg et al, 2008); we can estimate the Reynolds number to be of order 10 −3 . A similar phenomenon is observed in the cephalopod mollusk Loligo pealei (Arnold and Williams-Arnold, 1980); as this ciliary flow in the embryo is found in both snails and squid, it presumably has a certain generality in mollusks.…”