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

J Exp Biol. 2008 Jun;211(Pt 11):1729-36. doi: 10.1242/jeb.016014.

Abstract

Embryos 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 hypoxia-sensitive respiratory behaviour responsible for mixing the egg capsule fluid, thereby enhancing delivery of environmental oxygen to the embryo.

Publication types

  • Research Support, Non-U.S. Gov't
  • Review

MeSH terms

  • Afferent Pathways / physiology
  • Animals
  • Cell Hypoxia
  • Cell Respiration
  • Cilia / physiology
  • Embryo, Nonmammalian / cytology
  • Embryo, Nonmammalian / physiology*
  • Embryonic Development
  • Motor Neurons / physiology
  • Neurons, Afferent / physiology
  • Oxygen / metabolism
  • Signal Transduction
  • Snails / cytology
  • Snails / embryology*
  • Snails / physiology

Substances

  • Oxygen