Abstract

Molluscan shells exhibit a wide diversity of pigmentation patterns and are often used as models for understanding the mechanisms underlying biological pattern formation. Numerous mathematical models have been put forward to describe these patterns, but all rely on assumptions regarding the nature of the pigments and the cells from which they are secreted. We investigated pigmentation and cellular morphology of the mantle (shell-secreting organ) of the tropical abalone, Haliotis asinina, as a crucial step towards understanding the molecular mechanisms of shell patterning in this gastropod mollusc. Accumulation and release of pigmented products occurs within secretory tubules in the prismatic zone of the juvenile H. asinina mantle. The colour observed within these tubules closely matches the colour deposited most recently within the shell lying directly above. The pigments are autofluorescent, and confocal microscopy reveals that multiple pigments can be present within a single tubule at any one time. Examination of mantle morphology in other gastropods reveals that mantle tubules are not restricted to abalone, but are not universal. The presence of a tubule-based secretory system within the abalone mantle demonstrates that pigmentation is not controlled by a simple line of cells. Instead, co-ordination of patterning events is likely to be modular, with signals received by individual cells being transmitted throughout the entire tubule to synchronise the accumulation and secretion of pigmented material.

Highlights

  • The shells of molluscs represent a unique example of the emergence of complex patterns during the ontogeny of an organism in which a complete record of developmental processes is preserved

  • The prismatic zone of the abalone mantle contains numerous tubules Toluidine blue stained cross sections of the mantle of juvenile H. asinina reveal numerous invaginations of the epithelium that extend into the connective tissue of the mantle (Figure 2A, arrows, [10])

  • This is evidenced by the expression of the gene Sometsuke in this region, and the identification of the Sometsuke protein in the prismatic shell layer [19,21], we note the possibility that elements of the prismatic layer may be secreted from the periostracal groove [26]

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Summary

Introduction

The shells of molluscs represent a unique example of the emergence of complex patterns during the ontogeny of an organism in which a complete record of developmental processes is preserved This tractability led to mollusc shell pigmentation being used as one of the first models to explore the potential roles of reaction–diffusion mechanisms in morphogenesis [1]. Such mechanisms have since been shown to perform key roles during the development of various model species such as Drosophila, chicken, and zebrafish [2], interpretation of the mechanisms underlying molluscan shell pigmentation is mostly limited to mathematical modeling of hypothetical signaling events [3,4,5,6,7,8,9]. We investigated pigmentation and cellular morphology of the mantle (shell-secreting organ) of the tropical abalone, Haliotis asinina, as a crucial step towards understanding the molecular mechanisms of shell patterning in this gastropod mollusc

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