Abstract
BackgroundThe morphological variety displayed by the molluscan shell underlies much of the evolutionary success of this phylum. However, the broad diversity of shell forms, sizes, ornamentations and functions contrasts with a deep conservation of early cell movements associated with the initiation of shell construction. This process begins during early embryogenesis with a thickening of an ectodermal, ‘dorsal’ (opposite the blastopore) population of cells, which then invaginates into the blastocoel to form the shell gland. The shell gland evaginates to form the shell field, which then expands and further differentiates to eventually become the adult shell-secreting organ commonly known as the mantle. Despite the deep conservation of the early shell forming developmental program across molluscan classes, little is known about the fine-scale cellular or molecular processes that underlie molluscan shell development.ResultsUsing modern imaging techniques we provide here a description of the morphogenesis of a gastropod shell gland and shell field using the pulmonate gastropod Lymnaea stagnalis as a model. We find supporting evidence for a hypothesis of molluscan shell gland specification proposed over 60 years ago, and present histochemical assays that can be used to identify a variety of larval shell stages and distinct cell populations in whole mounts.ConclusionsBy providing a detailed spatial and temporal map of cell movements and differentiation events during early shell development in L. stagnalis we have established a platform for future work aimed at elucidation of the molecular mechanisms and regulatory networks that underlie the evo-devo of the molluscan shell.
Highlights
The morphological variety displayed by the molluscan shell underlies much of the evolutionary success of this phylum
Regulatory genes encoding transcription factors and signalling molecules are expressed in embryonic shell forming tissue in disparate molluscan taxa [18,19,20,21,22,23,24,25]. This raises the possibility that extant shelled molluscs may all initiate shell formation using the same developmental program inherited from a distant ancestor, and that it is the downstream shell forming programs operating in the mature mantle which, during evolution, have generated today’s diversity of shelled adult molluscs
If such a scenario were true, this would mean that a common ancestor of the shelled molluscs evolved a developmental program to form a shell which was passed on to all of its future descendants; a 540+ million year old innovation that was of great importance to the future evolutionary success of the phylum
Summary
The morphological variety displayed by the molluscan shell underlies much of the evolutionary success of this phylum. Regulatory genes encoding transcription factors and signalling molecules (such as members of the Hox cluster, engrailed and decapentaplegic) are expressed in embryonic shell forming tissue in disparate molluscan taxa [18,19,20,21,22,23,24,25] This raises the possibility that extant shelled molluscs may all initiate shell formation using the same developmental program inherited from a distant ancestor, and that it is the downstream shell forming programs operating in the mature mantle which, during evolution, have generated today’s diversity of shelled adult molluscs. If such a scenario were true, this would mean that a common ancestor of the shelled molluscs evolved a developmental program to form a shell which was passed on to all of its future descendants; a 540+ million year old innovation that was of great importance to the future evolutionary success of the phylum
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