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The evolution of mollusc shells

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Molluscan shells are externally fabricated by specialized epithelial cells on the dorsal mantle. Although a conserved set of regulatory genes appears to underlie specification of mantle progenitor cells, the genes that contribute to the formation of the mature shell are incredibly diverse. Recent comparative analyses of mantle transcriptomes and shell proteomes of gastropods and bivalves are consistent with shell diversity being underpinned by a rapidly evolving mantle secretome (suite of genes expressed in the mantle that encode secreted proteins) that is the product of (a) high rates of gene co‐option into and loss from the mantle gene regulatory network, and (b) the rapid evolution of coding sequences, particular those encoding repetitive low complexity domains. Outside a few conserved genes, such as carbonic anhydrase, a so‐called “biomineralization toolkit” has yet to be discovered. Despite this, a common suite of protein domains, which are often associated with the extracellular matrix and immunity, appear to have been independently and often uniquely co‐opted into the mantle secretomes of different species. The evolvability of the mantle secretome provides a molecular explanation for the evolution and diversity of molluscan shells. These genomic processes are likely to underlie the evolution of other animal biominerals, including coral and echinoderm skeletons. This article is categorized under: Comparative Development and Evolution > Regulation of Organ Diversity Comparative Development and Evolution > Evolutionary Novelties
“Prosobranchia,” a plate from Ernst Haeckel’s “Kunstformen der Natur” (1904), is a beautiful depiction of the geometric beauty and diversity of sea shells
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Enrichment of domains in co‐opted gene families. (Reprinted with permission from Aguilera et al. ()). Broad functional categories are shown on the left vertical axis of the heat map, and individual domain names are indicated on the right. Domains are represented if they are significantly enriched in newly gained secreted gene families from at least two lineages. On the horizontal axis of the heat map, ancestral lineages are depicted on the left, current species on the right (refer to the tree in Figure for the phylogenetic tree). The color of the squares indicates the level of enrichment, only enrichments with a p‐value >.05 are shown
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Evolution of the molluscan secretome. (Reprinted with permission from Aguilera et al. ()). (a) Origin of secreted mantle proteins from gastropods (top) and bivalves (middle), with phylostrata (PS1–13) depicted below. The three main evolutionary periods are indicated in red. The phylostrata indicated in grey are those that predate the origin of Mollusca, these proteins must therefore have been co‐opted into the secretome. (b) Organismal tree with pie charts showing the proportion of secretome genes that have been gained (black), co‐opted (red), lost (blue) and maintained from the last common ancestor of gastropods and bivalves (BGLCA, brown). Examples of enriched domains that are inferred to have existed in BGLCA (orange box), ancestral bivalve (green box), and ancestral gastropod (blue box), are indicated. Three additional domains, carbonic anhydrase, tyrosinase, and chitin‐binding domain (white box), also existed in the BGLCA secretome, these genes have also been identified in a study by Arivalagan et al. ()
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Shell microstructure. (a) Schematic of the organization of the molluscan shell and mantle. (Reprinted with permission from Beedham ()). (b) SEM of a transverse section of the juvenile shell of the abalone, Haliotis asinina. The top layer displays prismatic microstructure (P), the lower layer is columnar nacre (N). Image by Kathryn Green
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The development of the shell of the abalone, Haliotis asinina. (a). Scanning electron micrograph (SEM) of a trochophore larva. sf., shell field. (b) SEM of the expanding protoconch (pc) in the larva. (c) SEM of the complete larval protoconch. (d) SEM of early teloconch development in a recently settled juvenile. The division between the protoconch and teloconch is indicated by an arrow. (e) Bright field image of a juvenile of a similar age to that in (d). (f) Eight week old juvenile showing the beginnings of shell patterning. (g) Juvenile shell. (h) Adult shell. Arrow shows the spire, where the juvenile shell is visible. Inset: higher magnification of the spire of “(f)” The location of the larval and early juvenile shell is visible indicated by dotted lines. (SEM images reprinted with permission from Jackson, Wörheide, and Degnan ())
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Current consensus of the relationships of molluscan classes from recent studies (Kocot et al., ; Smith et al., ; Vinther, Sperling, Briggs, & Peterson, ). The position of Monoplacophora is unresolved. (Photographs reprinted with permission from Wanninger and Wollesen ())
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