Abstract
ABSTRACTMolluscs are extremely diverse invertebrate animals with a rich fossil record, highly divergent life cycles, and considerable economical and ecological importance. Key representatives include worm‐like aplacophorans, armoured groups (e.g. polyplacophorans, gastropods, bivalves) and the highly complex cephalopods. Molluscan origins and evolution of their different phenotypes have largely remained unresolved, but significant progress has been made over recent years. Phylogenomic studies revealed a dichotomy of the phylum, resulting in Aculifera (shell‐less aplacophorans and multi‐shelled polyplacophorans) and Conchifera (all other, primarily uni‐shelled groups). This challenged traditional hypotheses that proposed that molluscs gradually evolved complex phenotypes from simple, worm‐like animals, a view that is corroborated by developmental studies that showed that aplacophorans are secondarily simplified. Gene expression data indicate that key regulators involved in anterior–posterior patterning (the homeobox‐containing Hox genes) lost this function and were co‐opted into the evolution of taxon‐specific novelties in conchiferans. While the bone morphogenetic protein (BMP)/decapentaplegic (Dpp) signalling pathway, that mediates dorso‐ventral axis formation, and molecular components that establish chirality appear to be more conserved between molluscs and other metazoans, variations from the common scheme occur within molluscan sublineages. The deviation of various molluscs from developmental pathways that otherwise appear widely conserved among metazoans provides novel hypotheses on molluscan evolution that can be tested with genome editing tools such as the CRISPR/Cas9 (clustered regularly interspaced short palindromic repeats/clustered regularly interspaced short palindromic repeats‐associated protein9) system.
Highlights
Molluscs are extremely diverse invertebrate animals with a rich fossil record, highly divergent life cycles, and considerable economical and ecological importance
While the bone morphogenetic protein (BMP)/decapentaplegic (Dpp) signalling pathway, that mediates dorso-ventral axis formation, and molecular components that establish chirality appear to be more conserved between molluscs and other metazoans, variations from the common scheme occur within molluscan sublineages
The deviation of various molluscs from developmental pathways that otherwise appear widely conserved among metazoans provides novel hypotheses on molluscan evolution that can be tested with genome editing tools such as the CRISPR/Cas9 system
Summary
Molluscan interrelationships have been contentious for a long time. In the pre-genomic era, cladistic analyses based on morphological data sets largely agreed on a phylogenetic scenario that placed the aplacophoran taxa (Neomeniomorpha and Chaetodermomorpha) as the earliest extant offshoots, either with a monophyletic Aplacophora as sister to the remaining molluscs (Testaria), of which Polyplacophora was considered the sister clade to all primarily single-shelled forms (Conchifera) (Waller, 1998), or with either of the two aplacophoran groups as sister to the remaining class-level taxa (Salvini-Plawen, 1972, 1991; Haszprunar, 1992, 2000; Salvini-Plawen & Steiner, 1996, 2014) (Fig. 2). Are conchiferan interrelationships still highly controversial (Haszprunar & Wanninger, 2012; Schrodl & Stoger, 2014), but the vast phenotypic diversity of its individual class-level clades renders ground-pattern reconstruction difficult no matter what kind of topology will eventually be agreed on With their simple single shell and repetitive organ systems including gills, nephridia, commissures, and, most importantly, eight sets of dorso-ventral muscles, the monoplacophorans intuitively make good candidates to be directly compared to the aculiferan condition. These findings once more confirm the commonly emerging picture that developmental pathways and gene functions appear to be highly plastic in molluscs, with a strong tendency towards co-option as well as loss-of-function events occurring even at low hierarchical taxonomic levels
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