The evolution of molluscs

Abstract

Molluscs 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.

Development and evolution of the metazoan heart

“…In mollusks, essential functions are performed in determining left/right asymmetry and chirality by the already described cardiac signaling network, such as decapentaplegic/BMP, Nodal signaling, and also dose‐dependent formin genes . Due to the complex evolution and diversification of these species, various interactions are proposed . Nodal signaling is a key factor in the determination of left/right asymmetry, characteristic for body plan development in, for example, snails, and also in cardiogenesis .…”

“…32 Due to the complex evolution and diversification of these species, various interactions are proposed. 33 Nodal signaling is a key factor in the determination of left/right asymmetry, characteristic for body plan development in, for example, snails, 34 and also in cardiogenesis. 35 In the freshwater snail Lymnaea, a set of tool kit genes involved in vertebrates both in cardiogenesis and in left/right body asymmetry (Nodal, BMP4, FGF8, Lrd, Inversin, Brachyury) is expressed in embryonic stages 36 and related to the sidedness in other molluscan species.…”

Unravelling spiral cleavage

“…CRISPR and transgenesis) and imaging approaches (Neal et al, 2019;Perry and Henry, 2015;Zantke et al, 2014;Gline et al, 2011;Song et al, 2002;Weisblat and Kuo, 2014) (Table 1). However, a broad range of other spiralian species have been or are being used to study spiral cleavage employing molecular approaches, includingbut not limited tothe annelids Owenia fusiformis and Streblospio benedicti (Zakas et al, 2018;Martín-Durán et al, 2018); the molluscs Tritia (also known as Ilyanassa) obsoleta, Biomphalaria glabrata, Patella vulgata, Lymnaea stagnalis, Antalis entalis and Acanthochitona crinita (Wanninger and Wollesen, 2018;Abe and Kuroda, 2019;Lambert and Nagy, 2001;Grande and Patel, 2009;Damen and Dictus, 1994); the nemerteans Cerebratulus lacteus, Lineus ruber and Micrura alaskensis (Martín-Durán et al, 2018;Hiebert and Maslakova, 2015;; the flatworm Prostheceraeus crozieri (Girstmair and Telford, 2019); and other spiralian species that have secondarily lost spiral cleavage, such as cephalopod molluscs (Tarazona et al, 2019), the bryozoan Membranipora membranacea (Vellutini et al, 2017), and the brachiopods Terebratalia transversa and Novocrania anomala (Martín-Durán et al, 2016). This combination of established and emerging research systems covering most major lineages of Spiralia is bringing a more comprehensive understanding of spiral cleavage, the plasticity and regularities of this mode of development, and the mechanisms that generate a vast diversity of morphological outcomes from a widely shared embryonic program.…”

“…Each defined by a relatively distinct body plan, some of these groups are among the most diversified animal clades, such as Platyhelminthes, Mollusca and Annelida. Not surprisingly, there are countless examples of morphological innovations in Spiralia, some of them among the most iconic in the animal tree of life, such as molluscan shells (Wanninger and Wollesen, 2018), and others less known but equally exciting, such as annelid and brachiopod chaetae (Schiemann et al, 2017), and molluscan and brachiopod cartilage (Tarazona et al, 2016). What distinguishes spiralians from other vastly diverse animal groups, such as arthropods and vertebrates, is that, to a large extent, this morphological diversity emerges through the same early spiral cleavage program.…”

“…For developmental biology this is of great importance, because embryos of very distantly related and morphologically different species can be perfectly matched at the single-cell resolution, allowing the precise identification of the cellular and molecular mechanisms that drive morphological change. For example, molluscan shells emerge from derivatives of the 2a-2d micromere quartet (Mohri et al, 2016;Chan and Lambert, 2014;Lyons et al, 2015), which form an initial cluster of ectodermal cells, the 'shell field', that will differentiate into a novel cell type with biomineralising potential (Wanninger and Wollesen, 2018). However, the 2d micromere and its progeny generate the majority of the segmented trunk ectoderm and the ventral nerve cords in annelids, where they do not differentiate into biomineralising cell types (Meyer et al, 2010).…”