The cell lineage of the polyplacophoran, Chaetopleura apiculata: variation in the spiralian program and implications for molluscan evolution

Abstract

Polyplacophorans, or chitons, are an important group of molluscs, which are argued to have retained many plesiomorphic features of the molluscan body plan. Polyplacophoran trochophore larvae posses several features that are distinctly different from those of their sister trochozoan taxa, including modifications of the ciliated prototrochal cells, the postrochal position of the larval eyes or ocelli, epidermal calcareous spicules, and a collection of serially reiterated epidermal shell plates. Despite these differences, chitons demonstrate a canonical pattern of equal spiral cleavage shared by other spiralian phyla that permits the identification of homologous cells across this animal clade. Cell lineage analysis using intracellular labeling on one chiton species, Chaetopleura apiculata, shows that the ocelli are generated from different lineal precursors (second-quartet micromeres: 2a, 2c) compared to those in all other spiralians studied to date (first-quartet micromeres: 1a, 1c). This situation implies that significant changes have also occurred in terms of the inductive interactions that control eye development in the spiralians. Although radical departures from the spiralian developmental program are seen in some molluscs (i.e., cephalopods), the findings presented here indicate that important changes can occur even within the highly constrained framework of the spiral cleavage program. Among spiralians, variation has been reported for the origin of the anterior, sensory, apical organ, which arises from the 1c and 1d micromeres in C. apiculata. The prototroch of C. apiculata consists of two to three irregular rows of ciliated cells but arise from 1q and 2q daughters, similar to that of Ischnochiton rissoi, as well as the gastropod, Patella vulgata. Despite certain early claims, there is no supporting evidence that any of the shell plates arise pretrochally in C. apiculata. The first seven of eight definitive shell plates that arise in the larva originate from shell secreting grooves in the postrochal region (derived from 2c, 2d, 3d). Earlier descriptions indicate that the eighth plate arises later at metamorphosis, and as this is formed posteriorly, it too forms in the postrochal region. On the other hand, epidermal spicules originate from both pretrochal and postrochal cells (1a,1d, 2a, 2c, 3c, 3d). The significance of these observations is discussed in light of various hypotheses concerning the origin of the conchiferan shell. This study reveals conservation, as well as evolutionary novelty, in the assignment of specific cell fates in the spiralians.

Spiralian model systems

“…Additional work was carried out by their counterparts in Europe (e.g., Heymons, 1893;Wierzejski, 1905). That early work has been extended in recent decades using modern cell-autonomous lineage tracers for a number of species (i.e., the gastropod molluscs Crepidula fornicata and C. convexa, Hejnol et al, 2007;Lyons et al, 2012, and Ilyanassa obsoleta, Render 1991, 1997Chan and Lambert 2014; the polyplacophoran mollusc, Chaetopleura apiculata, Henry et al, 2004; the nemerteans, Cerebratulus lacteus, Carinoma tremaphoros, Maslakova et al, 2004a,b; the polyclad turbellarian Hoploplana inquilina, Boyer et al, 1996Boyer et al, , 1998; and the annelids Capitella teleta, , Meyer and Seaver, 2009, 2010, and Platynereis dumerilii, Ackerman et al, 2005Fischer and Arendt, 2013). Together, this body of work has revealed that the ultimate fates of these quadrants are, to a large extent, homologous across the embryos of different spiralian phyla.…”

How to make a protostome

“…the gastropods Patella Damen 1997), Ilyanassa (Goulding 2009;Render 1997) and Crepidula Henry et al 2010), and the polyplacophoran Chaetopleura (Henry et al 2004) (Figs 6, 7). Unfortunately, none of the studies make it possible to follow the movements of the various blastomeres during differentiation.…”

A soft-bodied mollusc with radula from the Middle Cambrian Burgess Shale

“…Shells in the Polyplacophora and possibly Halkieria have been thought to be the result of merging of sclerites 23 . However, it is more likely that the acquisition of shell fields provided the functional ability to deposit calcareous shell (developmentally separate from sclerite formation in the Polyplacophora 22,24 ). The polytomy of Halkieria (and other halkieriids), Neomeniomorpha, and Polyplacophora ( Fig.…”