Comparison of the neuromuscular systems among actinotroch larvae: systematic and evolutionary implications

Abstract

A comparative analysis of the larval and presumptive juvenile neuromuscular systems among actinotroch larvae was performed using confocal laser microscopy with probes for F-actin and serotonin. Currently, there are two main categories of larval nervous systems based on the origin of the nerve fibers that innervate the larval tentacles. Characteristics of the serotonergic cells of the larval apical ganglion and juvenile nervous system have remained relatively conserved, but the structure of the secondary (hood) sense organ and the juvenile tentacles has diversified among species. Differences in larval musculature are mainly associated with differences in hood morphology. The presumptive, juvenile neuromuscular system is either integrated or separated from that of the larva based on the origin of the juvenile tentacles. Among species, the juvenile tentacles are made by remodeling the larval tentacles, developed from a basal tentacular thickening, or developed as a completely separate set in the larva. Differentiation of the neuromuscular structures of the juvenile tentacles is more diverse than their outward morphological characteristics would suggest. Importance of these larval characters is discussed in terms of current problems that exist within phoronid systematics. Evolutionary implications of these morphological characters are discussed among the phoronids, brachiopods, and related bilaterians. Overall, the integration or separation of larval and juvenile neuromuscular characters may yield insights into the evolution of lophotrochozoan body plans.

Evolutionary and Structural Diversification of the Larval Nervous System Among Marine Bryozoans

“…Similar features were noted for the creeping larva of the entoproct Loxosomella murmanica (Wanninger et al, 2007). Phoronids and brachiopods have different levels of functional and developmental integration of their larval and juvenile tissues among species (detailed in Santagata and Zimmer, 2002), but in general, the juvenile neuromuscular system is developed precociously within the body of the larva, and neuronal connections are shared between the larval nervous system (apical ganglion and tentacular nerve rings) and the juvenile neuromuscular system. Contrary to these examples, the tissues that eventually form the polypide and cystid of bryozoan ancestrulae are largely undifferentiated in all bryozoan larval forms except for those of phylactolaemates (see Franzen and Sensenbaugh, 1983).…”

“…Despite deep evolutionary conservation of serotonin as a signal molecule among metazoans (Hay-Schmidt, 2000), failure of the available serotonin antibody to label all serotonergic cell types in particular evolutionary lineages cannot be ruled out. However, despite many morphological differences among the larval nervous systems of the "lophophorates" and those of annelids and molluscs, phoronids and brachiopods also have numerous serotonergic cells, consisting of bipolar sensory cells and additional peripheral cells, in their apical organs (Santagata, 2002;Santagata and Zimmer, 2002). The cyphonautes larva of Membranipora membranacea and the nonfceding larva of Bugula neritina each have a single pair of serotonergic neural plate cells within their respective apical discs (this paper and Pires and Woollacott, 1997).…”

“…One additional theme among lophotrochozoan nervous systems is the repeated heterochronic shifts that occur with respect to the separation or integration of larval and juvenile tissues (Santagata and Zimmer, 2002). Overall, the larvae of annelids, molluscs, and sipunculids show a general trend toward developing the juvenile (post-trochal) nervous system precociously and integrating it with that of the larval (pre-trochal) nervous system.…”

“…The more divergent morphologies present within the Lophotrochozoa confound traditional evolutionary interpretations of many larval and adult characters, especially with regard to the "lophophorates." More recent studies on the development and larval anatomy of phoronids and brachiopods have expanded our understanding of their evolutionary affinities (Santagata and Zimmer, 2002;Santagata, 2004b;Cohen and Weydmann, 2005). However, often left anatomically and phylogenetically orphaned by these reports, are the bryozoans.…”

The morphology and evolutionary significance of the ciliary fields and musculature among marine bryozoan larvae

“…Several investigations have concluded that the transition from a feeding to a nonfeeding larva (or vice versa) is a common evolutionary switch among marine invertebrates having no significant phylogenetic signal (Hart et al, 1997;Duda and Palumbi, 1999;Nü tzel et al, 2006). However, in some cases, the structure of larval and presumptive juvenile tissues is conserved among closely related species (Lyke et al, 1983;Santagata and Zimmer, 2002).…”