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

Abstract

Despite the embryological and anatomical disparities present among lophotrochozoan phyla, there are morphological similarities in the cellular arrangements of ciliated cells used for propulsion among the nonfeeding larval forms of kamptozoans, nemerteans, annelids, mollusks, and bryozoans. Evaluating whether these similarities are the result of convergent selective pressures or a shared (deep) evolutionary history is hindered by the paucity of detailed cellular information from multiple systematic groups from lesser-known, and perhaps, basal evolutionary phyla such as the Bryozoa. Here, I compare the ciliary fields and musculature among the major morphological grades of marine bryozoan larvae using light microscopy, SEM, and confocal imaging techniques. Sampling effort focused on six species from systematic groups with few published accounts, but an additional four well-known species were also reevaluated. Review of the main larval types among species of bryozoans and these new data show that, within select systematic groups of marine bryozoans, there is some conservation of the cellular arrangement of ciliary fields and larval musculature. However, there is much more morphological diversity in these structures than previously documented, especially among nonfeeding ctenostome larval types. This structural and functional diversification reflects species differences in the orientation of the apical disc during swimming and crawling behaviors, modification of the presumptive juvenile tissues, elongation of larval forms in the aboral-oral axis, maximizing the surface area of cell types with propulsive cilia, and the simplification of ciliary fields and musculature within particular lineages due to evolutionary loss. Considering the embryological origins and functional plasticity of ciliated cells within bryozoan larvae, it is probable that the morphological similarities shared between the coronal cells of bryozoan larvae and the prototrochal cells of trochozoans are the result of convergent functional solutions to swimming in the plankton. However, this does not rule out cell specification pathways shared by more closely related spiralian phyla. Overall, among the morphological grades of larval bryozoans, the structural variation and arrangement of the main cell groups responsible for ciliary propulsion have been evolutionarily decoupled from the more divergent modifications of larval musculature. The structure of larval ciliary fields reflects the functional demands of swimming and substrate exploration behaviors before metamorphosis, but this is in contrast to the morphology of larval musculature and presumptive juvenile tissues that are linked to macroevolutionary differences in morphogenetic movements during metamorphosis.

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

“…What have traditionally been referred to as the carnose and stoloniferous ctenostome bryozoans may not be natural groupings, and the organization of families within superfamily assemblages often depends on the interpretation given to a few zooidal characters. For the reasons discussed in Santagata (2008), I will retain Nolella stipata under the superfamily Victorelloidea. Since many structures and cell types for bryozoan larvae have been originally described from cheilostome bryozoans, it is simplest to begin with these forms.…”

“…Current morphological and molecular phylogenetic evidence resolves the bryozoans within the Lophotrochozoa and suggests that the suite of larval and adult colonial traits expressed by basal ctenostome (uncalcified) bryozoans represents the pleisiomorphic condition for the phylum (Dick et al, 2000;Todd, 2000;Waeshenbach et al, 2006). Recent efforts to broaden the taxonomic scope of knowledge concerning bryozoan larval morphologies have revealed that the structural and functional diversity in the main propulsive ciliary fields and musculature is much greater within nonfeeding ctenostome larval types than in other grades of bryozoans (Santagata, 2008). Much of this structural variation is linked to the musculature involved with tissue rearrangements at metamorphosis and to maximizing the surface area of ciliary fields used for propulsion.…”

“…Perhaps the most significant problem has been the mapping of all neuronal cell types within the nervous system and reconstructing the pathways of sensory/motor fibers in three dimensions. Much of the diversity in ciliary fields has been reviewed Reed, 1991;Santagata, 2008), but in general, sensory types are classified by the morphology of their multiciliated tufts and position relative to the main propulsive ciliary fields-the coronal cells and oral ciliated cells. According to this classification scheme, sensory structures are found in three general regions of the larval surface: (1) within a band of oligociliated cells called the supracoronal cells that are positioned aborally to the coronal cells and bordered by the pallial epithelium, (2) between adjacent coronal cells are the intercoronal cells, and (3) within an unciliated (and often undifferentiated) band of cells called the infracoronal cells that are oral to the coronal cells.…”

“…According to this classification scheme, sensory structures are found in three general regions of the larval surface: (1) within a band of oligociliated cells called the supracoronal cells that are positioned aborally to the coronal cells and bordered by the pallial epithelium, (2) between adjacent coronal cells are the intercoronal cells, and (3) within an unciliated (and often undifferentiated) band of cells called the infracoronal cells that are oral to the coronal cells. The classification of sensory cell types is somewhat unclear within particular lineages in which the typical cellular characteristics of the coronal cells have been lost (see Santagata, 2008), and also when any of the previously mentioned cellular bands are either expanded or reduced. In these cases, a comparative study on more closely related species often provides insight into the derivation of ciliary fields and sensory cell types.…”

“…Here, I demonstrate that regardless of the morphological divergence that is found in the gross larval anatomy among marine bryozoans, the larval nervous system and its major effector organs are largely molded on the basis of the functional demands of feeding, ciliary propulsion, phototactic behaviors, and substrate exploration. Considering the evolutionary relationships among the morphological grades of marine bryozoans, lineages within the ctenostomes and cheilostomes are independently evolving larval traits that convey a greater range of sensory abilities and increased propulsive capacity (Santagata, 2008). The shared absence of specific neuromuscular structures in several lineages is likely the result of convergent evolutionary loss.…”