The Functional Morphology of Avicularia in Cheilostome Bryozoans

Abstract

<p>Avicularia are modified zooids characteristic of cheilostome bryozoans. Through evolutionary time the functional capacity of the polypide has evolved and is now a vestigial feature within the avicularium. The functional role of avicularia in the colony is unclear. Unable to feed, avicularia are dependent on nutrients from the parental or neighbouring zooids and therefore constitute a significant metabolic cost in production and maintenance, a cost which must be met by some reciprocal function. Details on the functional morphology of avicularia are severely lacking with avicularia constituting a large gap in the knowledge of cheilostome biology. By examining their biology, this study will enhance our understanding of the evolution and functional capacity of avicularia. Fundamentally this study will provide insight into the degree of morphological and morphometric divergence among avicularia. The objective of this study was to: (1) conduct a morphological survey of the putative sensory structures associated with the palate (or orificial structures) of avicularia (SEM); (2) conduct an ultrastructural-level study (TEM) of the vestigial polypide from two species of bugulids from disparate habitats; and (3) incorporate a holistic study on the behaviour and functional evolution of character traits in Bugula flabellata. The avicularia from 38 species of cheilostome bryozoans were examined covering 11 superfamilies, 18 families and 29 genera. The results indicate that avicularia are morphologically diverse and display extensive variation in avicularian orifice morphology. Structures associated with the orifice varied from tufts of cilia, simple pores, tubular protuberances, and pores with an organic exude. The adventitious avicularia dominated (83%) and displayed the greatest morphometric diversity compared with interzooidal, vicarious and vibracular types. Within superfamilies, only the catenicellids displayed a significant level of morphometric and anatomical congruence. The density of avicularia within a colony was greatest by combining adventitious and vibracular types (e.g. Caberea). This finding may represent an evolutionary shift towards maximisation of function within a smaller spatial scale. The ultrastructure of the vestigial polypide of the subtidal B. flabellata and deep-sea Nordgaardia cornucopioides revealed disparities suggestive of differing functional roles either as a result of habitat differences or differing stages of evolutionary development. The avicularium of B. flabellata has undergone significant modification in character traits from the plesiomorphic autozooid. The current anatomy and behaviour of this avicularium provides strong evidence for a mechanoreceptive function whereby detection of tactile stimuli from passing invaders is important in the functional role of the bird's-head avicularium of B. flabellata. This study is the first to examine the functional morphology of avicularia in such detail. The techniques used in this study have never been applied to avicularia before allowing numerous features such as the muscles, orificial structures and vestigial polypide anatomy to be discerned. The results indicate that avicularia are morphologically diverse and anatomically equipped to perform a variety of functions. The morphological diversity of avicularia may be of immense ecological importance and represent differing responses to various selective pressures in the environment.</p>

Origin of division of labor is decoupled from polymorphism in colonial animals

“…As with gene duplication, independent lineages may follow different evolutionary paths. This result explains why it is so difficult to pinpoint a single ancestral function of avicularia, because the later species of Wilbertopora already possess avicularian forms similar to the general classes of avicularian types observed today (14).…”

“…Many cheilostome bryozoans today have evolved division of labor, where their 'zooids', or colony members, perform specialized tasks within the colony and express different morphologies, termed polymorphism (3,(14)(15)(16)(17). The most common polymorphs include: autozooids that feed and produce gametes, ovicells that brood embryos (18), and avicularia that perform varied tasks from defense to hygiene ( [13], Fig.…”

“…Polymorphs in extant bryozoans can have discrete and continuous differences in both the types and ranges of their morphologies, which reflect differences in the mode and range of their functions (14,24). In extant colonies and lineages, autozooids and ovicells have constrained morphologies, corresponding to their functional requirements-avicularia show greater morphological variation, perhaps reflecting the many tasks they can perform (25).…”

“…For example, in gene duplication, one copy maintains ancestral functions while the other can evidently accommodate mutations (and thus eventually accrue new functions) (12). Modules in colonial animals may show similar dynamics, where some members of the colony maintain ancestral functions (13) and others see increased variation while maintaining viability owing to physiological connections with the rest of the colony (direct gut-to-gut connections in bryozoans or communal feeding in ants) (10,14). To test the relative contributions of functional and morphological change to the evolution of division of labor, we couple direct observations on the functional and morphological variation in an evolutionary time series of a fossil bryozoan lineage with a model of energetic flux.…”