Colonial origin for Eumetazoa: major morphological transitions and the origin of bilaterian complexity

Abstract

A new hypothesis for the evolution of Bilateria is presented. It is based on a reinterpretation of the morphological characters shared by protostomes and deuterostomes, which, when taken together with developmental processes shared by the two lineages, lead to the inescapable conclusion that the last common ancestor of Bilateria was complex. It possessed a head, a segmented trunk, and a tail. The segmented trunk was further divided into two sections. A dorsal brain innervated one or more sensory cells, which included photoreceptors. “Appendages” or outgrowths were present. The bilaterian ancestor also possessed serially repeated “segments” that were expressed ontogenetically as blocks of mesoderm or somites with adjoining fields of ectoderm or neuroectoderm. It displayed serially repeated gonads (gonocoels), each with a gonoduct and gonopore to the exterior, and serially repeated “coeloms” with connections to both the gut and the exterior (gill slits and pores). Podocytes, some of which were serially repeated in the trunk, formed sites of ultrafiltration. In addition, the bilaterian ancestor had unsegmented coeloms and a contractile blood vessel or “heart” formed by coelomic myoepithelial cells. These cells and their underlying basement membrane confine the hemocoelic fluid, or blood, in the connective tissue compartment. A possible scenario to account for this particular suite of characters is one in which a colony of organisms with a cnidarian grade of organization became individuated into a new entity with a bilaterian grade of organization. The transformation postulated encompassed three major transitions in the evolution of animals. These transitions included the origins of Metazoa, Eumetazoa, and Bilateria and involved the successive development of poriferan, cnidarian, and bilaterian grades of organization. Two models are presented for the sponge‐to‐cnidarian transition. In both models the loss of a flow‐through pattern of water circulation in poriferans and the establishment of a single opening and epithelia sensu stricto in cnidarians are considered crucial events. In the model offered for the cnidarian‐to‐bilaterian transition, the last common ancestor of Eumetazoa is considered to have had a colonial, cnidarian‐grade of organization. The ancestral cnidarian body plan would have been similar to that exhibited by pennatulacean anthozoans. It is postulated that a colonial organization could have provided a preadaptive framework for the evolution of the complex and modularized body plan of the triploblastic ancestor of Bilateria. Thus, one can explore the possibility that problematica such as ctenophores, the Ediacaran biota, archaeocyaths, and Yunnanozoon reflect the fact that complexity originated early and involved the evolution of a macroscopic compartmented ancestor. Bilaterian complexity can be understood in terms of Beklemishev “cycles” of duplication and colony individuation. Two such cycles appear to have transpired in the early evolution of Metazoa. The first gave rise to a mult...

Prey capture and digestion in the carnivorous sponge Asbestopluma hypogea (Porifera: Demospongiae)

“…This confirms its sponge nature, already evident from the similarity of the spicule complement with a common family of non-carnivorous poriferans. This is evidence that a fully functional metazoan with a macrophagous habit could derive from the filter-feeding sponge body plan, which constitutes an actual example of the possibility of transition from sponge to non-sponge metazoans that has been hypothesized in the early evolution of Metazoa (Dewel 2000). However, a functional digestive cavity similar to that of cnidarians is not achieved.…”

“…There is some evidence that all non-poriferan metazoans evolved from a sponge-like organization (Borchiellini et al 2001;Collins and Valentine 2001;Medina et al 2001). If this were true, the poriferan system of water circulation must have been lost during this evolution (Dewel 2000). Carnivorous sponges provide evidence, through a functional example, that such a loss can occur along with an altered mode of nutrition, resulting in an organization able to perform carnivorous feeding.…”

Ultrastructure and formation of the body cavity lining in Phoronis muelleri (Phoronida, Lophophorata)

“…Until today Masterman's idea directly or indirectly influences the discussion on a coelomate ancestor of the Bilateria (Dewel 2000). Even those who argue for an acoelomate ancestor of the Bilateria accept the trimeric organization of the coelom, consisting of proto-, meso-, and metacoel as an indication for a common stem lineage of Phoronida, Bryozoa, and Brachiopoda and the Deuterostomia (Ax , 1995Nielsen 1995).…”

Redox control and the evolution of multicellularity

“…In the case of multicellular animals (metazoans), the first animals were likely clonal or colonial, since basal metazoans (the most primitive living animals) and closely related protists (e.g., choanozoans) exhibit these traits. (8,11) Hypotheses for the evolution of multicellularity in animals must therefore take into account the particular features of clonal and colonial life histories. (8,11,15) In the context of clonal biology, redox control may be of particular consequence.…”

“…(8,11) Hypotheses for the evolution of multicellularity in animals must therefore take into account the particular features of clonal and colonial life histories. (8,11,15) In the context of clonal biology, redox control may be of particular consequence. Consider, for instance, a colonial cnidarian: the arrangements of polyps (feeding structures) and stolons (vascular connections) are major determinants of a colony's ability to acquire food and compete for space.…”