The origin of the pelagobenthic metazoan life cycle: what's sex got to do with it?

The biphasic (pelagobenthic) life cycle is found throughout the animal kingdom, and includes gametogenesis, embryogenesis, and metamorphosis. From a tangled web of hypotheses on the origin and evolution of the metazoan pelagobenthic life cycle, current opinion appears to favor a simple, larval-like holopelagic ancestor that independently settled multiple times to incorporate a benthic phase into the life cycle. This hypothesis derives originally from Haeckel's (1874) Gastraea theory of ontogeny recapitulating phylogeny, in which the gastrula is viewed as the recapitulation of a gastracan ancestor that evolved via selection on a simple, planktonic hollow ball of cells to develop the capacity to feed. Here, we propose an equally plausible hypothesis that the origin of the metazoan pelagobenthic life cycle was a direct consequence of sexual reproduction in a likely holobenthic ancestor. In doing so, we take into account new insights from poriferan development and from molecular phylogenies. In this scenario, the gastrula does not represent a recapitulation, but simply an embryological stage that is an outcome of sexual reproduction. The embryo can itself be considered as the precursor to a biphasic lifestyle, with the embryo representing one phase and the adult another phase. This hypothesis is more parsimonious because it precludes the need for multiple, independent origins of the benthic form. It is then reasonable to consider that multilayered, ciliated embryos ultimately released into the water column are subject to natural selection for dispersal/longevity/feeding that sets them on the evolutionary trajectory towards the crown metazoan planktonic larvae. These new insights from poriferan development thus clearly support the intercalation hypothesis of bilaterian larval evolution, which we now believe should be extended to discussions of the origin of biphasy in the metazoan last common ancestor.

Prismatic dentine in the Australian lungfish, Neoceratodus forsteri (Osteichthyes : Dipnoi)

The Australian lungfish, Neoceratodus forsteri, has a dentition consisting of enamel, mantle dentine and bone, enclosing circumdenteonal, core and interdenteonal dentines. Branching processes from cells that produce interdenteonal dentine leave the cell surface at different angles, with collagen fibrils aligned parallel to the long axis of each process. In the interdenteonal dentine, crystals of calcium hydroxyapatite, form within fibrils of collagen, and grow within a matrix of non-collagenous protein. Crystals are aligned parallel to the cell process, as are the original collagen fibrils. Because the processes are angled to the cell surface, the crystals within the core or interdenteonal dentine are arranged in bundles set at angles to each other. Apatite crystals in circumdenteonal dentine are finer and denser than those of the interdenteonal dentine, and form outside the fibrils of collagen. In mature circumdenteonal dentine the crystals of circumdenteonal dentine form a dense tangled mass, linked to interdenteonal dentine by isolated crystals. The functional lungfish tooth plate contains prisms of large apatite crystals in the interdenteonal dentine and masses of fine tangled crystals around each denteon. This confers mechanical strength on a structure with little enamel that is subjected to heavy wear. (c) 2006 Elsevier Ltd. All rights reserved.