Origins of the other metazoan body plans: the evolution of larval forms

Abstract

Bilaterian animal body plan origins are not solely about adult forms. Most animals have larvae with body plans, ontogenies and ecologies distinct from adults. There are two primary hypotheses for larval origins. The first hypothesis suggests that the first animals were small pelagic forms similar to modern larvae, with adult bilaterian body plans evolved subsequently. The second hypothesis suggests that adult bilaterian body plans evolved first and that larval body plans arose by interpolation of features into direct-developing ontogenies. The two hypotheses have different consequences for understanding parsimony in evolution of larvae and of developmental genetic mechanisms. If primitive metazoans were like modern larvae and distinct adult forms evolved independently, there should be little commonality of patterning genes among adult body plans. However, sharing of patterning genes is observed. If larvae arose by co-option of adult bilaterian-expressed genes into independently evolved larval forms, larvae may show morphological convergence, but with distinct patterning genes, and this is observed. Thus, comparative studies of gene expression support independent origins of larval features. Precambrian and Cambrian embryonic fossils are also consistent with direct development of the adult as being primitive, with planktonic larvae arising during the Cambrian. Larvae have continued to co-opt genes and evolve new features, allowing study of developmental evolution.

Figure 1

Examples of larval forms (four lophotrochozoans): (a) planktotrophic pilidium larva of a nemertine worm; (b) planktotrophic Müller's larva of a platyhelminth flatworm; (c) planktotrophic trochophore of a polychaete annelid; and (d) non-feeding trochophore-like larva of a basal mollusc. All oriented with the apical tuft up. Ciliary bands of various types are present on all. Guts are diagrammed for larvae as shown in (a,c). Adapted with permission from Rouse (2000). © Blackwell Science. Figures courtesy of G. Rouse.

Figure 2

Conflicting larva-first and adult-first hypotheses of bilaterian origins. The hypotheses posit amounts of evolutionary change along branches leading to more derived developmental changes. (a) In the larva-first hypothesis, most evolution of developmental characters lies on the branch leading to the benthic adult, with the larva retaining ancestral features. (b) In the benthic adult-first hypothesis, most evolution lies in the line to the planktonic larva, with the adult retaining ancestral features. Both hypotheses illustrate single lineages, but in the metazoan radiation, numerous lineages evolved in parallel. A large degree of homoplasy resulted in either case. The amount of convergence required to evolve planktonic larvae with their relatively simple organization is substantially less than that to evolve the entire basic suite of adult bilaterian features in 35 or so lineages.

Figure 3

Developmental modes plotted on a bilaterian phylogenetic tree (open bars, direct development; stippled bar, ambiguous developmental mode; filled bars, planktotrophic indirect development; after Jenner (2000) and Peterson et al. (2005)).

Figure 4

Rapid evolution of larvae shown by two congeneric sea urchins, 4 Myr diverged. (a) Planktotrophic pluteus larva of the indirect developer Heliocidaris tuberculata. The notable features are: the arms (ar), each supported by a skeletal rod and bearing a ciliary band; the large gut (g); the mouth (m); and the developing adult rudiment (r) that will grow to become the juvenile sea urchin released at metamorphosis (approx. six weeks post-fertilization). (b) Non-feeding direct-developing larva of Heliocidaris erythrogramma. All internal features are those of the developing adult. Metamorphosis is 3–4 days post-fertilization (scale bar, 100 μm).