Unravelling body plan and axial evolution in the Bilateria with molecular phylogenetic markers

jaume baguna, pere martinez, jordi paps and marta riutort setting the problem

The emergence of dramatic morphological differences (disparity) and the ensuing bewildering increase in the number of species (diversity) documented in the fossil record at key stages of animal and plant evolution have defied, and still defy, the explanatory powers of Darwin's theory of evolution by natural selection. Among the best examples that have captured the imagination of the layman and the interest of scores of scientists for 150 years are the origins of land plants from aquatic green plants, of flowering plants from seed plants, of chordates from non-chordates and of tetrapod vertebrates from non-tetrapods; and the conquest of the land by amphibians; the emergence of endotherms from ectotherm animals; the recurrent invention of flight (e.g. in arthropods, birds and mammals) from non-flying ancestors; and the origin of aquatic mammals from four-legged terrestrial ancestors.

Key morphological transitions pose a basic difficulty: reconstruction of ancestral traits of derived clades is problematic because of a lack of transitional forms in the fossil record and obscure homologies between 'ancestral' and derived groups. Lack of transitional forms, in other words gaps in the fossil record, brought into question one of the basic tenets of Darwin's theory, namely gradualism, as Darwin himself acknowledged. Since Darwin, however, and especially in the past 50 years, numerous examples that may reflect transitional stages between major groups of organisms have accumulated. Good examples

Evolving Pathways: Key Themes in Evolutionary Developmental Biology, ed. Alessandro Minelli and Giuseppe Fusco. Published by Cambridge University Press. # Cambridge University Press 2008.

are the numerous fossils that connect whales, sirenians, seals and sea lions with different lineages of terrestrial mammals, the converse transitional series from swimming tetrapods to land tetrapods, the many fossils showing the transition from dinosaurs to birds illuminating the origin and early functions of feathers and flight, and those fossils illustrating the intermediate changes during the transition from aquatic green plants to land plants and from these to vascular plants.

Back in geological time, the last and potentially crippling example to the acceptance of the Darwinian theory is the advent of bilaterally symmetrical animals and its coincidence with the abrupt appearance of large-bodied skeletonised remains of most extant phyla. The event is usually referred to as the Cambrian 'explosion'. A great deal has been written about it, namely the recent reviews by Budd (2003), Valentine (2004), Conway Morris (2006) and Marshall (2006), to which readers are referred. In the writings of Gould (1989) the Cambrian 'explosion' has been considered the pivotal event in animal evolution for which special mechanisms have been sought, e.g. in terms of macro-evolutionary events. However, because the Cambrian 'explosion' mainly refers to the 'explosion' of bilaterally symmetrical body plans, we will argue that an understanding of the origin of bilateral organisms is even more important than the so-called Cambrian 'explosion', as well as a necessary step to explain it.

tracking down the earliest extant bilaterians:

a simple or a complex last common ancestor (lca)?

By any standard, the appearance of bilateral organisms is the most thrilling success in animal evolution: 34 out of the 38 living phyla and over 99% of described living animal species are bilaterians, far more complex in structure and far more diverse in morphology and ecology than their radial forebears. A brief glimpse at any bilaterian organism, however simple, uncovers the main reasons for their evolutionary success: two oriented body axes and directed locomotion. The main or primary axis (antero-posterior, or A-P) distinguishes 'front' from 'back' of the body and is associated with the direction of locomotion, with the mouth, brain and sensory structures located at or near the anterior end, and the anus and other structures located at or near the posterior end. The second axis (dorso-ventral or D-V), orthogonal to the first, identifies the 'top' from the 'bottom' of the body, the latter usually related to locomotion, while the 'top' or dorsal bears sensory and defensive structures to avoid predation. Oriented locomotion was the key to the colonisation by the pre-Cambrian benthos and thereafter the plankton, and aided by the development of sensory structures and feeding organs at the anterior/ventral end that increased predatory and escape capabilities. Another key feature of bilaterians is the presence of a third embryonic layer, the mesoderm, between the ectoderm and endoderm. In combination with either the ecto- or endoderm, the mesoderm provides an extraordinary variety of new tissues and organs not seen in any radial organism. Finally, other features often considered to be present in the first bilaterians are a true brain, a through-gut, excretory system, body cavities (coelom), segments, and even appendages and simple hearts and eyes (Table 12.1).

Current views suggest that the bilaterians arose from ancestors that were radially symmetric instead of bilateral and, therefore, had a single body axis (the oral-aboral, or O-AB) and no mesoderm (hence diplo-blastic). In addition, they had a decentralised nerve net and a blind gut. These features are maintained by the extant members of the phylum

Table 12.1 Character states of the main morphological and developmental components at the dawn of bilaterians. The simple Urbilateria scenario assumes a structurally simple organism. The alternative complex Urbilateria scenario considers that most morphological and developmental components of extant bilaterians were also functionally conserved in the bilaterian ancestor.

Developmental and

Table 12.1 Character states of the main morphological and developmental components at the dawn of bilaterians. The simple Urbilateria scenario assumes a structurally simple organism. The alternative complex Urbilateria scenario considers that most morphological and developmental components of extant bilaterians were also functionally conserved in the bilaterian ancestor.

Developmental and

morphological characters

Simple Urbilateria

Complex Urbilateria

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