Phylogenetic Framework

Understanding the pattern of developmental and morphological change leading to the diversity of existing animal bodyplans and others documented only from the fossil record requires a well-developed phylogenetic framework. Fortunately, combined molecular and morphological data sets have revolutionized our views of metazoan relationships over the past several decades (see recent reviews by Eernisse and Peterson, 2004; Halanych, 2004; Giribet, 2003; Valentine, 2004). The growing number of workers in this area and the steady development of both analytical techniques and growing data sets will probably provide further surprises in the years ahead.

A number of nodes on the metazoan tree remain uncertain, but consensus between molecular and morphological analyses has been achieved in others. Several critical issues in metazoan phylogeny remain in dispute (contrast Fig. 1A and Fig. 1B). Areas of agreement include: 1) Choanoflagellates are the closest sister group to metazoans; 2) The siliceous and calcareous sponges arose independently (e.g., Botting and Butterfield, 2005 and references therein); 3) Ctenophores are the most basal Eumetazoan clade, with cnidarians the next most basal branch; 4) The Ecdysozoa (Arthropoda,

Figure 1. Phylogenetic framework for the metazoa used in this paper, based on recent molecular and morphological analyses. This topology largely follows Eernisse and Peterson (2004). Fig. 1A shows the topology accepted by many, uniting the Ecdysozoa and the Lophotrochozoa into the classic protostomes. Fig. 1B shows Eernisse and Peterson's preferred topology with the Ecdysozoa the sister clade to the deuterostomes, to the exclusion of the Lophotrochozoa. The square represents the position of the Urbilaterian node in the two topologies.

Figure 1. Phylogenetic framework for the metazoa used in this paper, based on recent molecular and morphological analyses. This topology largely follows Eernisse and Peterson (2004). Fig. 1A shows the topology accepted by many, uniting the Ecdysozoa and the Lophotrochozoa into the classic protostomes. Fig. 1B shows Eernisse and Peterson's preferred topology with the Ecdysozoa the sister clade to the deuterostomes, to the exclusion of the Lophotrochozoa. The square represents the position of the Urbilaterian node in the two topologies.

tardigrades, nematodes and priapulids plus others) are a monophyletic clade (Giribet, 2003). Areas of continuing uncertainty involve: 1) The position of the acoel flatworms, which have been separated from the remaining playhelminthes and appear to be the most basal bilaterians (Ruiz-Trillo et al., 1999); 2) The relationships among the remaining major bilaterian clades. Since Aguinaldo et al. (1997), many have accepted the division between three large bilaterians subclades, the Ecdysozoa (arthropods, priapulids and allies), the deuterostomes (chordates, echinoderms and hemichordates) and the lophotrochozoans (annelids, molluscs, lophophorates and others). Although the Lophotrochozoa and Ecdysozoa have generally been united in the classic protostomes (Fig. 1A) Eernisse and Peterson note that there is a lack of support for this claim, and their analysis shows the Lophotrochozoa and deuterostomes as sister taxa (Fig. 1B) while Philip et al. (2005) claim support for the old coelomata hypothesis of arthropoda + chordata based on their molecular phylogeny. Halanych (2004), although cognizant of the difficulties identified by Eernisse and Peterson favors the Ecdysozoan + Lophotrochozoan topology based on the purported lophotrochozoan signatures in five hox genes (Balvoine et al., 2002) as does Phillippe et al.'s (2005) reanalysis of molecular data. Note that the classic protostome-deuterostome ancestor does not exist in topology 1B where the critical node becomes the origin of the Bilateria and thus the critical hypothetical ancestor is that of the Urbilateria.

2.2 Unicellular Development

Multicellularity arose multiple times across a variety of eukaryotic lineages (Buss, 1987; Kaiser, 2001; King, 2004). The asymmetric pattern of these appearances suggests that some clades possessed more of the requirements for multicellularity than others (King, 2004). It has long been apparent that many features once considered as defining elements of the Metazoa are shared with a range of unicellular ancestors (see discussions in Wolpert, 1990, Erwin, 1993). On a molecular level, the specific cell-cell signalling pathways are also highly conserved (e.g., Gerhart, 1999).

The similarities between choanoflagellates and the collar cells of sponges have fueled views that they were the closest relatives of metazoa, a view now amply supported by molecular evidence (reviewed by King, 2004). The antecedents of cell adhesion, signal transduction and cellular differentiation are all found among the choanoflagellates. King et al. (2003) analyzed more than 5000 expressed sequence tags (ESTs) to identify representatives of a number of cell signalling and adhesion protein families in two choanoflagellate species. They found a variety of elements involved in cell-cell interactions in Metazoa including cadherins, C-type lectins, tyrosine kinases, and discovered that cell proliferation is controlled by tyrosine kinase inhibitors. Their presence in choanoflagellates demonstrates that they are exaptations co-opted for their role in animals. Much of metazoan diversity of tyrosine kinases, a critical component in cell proliferation and differentiation, apparently evolved between choanoflagellates and the base of Metazoa (Suga et al., 2001), perhaps via rapid shuffling of protein domains (King, 2004).

Thus by the time extant metazoan lineages appeared, the earliest metazoa had acquired an extracellular matrix for cell support, differentiation and movement (as has long been apparent from microscopy); differentiated cell types produced by linking signalling pathways and the multitude of metazoan-specific transcription factors (Degnan et al., 2005); cell junctions to facilitate communication between cells and the extra-cellular communication mediated by the tyrosine kinases.

2.3 Poriferan Development

In a recent review of sponge development Müller et al. (2004) described them as "complex and simple but by far not primitive" (p. 54). Müller and his group in Mainz coined the term "Urmetazoan" for the ancestral metazoan and for the past decade have been applying a range of molecular techniques to understanding the novelties that lie at the base of the metazoa. The urmetazoan appears to have had a suite of cell adhesion molecules with intracellular signal transduction pathways, the ability to produce morphogenic gradients, an immune system and a simple ability to pass messages between nerve cells (Müller, 2001; Müller et al., 2004: this is the basis for the following review). Sponge morphogenesis is facilitated by extracellular morphogens and several transcription factors. Two T-box transcription factors have been recovered from the demosponge Suberites douncula, one a Brachyury homologue and the other related to Tbx3-4-5 from chordates; the former appears to be involved in axis formation. A Forkhead homologue has also been recovered from sponges and is apparently active in early morphogenetic cell movements. Among the homeodomain genes, a paired-class gene (Pax-2/5/8) and LIM and Iroquois transcription factors have been isolated and the available information suggests they are expressed in specific tissue regions. The identification of a frizzled gene, a receptor in the Wnt pathway, and other components has demonstrated that the Wnt signalling pathways is involved in cell specification and morphogenesis. The cell-cell and cell-matrix adhesion molecules include receptor tyrosine kinases, but cell adhesion is a prerequisite for immunity. The sponge immune system contains Ig-like molecules and pathways similar to deuterostomes, but not protostomes. (This is an interesting pattern that we will see repeatedly, with closer affinities between pre-bilaterians and deuterostomes than with protostomes.) Apopotosis (programmed cell death) also occurs among sponges, with molecules identified that are similar to tumor necrosis factor-a and caspases.

Müller et al. (2004) proposed a model for the appearance of the urmetazoan in which the critical evolutionary innovation was the construction of cell-cell and cell-matrix adhesion systems. This allowed cell aggregates to form and signal transduction facilitated cell differentiation and specialization. The addition of an immune system, apopototic machinery and the initial transcription factors permitted homeostasis and furthered differentiation of a body axis. Müller et al. do not consider the developmental data from choanoflagellates, but the presence of cell adhesion factors and the diversity of tyrosine kinases (King et al., 2003) is generally consistent with the Müller hypothesis.

Figure 2. Major developmental innovations leading to the origin of bilateria, emphasizing features shared with sponges, cnidarians and acoel flatworms. See text for discussion.

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