Phylogenetic Context and Basal Metazoan Model Systems1

Integrative and Comparative Biology, Sep 2005 by Collins, Allen G, Cartwright, Paulyn, McFadden, Catherine S, Schierwater, Bernd

SYNOPSIS.

In comparative studies using model organisms, extant taxa are often referred to as basal. The term suggests that such taxa are descendants of lineages that diverged early in the history of some larger taxon. By this usage, the basal metazoans comprise just four phyla (Placozoa, Porifera, Cnidaria, and Ctenophora) and the large clade Bilateria. We advise against this practice because basal refers to a region at the base or root of a phylogenetic tree. Thus, referring to an extant taxon or species as basal, or as more basal than another, can be misleading. While much progress has been made toward understanding some of the phylogenetic relationships within these groups, the relationships among them are still largely not known with certainty. Thus, sound inferences from comparative studies of model organisms demand continued illumination of phylogeny. Hypotheses about the mechanisms underlying metazoan evolution can be drawn from the study of model organisms in Cnidaria, Ctenophora, Placozoa, and Porifera, but it is clear that these model organisms are likely to be derived in many respects. Therefore, testing these hypotheses requires the study of yet additional model organisms. The most effective tests are those that investigate model organisms with phylogenetic positions among two sister groups comprising a larger clade of interest.

INTRODUCTION

As the rest of this volume attests, enormous insight can be gained through the study of model organisms belonging to the animal groups that diverged earliest in the history of Metazoa. Specifically, detailed knowledge of these so-called "basal metazoans" makes it possible to conceive of and evaluate hypotheses concerning early animal evolution, and these in turn provide clues about the origin of metazoan diversity. A key element of these comparative studies is that they are placed in a sound phylogenetic context. Thus, our aims in this review are threefold. First, we attempt to clarify how use of the term basal, as in the title of this symposium, can often lead to confusion. Second, we review current understanding of phylogenetic relationships between and within the early-diverging metazoan groups. Our discussion of Porifera is slight because a recent symposium (Integr. Comp. Biol., Vol. 45, 2) was dedicated entirely to this group, and Cnidaria is treated in greater depth because cnidarians outnumber the other groups in terms of model organisms. Finally, we reiterate and illustrate the importance of phylogenetic hypotheses for interpreting the evolutionary significance of observations made upon model organisms.

WHAT DOES BASAL MEAN?

In the context of a discussion of evolutionary relationships, basal refers to the region of the base or root of a phylogenetic tree. Often basal is used as an adjective to describe clades or taxa that branch near the root of a hypothesized phylogeny. For instance, as of 14 March 2005, a search of Google Scholar using the terms "basal Metazoa" OR "basal metazoan" OR "basal cnidarian" brings up 126 results, the vast majority representing papers dealing with model organisms published within the last six years. None of these papers define what a basal taxon is, but one can infer that the term is applied to taxa (often species) that derive from lineages that diverged early in the history of some larger clade. This usage can lead to conceptual problems (see also Krell and Cranston, 2004; Crisp and Cook, 2005). For example, in terms of metazoan phylogeny, there is little doubt that the lineages leading to extant members of the phyla Cnidaria, Ctenophora, Placozoa, and Porifera diverged relatively early in the history of Metazoa, and it is to these taxa (less Porifera) that "basal Metazoa" refers in the title of this symposium. However, Bilateria has a comparably ancient divergence within Metazoa because it is in all likelihood the sister group to one or some combination of these four phyla, and therefore is basal in the same sense.

Bilateria is probably not thought of as a basal metazoan group because bilaterians are relatively complex and likely derived in many respects, highlighting what might be a common misunderstanding about the word. Basal carries no explicit connotation about character states (see Crisp and Cook, 2005). Nevertheless, representatives of early-diverging taxa appear often to be chosen as subjects in comparative studies because of a priori expectations that these basal taxa possess character states that are more likely to be ancestral relative to those of later diverging taxa. Only in a comparative context can it be determined if these prior expectations are borne out. As a case in point, recent studies of gene expression have brought into question whether radial symmetry and diploblasty, two characters often assumed to be ancestral for Cnidaria, are actually derived from bilateral symmetry and triploblasty inherited from the common ancestor of cnidarians and bilaterians (Finnerty et al., 2004; Martindale et al., 2004)

We concur with Krell and Cranston (2004) that taxa should not be identified as more (or less) basal than others, and that making explicit statements about relationships, especially sister group relationships, would lead to greater clarity in phylogenetic and evolutionary discussions. For example, Anthozoa, widely accepted as the sister group to all other cnidarians (Bridge et al., 1992; and see discussion in Marques and Collins, 2004), is often referred to as basal within Cnidaria. The impression that Anthozoa is the basal cnidarian group may depend upon the taxa being discussed. In the context of relationships among cnidarian taxa assigned the Linnaean rank of class, Anthozoa may be perceived as basal (Fig. 1A). However, this tree can be redrawn with Anthozoa presented in greater phylogenetic detail, exposing much of the diversity present within it, and Medusozoa (comprising non-anthozoan cnidarians) in lesser detail (Fig. 1B). Relative to those leading to the orders within Anthozoa, the lineage leading to Medusozoa diverges earliest within Cnidaria. In this context, Medusozoa might therefore be perceived as the basal cnidarian group, even though the underlying hypothesized relationships are unchanged. Use of this example may appear as gamesmanship, but we contend that elements of both arbitrariness and subjectivity are often conveyed in statements about the basal taxon of a group (see also Crisp and Cook, 2005).