lesser-known protostome taxa: An introduction and a tribute to Robert P. Higgins, The

Integrative and Comparative Biology, Jun 2002 by Garey, James R

The Lesser-Known Protostome Taxa: An Introduction and a Tribute to Robert P. Higgins1

SYNOPSIS. Most biologists are familiar only with a few of the approximately 40 extant animal phyla. The purpose of this symposium was to renew interest in the lesser-known invertebrate taxa, encourage their use in research and teaching and to promote the relevance of high-level systematic studies. This paper reviews the two major views of metazoan evolutionary relationships with particular attention to the lesser-known taxa and to some of the new and/or conflicting terminology used in current animal phylogenetic study. The current use of lesser-known taxa in research is briefly described, and the discussion that followed the symposium is summarized. The paper concludes with a brief history of the symposium and a tribute to Robert P. Higgins, who organized three "Symposia on the Lesser-Known Invertebrates" over the past 25 yr.

INTRODUCTION

Most biologists are familiar with only a few of the approximately 40 extant animal phyla such as annelids, arthropods, molluscs, echinoderms and chordates. How many are familiar with the more obscure groups such as gnathostomulids, kinorhynchs, priapulids and cycliophorans? This symposium was designed to play a role in renewing interest in the lesser-known animal groups, encourage their use in research and teaching and promote the relevance of high-level systematic studies. The symposium was restricted to protostomes simply to narrow the scope so that it could be completed in a single day. The order of papers in this volume is random and not related to the phylogenetic position of the taxa. The participants of the symposium are shown in Figure 1.

Current advances in evolutionary, developmental and ecological studies make it apparent that the lesser-- known animal groups are important subjects of study. Now that we have the tools to study both molecular and morphological aspects of animal evolution it is clear that we cannot understand animal evolution without paying attention to the lesser-known taxa (Garey and Schmidt-Rhaesa, 1998). Many lesser-known groups are far more important ecologically than is generally known, particularly the phyla represented by mostly meiofaunal (microscopic) species. The small body size of many of these species has confounded their placement in metazoan phylogeny. Advances in ultrastructure-level morphology and molecular analysis show promise in determining the relationships of these groups to metazoans as a whole, and it is certain that the lesser-known taxa will play an important role in future studies of metazoan phylogeny.

THE PLACEMENT OF THE LESSER-KNOWN GRoups WITHIN METAZOA

This section reviews the morphological and molecular evidence used to define evolutionary relationships among the Metazoa. Some of the conflicting terminology and definitions of various monophyletic groups used in other papers from these proceedings will be clarified as well. For reviews of morphological analyses, see the recent works of Nielsen (2001) and Ax (1996, 2000). Molecular and combined analyses are reviewed in Garey (2001), Giribet et al. (2000), Peterson and Eernisse (2001), and Zrzavy et al. (1998).

In the traditional view, segmented protostomes are placed together in a clade known as Articulata (Cuvier, 1812), and lophophorates are considered to be basal deuterostomes (Nielsen, 2001). In recent years, a new hypothesis of evolution has been proposed in which all molting animals fall into a single clade called Ecdysozoa (Aguinaldo et al., 1997) and in which the lophophorate groups are considered to be protostomes rather than deuterostomes (Halanych et al., 1995; Mackey et al., 1996). Although controversial, this new hypothesis is gaining significant support in the scientific community (e.g., see Adoutte et al., 2000). These unresolved conflicting views of metazoan phylogeny cause considerable confusion in the interpretation of the current literature. To complicate matters, terminology used to describe the higher taxonomic groupings of metazoans is somewhat fluid, and the names used by American and European workers differ. Table 1 defines some of these terms.

Two contrasting hypotheses of animal phylogeny are shown in Figure 2, one based on the Articulata concept, the other on Ecdysozoa. Articulata (Cuvier, 1812) is based on the hypothesis that segmentation arose only once and unites the annelids and arthropods. It should be noted that the idea that animals evolved as a series of grades, with acoelomate, pseudocoelomate and eucoelomate animals each forming a monophyletic clade is an issue separate from Articulata, and has never been seriously considered by morphologists. Unfortunately it is still commonly taught in introductory biology and invertebrate zoology courses, partly because Libbie Hyman organized her treatise on the invertebrates along those lines (Hyman, 1951). The Ecdysozoa hypothesis, originally discovered from the analysis of gene sequences (Aguinaldo et al., 1997) is that molting evolved a single time and so all molting animals are united by the character of growth by ecdysis. Detailed discussions of the morphological characters related to segmentation and molting can be found in Schmidt-Rhaesa et al. (1998) and Garey (2001). Molecular studies have also shown that the lophophorates, long thought to be related to the deuterostomes, are clearly protostomes, and fall within a clade of the non-molting protostomes named Lophotrochozoa (Halanych et al., 1995; Mackey et al., 1996). The main difference between the morphological tree and the molecular tree is the placement of the lophophorates relative to the deuterostomes and protostomes and the relative position of the annelids and arthropods. The details of the topology within each of the two phylogenies in Figures 1 and 2 are continuously debated, and the two trees shown should be considered as examples of each. Despite the differences between the morphology- and molecular-based trees, some remarkable congruencies highlight the power of using both approaches.