CHAPTER 9 Introduction to the Bilateria and the Phylum Xenacoelomorpha Triploblasty and Bilateral Symmetry Provide New Avenues for Animal Radiation long the evolutionary path from prokaryotes to modern animals, three key innovations led to greatly expanded biological diversification: (1) the evolution of the eukaryote condition, (2) the emergence of the A Metazoa, and (3) the evolution of a third germ layer (triploblasty) and, perhaps simultaneously, bilateral symmetry. We have already discussed the origins of the Eukaryota and the Metazoa, in Chapters 1 and 6, and elsewhere. The invention of a third (middle) germ layer, the true mesoderm, and evolution of a bilateral body plan, opened up vast new avenues for evolutionary expan- sion among animals. We discussed the embryological nature of true mesoderm in Chapter 5, where we learned that the evolution of this inner body layer fa- cilitated greater specialization in tissue formation, including highly specialized organ systems and condensed nervous systems (e.g., central nervous systems). In addition to derivatives of ectoderm (skin and nervous system) and endoderm (gut and its de- Classification of The Animal rivatives), triploblastic animals have mesoder- Kingdom (Metazoa) mal derivatives—which include musculature, the circulatory system, the excretory system, Non-Bilateria* Lophophorata and the somatic portions of the gonads. Bilater- (a.k.a. the diploblasts) PHYLUM PHORONIDA al symmetry gives these animals two axes of po- PHYLUM PORIFERA PHYLUM BRYOZOA larity (anteroposterior and dorsoventral) along PHYLUM PLACOZOA PHYLUM BRACHIOPODA a single body plane that divides the body into PHYLUM CNIDARIA ECDYSOZOA two symmetrically opposed parts—the left and PHYLUM CTENOPHORA Nematoida PHYLUM NEMATODA right sides. The evolution of bilaterality also Bilateria PHYLUM NEMATOMORPHA resulted in cephalization, the concentration of (a.k.a. the triploblasts) Scalidophora sensory and feeding structures at a head end. PHYLUM XENACOELOMORPHA PHYLUM KINORHYNCHA Bilaterians further evolved a complete gut (or Protostomia PHYLUM PRIAPULA through gut), with a mouth and an anus and PHYLUM CHAETOGNATHA PHYLUM LORICIFERA excretory organs in the form of protonephridia SPIRALIA Panarthropoda PHYLUM PLATYHELMINTHES PHYLUM TARDIGRADA and metanephridia (except in the phylum Xe- PHYLUM GASTROTRICHA PHYLUM ONYCHOPHORA nacoelomorpha, likely the most primitive living PHYLUM RHOMBOZOA PHYLUM ARTHROPODA bilaterians). PHYLUM ORTHONECTIDA SUBPHYLUM CRUSTACEA* As noted in Chapter 1, the oldest fossils PHYLUM NEMERTEA SUBPHYLUM HEXAPODA PHYLUM MOLLUSCA SUBPHYLUM MYRIAPODA thought to be bilaterians are from the Ediacaran PHYLUM ANNELIDA SUBPHYLUM CHELICERATA period—embryos found in the Doushantuo de- PHYLUM ENTOPROCTA Deuterostomia posits of China, dating 600–580 million years PHYLUM CYCLIOPHORA PHYLUM ECHINODERMATA ago. The most recent molecular dating studies Gnathifera PHYLUM HEMICHORDATA also suggest that the origin of the Bilateria was PHYLUM GNATHOSTOMULIDA PHYLUM CHORDATA PHYLUM MICROGNATHOZOA probably in the Ediacaran, about 630–600 million PHYLUM ROTIFERA *Paraphyletic group years ago, although some dated trees have esti- mated the origin even earlier. © 2016 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 346 Chapter Nine together might allow us to reconstruct the nature of the BOX 9A Characteristics first bilaterian animal—the so-called Urbilaterian. of the Phylum Xenacoelomorpha The Basal Bilaterian 1. Soft-bodied, dorsoventrally flattened, acoelomate; almost exclusively marine worms The notion that acoel flatworms are the most primi- 2. Epidermis with unique pulsatile bodies, found in tive living bilaterians has been around for many years. no other Metazoan phylum; cilia of epidermis with In the past, some workers have even speculated that distinctive arrangement of microfilaments, with the acoels might be the most primitive living metazoans, standard 9+2 arrangement extending for most of having evolved from a ciliate protist ancestry (the “syn- the shaft, but microfilament doublets 4–6 fail to reach the end of the cilium (the “xenacoelomorphan cytial, or ciliate–acoel hypothesis”). But most biologists cilia”) have favored some version of the “planuloid–acoeloid 3. Midventral mouth and incomplete gut (i.e., lacking hypothesis,” which postulated acoels to be the link be- an anus) tween diploblasts (via a planula larva) and triploblasts. 4. Largely lacking discrete organs (e.g., no discrete A third hypothesis, which gained traction for a short circulatory system, protonephridia or nephridia, or while, was that the simplicity of acoels was the result of organized gonads) loss of derived features from a more complex ancestor 5. Cerebral ganglion with a neuropil; with anterior (the “archicoelomate hypothesis”). statocysts and a diffuse intraepithelial nervous Recent molecular phylogenetic research strong- system ly suggests that acoelomorph worms (Acoela and 6. With circular and longitudinal muscles Nemertodermatida), perhaps along with worms of 7. Hox and ParaHox genes present (but fewer in num- the genus Xenoturbella, are likely to be the oldest living ber than in other metazoans) bilaterian lineages, or perhaps basal deuterostomes— 8. With direct development (no larval forms) but either way, sharing a great many characteristics in common with an ancestral bilaterian, the so-called hypothetical “Urbilaterian.” Acoelomorphs are small, direct-developing (no larval stage), unsegmented, cili- Monophyly of the Bilateria is strongly support- ated worms. They have mesodermally-derived mus- ed by both molecular and morphological analyses. cles (but no coelom, circulatory, or excretory system), Anatomical synapomorphies of this clade include: multiple parallel longitudinal nerve cords and a cen- presence of a third germ layer (mesoderm), bilateral tralized nervous system, and a single opening to the symmetry, cephalization, and a body with both circu- digestive cavity. Importantly, research suggests that lar and longitudinal musculature—although there are their mouth—the single gut opening—does not derive prominent reversals or losses in all of these characters. from the blastopore (i.e., they are deuterostomous in The field of molecular phylogenetics has recently their development). Thus, the origin of the Bilateria provided us with better resolution of evolutionary may have been accompanied by an embryological shift relationships among animals. Molecular biology has in the origin of the mouth from the blastopore (as seen also led to the expansion of a field called evolutionary in Cnidaria and Ctenophora) to elsewhere. developmental biology (“EvoDevo”), which attempts Many bilaterian phyla have a larval type that has to understand the evolution of the molecular under- been described as primary larvae. These are ciliated pinnings of differences in the organization of animal larvae with a characteristic apical organ—a true lar- body plans. In large part, understanding the evolution val organ that disappears, in part or entirely, before of animal body plans is about unraveling the transi- or at metamorphosis. The apical organ is a putative tion from basal Metazoa (Porifera, Placozoa, Cnidaria, sensory structure that develops from the most apical Ctenophora) to the Bilateria, and their subsequent ra- blastomeres during embryogenesis. It does not fit the diation. However, genomic-level research has also narrow definition of a ganglion, because it seems to shown that there is no simple relationship between comprise only sensory cells. However, many spiralians genomic/molecular complexity and organismal/de- develop lateral (cerebral) ganglia in close apposition velopmental complexity, so contrary to earlier assump- to the apical organ, and this compound structure was tions the mere presence of members of conserved gene called the “apical organ” in some of the older literature. families (e.g., “segmentation genes”) in an organism’s It appears the apical organ is commonly used in larval genome reveals little about the evolutionary relation- settlement, and it is lost once a larva settles (the settle- ships of that organism to other animals. Thus, recon- ment process typically uses cells around the apical structing the phylogenetic tree of the animal kingdom pole). In spiralian protostomes, the apical organ differ- using conserved genes and morphological characters is entiates from the most apical cells (the 1a1-1d1 cells in a critical step. Ultimately, phylogenetics and EvoDevo spiral-cleavage terminology). It is highly variable, and © 2016 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. INTRODUCTION TO THE BILATERIA AND THE PHYLUM XENACOELOMORPHA 347 aspects of it are sometimes retained in the adult cen- caudatus, typical metazoan foregut and hindgut gene tral nervous system. In the pilidium larva of nemerte- expressions accompany this development, and the ans the apical organ is shed at metamorphosis together hindgut/posterior markers brachyury (bra) and cau- with the whole larval body, which in some cases is in- dal (cdx) are expressed as the anus emerges from the gested by the emerging juvenile worm. blastopore. Continuing developmental work on crus- Deuterostomes are more difficult to interpret, taceans is revealing that most species probably also and only in echinoderm and enteropneust