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Home , Choanoflagellate, Deuterostome, Lophophorata, Nematoida, Nemertodermatida, Nephrozoa

y the time you have gotten to this chapter, you will have "toured" almost all of the , given that com- prise roughly 1,324,402 (96%) of the approximately 7,382,402 described, living animal . What an incredible diversity of form and function you have seen! Isn't it curious how unevenly these are distributed across the 32 metazoan phyla? Vastly unevenly distributed-81.5% of all described animals are , 5.8% are mol- luscs, and only 4.4'h are . The other 29 phyla make up the re- maining 7%! Eight phyla have fewer than 100 described species in them, and half of those have fewer than a dozen known species-what are we to make of that? In fact, only 6 phyla comprise more than one percent each of the described animal species on Earth (Arthropoda, , Annelida, Platyhelminthes, Nematoda, and Chordata). It would seem that the world belongs to insects,, spiders, molluscs, , and . Indeed, these are the only animals most humans ever see in their lifetimes (unless they happen to go diving on a tropical coral reef, in which case they are confronted by myriad , cnidarians, and ). How fortunate that you have now been introduced to all 32 animal phyla! In reading the "animal chapters" of this text, you have learned a good deal about the evolution of these phyla, how they are related to one anoth- er, and what their internal relationships are. You have learned that phylo- genies can be constructed from a variety of different kinds of data, and that most recently the field of molecular has proliferated, giving us new ideas about how Earth's creatures are related to one another. The idea of phylogenetic trees should now be quite familiar to you. But let's take one last look, a "higher view" of animal phylogeny, before we close the cover on this edition of Inaertebrates. Molecular phylogenetics had only just begun to bear fruit in 2002, when the second edition of this book went to press. While some tantalizing sug- gestions of new and very different kinds of relationships among the animal phyla had been suggested, these new hypotheses had not yet been broadly tested. Since then, molecular phylogenetics has exploded onto the scene at a pace never imagined, and it now plays the primary role in reconstructing an- imal phylogeny. In just the past 15 we have come from analyzing a few

This chapter has been revised by Richard C. Brusca and 1048 ChapterTwenty"-Eight ribosomal genes to the point where new genome-level presence of high concentrations of the compound analyses are being published almost daily. Molecular 24-isopropyl cholestane are now disputed. Some of phylogenetics is now being incorporated into studies of the oldest metazoan fossils are from the Doushantuo ecology, oceanography, biogeography, conservation bi- Formation of southern China, dating to 600 million ology, medicine, archeology, and anthropology. And it years ago. Sponges, cnidarians, and other apparent is building a new frar-nework for the tree of life. diploblastic animals have been reported from these de- Unraveling the phylogehetic history of the Animal posits, as well as ranging from two to thou- Kingdom has been one of biology's great challenges. sands of cells. However, many of these Doushantuo The "new phylogeny," built with molecular data, has metazoan fossils also have been disputed in one fash- many similarities to older trees built on morphological ion or another. It seems that interpreting ancient fossils and developmental data, but some big surprises have in rocks can be as challenging as inferring ancient phy- emerged and many uncertainties remain. The biggest logenies with morphology or molecules! challenge lies in the fact that life's deep lineages arose We discussed the origin of the Metazoa in several and began to diverge from one another so long ago, previous chapters. To reiterate, a large body of evi- over half a billion years ago for most phyla. So the traits dence, anatomical and molecular, has accumulated of animals, whether anatomical or genetic, that might since the 1960s that supports the view of multicellular be useful in revealing relationships among these an- animals sharing a common ancestor with the cient lineages are obscured by hundreds of millions of group Choanoflagellata. The flagellated collar cells years of evolutionary change. But, despite this, many of sponges and have been viewed relationships are now well resolved. as nearly identical and unique to these two groups. A Early molecular phylogenetic studies relied heav- few interesting differences between them have been ily on the 18S ribosomal RNA gene (also known as the noted (e.g., Mah et aL.2014),but some divergence over nuclear small-subunit ribosomal RNA gene, or SSU a half billion years is to be expected. The Metazoa are rRNA). However, it quickly became apparent that un- defined by a number of synapomorphies, the most ob- derstanding deep-level metazoan phylogeny required vious being multicellularity arising through the embry- analysis of additional genes, particularly nuclear pro- onic layering process called . Also, unlike tein-coding genes, and this led to an era of multigene coloniality, as seen in many protist groups (including trees that continues today as phylogeneticists add more choanoflagellates), in animals the epithelial cells are in and more genes (and taxa) to their datasets for analy- contact with each other through unique junction struc- sis (Chapter 2). Most recently phylogenomic stud- fures and molecules, some of which make transport of ies, using large parts of the genome (often using the nutrients between cells possible (e.g., septate or tight transcriptomel as a proxy for the whole genome) and junctions, desmosomes, zonula adherens). Additional analyzinghundreds or even thousands of genes, have metazoan synapomorphies include: striate myofibrils, begun to expand the scope of data available for phylo- -myosin contractile elements, the possession of genetic analysis, and these have added increased sta- animal (type IV) collagen (although collagen, or a col- bility to the structure of our phylogenetic framework. lagen homologue also occurs in some fungi), and a The advent of EvoDevo, or evolutionary developmen- beneath the . In addition. sexual tal biology, has also begun to significantly impact our reproduction in animals involves a djstinct pattern of understanding of how genes relate to specific morphol- egg development from one of the four cells of , ogies, how they work, and what roles they might have whereas the other three cells degenerate. played in the unfolding of animal radiations. These Figure 28.1 presents a consensus tree of metazoan new techniques have provided answers to fundamen- phylogeny, based primarily upon the most recent tal questions, such as the identity of append- molecular phylogenetic research. Phylogenetic stud- ages and the nature of segmentation in animals. ies have largely been in agreement that the oldest liv- Estimates of divergence times of the animal phyla, ing animal is Porifera, the sponges. However, based on molecular clock calculations, suggest that some recent molecular phylogenies have suggested the origin of the Metazoa was 875 to 650 million years might be the basalmost metazoans. The ago. Some trace fossils put the emergence of the bilat- draft genome of Pleurobrschia bachei,together with erians at around a billion years ago, although the na- other ctenophore , suggest that cteno- ture of those specimens has been disputed. Some re- phores may be rather distinct from other animal ge- cent datings that had assumed the presence of sponges nomes in their content of neurogenic, immune, and in (and even Cryogenian) rocks due to the developmental genes. However, a number of puta- tive synapomorphies link and Ctenophora with the , a that has been called Neuralia 'Whereas a genome is the complete set of genes present in a celi (Figure 28.1). The "basal Ctenophora" hypothesis (or organism) and is sequenced from DNA, a is a subset of those genes that are transcribed (or expressed) in a cell was challenged by J6kely et al. (2015) and Pisani et at any given time and is sequenced from RNA. al. (2015),both research groups suggesting it was an Metazoa

Bilateria

Deuterostomia Protostomia

Chordata

Lophophorata Hemichordata .G r---,r.---Scalid?phor?-\

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Metazoa: (1) Gastrulation and embryonic tissue layering; (2) septate junctions, tight junctions, and/or zonula adher- ens present in epithelial tissues; (3) type lV collagen; (4) collagenous basal lamina/basement membrane beneath epidermis; (5) striated myofibrils and actin-myosin contractile elements. Metazoa beyond Porifera: (6) striated ciliary rootlets. Cnidaria (and Ctenophora) + Bilateria: (7) Sap junctions; (8) fixed, organized gonads; (9) synaptic ; ('10) -lined gut (with digestive enzymes); (11) with primary , bearing apical (lost in Ecdysozoa); (12) presence of opsins. ('1 primary bilateral; (14) cephaliza- Figure 28.1 A phylogeny of Metazoa. This tree reflects a Bilateria: 3) symmetry tion, with concentration of neural cell bodies in head as consensus view based primarily on recent molecular phylo- ganglion (or rudiments thereof); ('15) with third genetic analyses. Uncerlainty still exists in several regions. a cerebral germ the , formed primarily by embryonic Strong resolution of the relative placement of , layer, Deuterostomia and Protostomia together Cnidaria, and especially Ctenophora is yet to be achieved. endoderm. The , united by their pos- The Bilateria comprise two lineages, Deuterostomia and comprise a clade called (i.e., to Protostomia, although the position of session of discrete excretory structures bilaterians is still being debated (a general consensus is that they are the exclusion of Xenacoelomorpha). basal bilaterians, not falling unambiguously within either Deuterostomia: (16) pharyngeal gill slits; ('17) trimeric Deuterostomia or Protostomia). Similarly, Protostomia has body . a difficult-to-place lineage ()and two large Chordata: (18) notochord; (19) dorsal hollow nerve cord; -Spiralia and Ecdysozoa. Limited developmental (20) endostyle (or its derivative); (21) tadpole lawa', (22) work suggests Chaetognatha might have a form of spiral oostanal tail. , but molecular phylogenies rarely place this Protostomia: (23) dorsal cerebral ganglia form circum- among the Spiralia. Other than the clades Gnathifera and esophageal connectives to ventral nerve cords. , the Spiralia have proven difficult to sort Ecdysozoa: (24) multilayered cuticle is shed/molted one out, and these phyla are represented as a starburst on the or more times during life history, regulated by ecdysteroid tree. The Ecdysozoa (the "molting Protostomia") are partly hormones; (25) loss of primary larva. resolved, although the relationships between the three Needless to say, in many cases these synapomorphies major clades (, Nematoida, Panadhropoda) have been secondarily altered or lost in some phyla. remain unclear. Putative morphological synapomorphies Synapomorphies of other clades and phyla depicted on defining the major animal clades are indicated by numbers this tree have already been described in previous chapters. on the tree, and are as follows. 1050 ChapterTwenty-Eight

artifact of methodological issues. Lr fact, the placement Deuterostomia, however, are largely settled, with the of Ctenophora is only one area of uncertainty in the an- Ambulacraria (Hemichordata + Echinodermata) being imal tree. Strong resolution of the positions of Placozoa the to the Chordata (Cephalochordata, and Cnidaria have also yet to be achieved (and placo- Urochordata, and Vertebrata / Crariata). zoans seem to be much more derived than their simple One of the major things we have learned from this body plan would first suggest). new view of phylogenetic relationships is that devel- That the Bilatefia comprise two main lineages, opmental systems are flexible. For example, a trait long Deuterostomia and Protostomia, seems largely settled, thought to define the Deuterostomia is deuterostomous although the position of the phylum Xenacoelomorpha development itself. However, we now know that this is still debated (a general consensus is that they are mode of embryogeny also occurs in some phyla belong- basal bilaterians, but do not fall unambiguously within ing to the clade Protostomia (e.g.,in , either Deuterostomia or Protostomia). Some molecu- Priapula, Brachiopoda, many Crustacea, perhaps lar research had suggested that Xenoturbellida (and Chaetognatha). Thus, as noted earlier in this book, the even Xenoturbellida + ) were deutero- clade Deuterostomia cannot be defined by deuterosto- stomes, but that hypothesis is not well supported. my/ nor can the clade Protostomia be defined by proto- The weight of molecular and morphological evidence stomy (which also occurs in Cnidaria and Ctenophora). places Xenacoelomorpha as a clade and sister group Similarly, radial cleavage is plesiomorphic among to all other bilaterians, as shown in our tree. Because Bilateria, while spiral cleavage, which is apomor- xenacoelomorphs lack excretory organs, and these (in phic for Spiralia, appears to have reverted back to ra- their many forms) are present in most other bilaterians, dial multiple times. The clade Spiralia in our tree has the sister group to Xenacoelomorpha (Deuterostomia + members whose cleavage patterns are radial (e.g., the Protostomia) has been called Nephrozoa. three lophophorate phyla), whereas the Gastrotricha The Protostomia can be divided into three main lin- seems to have a unique form of cleavage. Several phyla eages/ one containing the sole phylum Chaetognatha, of Spiralia have trochophore or trochophore-like lar- and two large clades-Spiralia and Ecdysozoa. Butnei- vae (e.g., Mollusca, Annelida, , and possibly ther molecular nor morphological data have convinc- ) but these have not consistently grouped to- ingly resolved relationships among these three clades. gether in the molecular phylogenies. Most chaetognath morphological traits have no clear This brings us back to the question of why ani- homologies in other lineages, and molecularly they mal species diversity is so strongly dominated by form a long branch that separates them from the early arthropods, molluscs, , and vertebrates. diversification of . Limited developmen- Unfortunately, there is no easy explanation for why tal work suggests Chaetognatha might have a form of these four groups have enjoyed such expansive radia- spiral cleavage, but molecular phylogenies rarely place tions. Could it be that this is an artifact of time-perhaps this genus among the Spiralia. However, their cerebral during earlier eras, the Mesozoic or Paleozoic, other ganglia resemble those of the spiralian phyla. phyla dominated Earth's biosphere, but simply left us Relationships within Spiralia need further refine- little fossil evidence of their prior dominance due to ment, but recent phylogenomic data have suggested their poorly fossilizable bodies? If this were true, many three clades-Gnathifera, Rouphozoa (Gastrotricha of those small phyla would be viewed today as "living + Platyhelminthes), and Lophophorata. The earlier relicts" (like horseshoe crabs). Did ctenophores, placo- named clade, , which includes both zoans/ acoel worms, gastrotrichs, nemerteans, chaeto- the lophophorates and some of the larger groups of gnaths, entoprocts, , and other phyla spiralians (annelids, mollusc, and nemerteans) has that today seem almost inconsequential once dominate also often been recovered. Many other suggestions for the world? Or perhaps the "big fout" taxahave always relationships among the spiralian lineages have been been dominant due to something intrinsic in their biol- published, but little consensus has so far been reached. ogy that remains to be discovered. Another possibility Within Spiralia, the concept of Annelida including is that we simply haven't looked hard enough, spent the former phyla and Echiura, as well as enough effort combing through interstitial habitats, Pogonophora and the mysterious meiofaunal worms deep-sea sediments, and the parasitic world-there Lobatocerebrum and Diur odrilus, is strongly supported. might well be an enormous biological diversity still The Ecdysozoa (the "molting Protostomia") are waiting to be discovered in such poorly sampled envi- partly resolved, although the sister group relation- ronments (certainly we know this is true for the round- ships among the three major clades (Scalidophora, worms/ Nematoda). Stay tuned for the Fourth Edition Nematoida, Panarthropoda) remain poorly studied of lnaertebrafes,to see what we have learned about the due to lack of appropriate data sets including genomic tree of life in a few years. data for and . In fact, no phy- We finish this chapter with a note of caution and logenomic analysis has yet included representatives one of hope. Molecular phylogenies are resolving the of all the ecdysozoan phyla. The relationships of the puzzle of the animal tree of life one piece at a time, PERSPECTIVESON INVERTEBRATEPHYLOGENY 1051 but morphology still has its role in phylogenetics. other. Molecular phylogenetics has given us a new Gnathifera, for example,was first recognizedby ana- way to look at the animal tree, and robust and stable lyzing morphologicaltraits, and has subsequentlybeen results have made us rethink certain long-held para- consistentlyrecovered by both morphological and mo- digrns (e.g.,Articulata versus Ecdysozoa; Atelocerata lecular analyses.The monophyly of other groups, such versus Tetraconata). Morphology canbe misleading in as Scalidophora,iq supportedmore strongly by mor- some cases/as molecular analyses can also be affected phological data thhn by rlrolecular data but this clade by many kinds of biases or be unable to reconstruct the is broadly acceptedby invertebratebiologists. Many interrelationships of some animal groups. Thus, only groups have been shuffled around the tree, mostly by combining the information derived from the careful becausethey were once positioned based on single study of both disciplines will we be able to generate a charactersystems (e.9., radial versusspiral cleavage; sound animal phylogeny, and be in a position to com- acoelomateversus blastocoelomate versus coelomate), prehend what that phylogeny means in terms of the and many of thesecharacter systems conflict with one evolution of animal body plans.

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