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10.1146/annurev.ecolsys.35.112202.130124

Annu. Rev. Ecol. Evol. Syst. 2004. 35:229–56
doi: 10.1146/annurev.ecolsys.35.112202.130124
c 2004 by Annual Reviews. All rights reserved
Copyright First published online as a Review in Advance on September 2, 2004

THE NEW VIEW OF ANIMAL PHYLOGENY
Kenneth M. Halanych
Annu. Rev. Ecol. Evol. Syst. 2004.35:229-256. Downloaded from arjournals.annualreviews.org
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Department of Biological Sciences, Auburn University, Auburn,
Alabama 36849; email: ken@auburn.edu

Key Words Metazoa, Lophotrochozoa, Ecdysozoa, Deuterostomia, Cambrian
explosion■ Abstract Molecular tools have profoundly rearranged our understanding of metazoan phylogeny. Initially based on the nuclear small ribosomal subunit (SSU or 18S)
gene, recent hypotheses have been corroborated by several sources of data (including
the nuclear large ribosomal subunit, Hox genes, mitochondrial gene order, concatenated mitochondrial genes, and the myosin II heavy chain gene). Herein, the evidence
supporting our current understanding is discussed on a clade by clade basis. Bilaterian animals consist of three clades: Deuterostomia, Lophotrochozoa, and Ecdysozoa. Each clade is supported by molecular and morphological data. Deuterostomia issmaller than traditionally recognized, consisting of hemichordates, echinoderms, chordates, and Xenoturbella (an enigmatic worm-like animal). Lophotrochozoa groups animals with a lophophore feeding apparatus (Brachiopoda, Bryozoa, and Phoronida) andtrochophore larvae (e.g., annelids and mollusk), as well as several other recognized
phyla (e.g., platyhelminthes, sipunculans, nemerteans). Ecdysozoa comprises molting
animals (e.g., arthropods, nematodes, tardigrades, priapulids), grouping together two
major model organisms (Drosophila and Caenorhabditis) in the same lineage. Platyhelminthes do not appear to be monophyletic, with Acoelomorpha holding a basal position in Bilateria. Before the emergence of bilateral animals, sponges, ctenophorans,
cnidarians, and placozoans split from the main animal lineage, but order of divergenceis less than certain. Many questions persist concerning relationships within Ecdysozoa
and Lophotrochozoa, poriferan monophyly, and the placement of many less-studied
taxa (e.g., kinorhynchs, gastrotrichs, gnathostomulids, and entoprocts).

INTRODUCTION
In the past decade, major new hypotheses of animal evolution have shaken traditional foundations and caused researchers to abandon long-standing hypotheses.
This change certainly provoked controversy, and many are critical of these new
hypotheses. Skepticism has focused on uncertainty about reliability of molecular data, apparent conflict between morphology and molecular data, lack of robust phylogenetic signal, lack of well-defined morphological synapomorphies,
and apparent contradictory conclusions from the same data source. In most cases,
the basis for such skepticism is limited. One must keep in mind that systematic
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biology is a dynamic field of research, with hypotheses constantly proposed andlater falsified. In contrast, many who are interested in animal phylogeny want awell-supported (i.e., static) evolutionary framework that they can use for comparative studies or teaching purposes.
Fortunately, consensus is emerging for many regions of the metazoan tree.
This review provides a conceptual framework of the current understanding ofanimal phylogeny in light of recent advances. In particular, this review supplements
invertebrate biology texts (e.g., Brusca & Brusca 2003, Ruppert et al. 2004) that
do not adequately convey the recent advances. Owing to space limitations, I do notdiscuss many of the important traditional hypotheses that are already well reviewed
in Willmer (1990) or viewpoints based solely on morphology (Nielsen 2001). I
draw mainly on recent analyses to (a) build a basic comparative framework ofmetazoan phylogeny, (b) discuss support, or lack thereof, of major hypotheses,and (c) catalog significant papers for those less familiar with the field.
Before I discuss animal relationships, a few salient points deserve mention.
1. Traditional understanding of animal phylogeny (Figure 1) was largely basedon (a) the concept that evolution proceeds from simple to complex, (b) asuite of purportedly conserved embryological features (e.g., cleavage patterns, blastopore fate, mode of coelom formation), and (c) overall bodyarchitecture (e.g., segmentation, type of coelom). These ideas were outlined in Libbie Hyman’s (1940, p. 38) figure 5, which presented her understanding of animal body plans. When compared with genetic information(or even cladistic morphological analyses), many traditional morphologicaland embryological characters are more evolutionarily labile than previously
thought (e.g., Halanych 1996a, Valentine 1997, Halanych & Passamaneck2001).
2. “Phyla” are man-made constructs erected because, in part, shared features
were lacking between organismal groups. The phylum concept has a long
history of being equated to body plans (or Baupläne), which can be misleading as to the age and diversity of a group. For example, despite very
different body plans, major lineages of the phylum Arthropoda are put together because of the presence of an exoskeleton. In contrast, the formerly
recognized phylum Vestimentifera (tube worms) are highly derived annelids
with limited diversity and recent origins (McHugh 1997; Halanych et al.
1998, 2001).
3. Molecular data are more objective and subject to considerably more rigor
than morphological data. DNA sequence contains four easily identified andmutually exclusive character states (analyses on protein coding genes usually employ translated nucleotide data). Morphological and embryologicalcharacter definitions and scoring of character states are far more subjective,
and most characters have been repeatedly used without critical evaluation,
calling into question the utility of morphological cladistic studies that span
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morphological cladistic analyses will reveal several characters scored differently by various workers. Furthermore, evolution at nucleotide and aminoacid levels of housekeeping and conserved developmental genes (i.e., thoseused for phylogenetics) is understood to a much better degree than evolutionary forces acting on morphology. As such, more sophisticated and accurate methods of phylogeny reconstruction are available to molecular data,
whereas morphological data are generally limited to parsimony methods.

NEW METAZOAN1 TREEIn 1988, Field and coworkers published on animal phylogeny using the 18S or
nuclear small ribosomal subunit (SSU) gene. Although this paper did have someinternal inconsistencies, it ushered in the era of molecular systematics for higherlevel animal phylogeny. The SSU was chosen at the time because enough RNA
could be obtained for sequencing, it was ubiquitous in animals, and regions of
the gene were conserved enough to make “universal primers.” Field et al. (1988)
were also one of the first to use explicit criteria and algorithms for building aphylogenetic tree of Metazoa (but see Bergstrom 1985). Thus, it provided a means
to critically test and evaluate traditional hypotheses of animal relationships.
Figure 2 illustrates our current understanding of animal relationships. The
topology presented is a conservative interpretation of available data. Because data
come from many different sources, we cannot reconstruct the tree from a single, allencompassing analysis. Throughout the text, I discuss support for the relationships
presented in Figure 2. Similarly, Table 1 summarizes some major changes in our
understanding of metazoan phylogeny.

BASAL METAZOAN CLADESMetazoa constitutes a monophyletic clade closely related to Choanoflagellata. This
traditional view and supporting evidence (e.g., morphological synapomorphies,
including extracellular matrix, septate junctions, and spermatozoa; and gene trees,
including rDNA, heat-shock proteins, and elongation factors) have been recently
covered by Cavalier-Smith et al. (1996), Eernisse & Peterson (2004), and Brooke& Holland (2003) and is not elaborated here.

Sponge Paraphyly
The question of poriferan monophyly has recently generated much discussion.
Molecular analyses of SSU data suggest that sponges form a basal paraphyletic
1

Note that others recognize a formal distinction between Metazoa and Animalia, using
Animalia to represent a more inclusive clade of Choanoflagellata plus Metazoa (e.g.,
Sørensen et al. 2000, Eernisse & Peterson 2004).

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P1: GJBHALANYCHTABLE 1 List of important hypothesesa supported by our current
understanding

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Hypothesis

Supportb

Sponge paraphyly

SSU, LSU, morph.

Cnidaria sister to Bilateria

SSU, SSU 2◦ structure, Hox, morph.

Platyhelminthes polyphyletic(Acoelomorphs basal)

SSU, LSU, myo II

Deuterostomia

SSU, LSU, Hox, morph.

Ambulacraria (Hemichordata
and Echindermata)

SSU, LSU, tRNA coding, multigene
protein coding, morph.

Xenoturbella is a deuterostome

SSU, COI, COII, mtDNA gene order,
codon usage

Lophotrochozoa

SSU, LSU, Hox, mtDNA gene trees,
mtDNA gene order, myo II, IF gene

Annelida includes siboglinids
and echiurids

EF-1α, SSU, LSU, CO1, morph.

Lophophorate polyphyly

SSU, LSU, Hox, morph.

Syndermata (Acanthocephalawithin Rotifera)

SSU, morph.

Gnathifera (Syndermata,Gnathostomulida,
Micrognathozoa)

SSU, morph.

Platyzoa (Platyhelminthes,
Gastrotricha, Cycliphora,
Entoprocta, Gnathifera)

SSU, LSU, morph.

Ecdysozoa

SSU, LSU, Hox, morph., HRP activity

Scalidophora (Kinorhyncha,
Loricifera, Priapula)

SSU, LSU, morph.

Pancrustacea (Hexapoda
within Crustacea)

EF-1α, SSU, LSU

aHypotheses that are either novel (e.g., based on molecular data) or are different from our
traditional understanding.

b

These are the primary sources of support. See text for full details for any given node.

grade in Metazoa with Hexactinellida (glass sponges), then Demospongia (spongin
fibers), and then Calcarea (calcareous sponges) branching off in order from themain metazoan lineage (Borchiellini et al. 2001). Recent combined studies provide
support for the claim that Calcarea shares a more recent common ancestor withother animals, but placement of the Demospongia relative to the Hexactinellida
is not clear (SSU and LSU, Medina et al. 2001; morphology and SSU, Zrzavy
et al. 1998, Peterson & Eernisse 2001). The presence of long cross-striated ciliary31 Oct 2004 12:33

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rootlets in calcareous sponge larvae and eumetazoans to the exclusion of othersponges is consistent with the recent SSU hypothesis (Amano & Hori 1992, Nielsen2001).
In phylogenetic analyses, taxonomic representation of sponges is often limited
because of problems with obtaining quality DNA or RNA free of contaminationfrom foreign genomes. In addition to more robust taxon sampling, future studies
examining the presence or absence of certain genes in different sponge lineages
will also yield valuable insight. As for morphological characters, sponges are often
problematic because many phylogenetic characters applied to other animals must
be coded as question marks, leading to undesirable effects in tree reconstruction
programs.
The paraphyletic nature of sponges has important consequences for understanding early animal evolution. Poriferans are typically considered monophyletic on thebasis of their body architecture, with a water canal system, presence of choanocytes,
and equatorial polar bodies during development (Nielsen 2001). However, molecular data suggest these features should be considered symplesiomorphies (sharedancestral characters) of Metazoa and not synapomorphies of Porifera. Interestingly,
Hox genes, involved in anterior/posterior body patterning, have not been easy tofind in sponges despite repeated attempts (Seimiya et al. 1994, Manuel & Le Parco2000), although Degnan et al. (1995) reports finding three divergent candidates.
Thus, transition from an organism with poorly defined or lacking axes to one withan anterior and posterior seems to have been accompanied by expansion of genetic
machinery (Finnerty 1998, Finnerty & Martindale 1998).

Cnidarians and Ctenophores
Coelenterata is a dated term that referred to a taxon comprising Cnidaria andCtenophora (and originally Porifera; Hyman 1940). A Cnidaria/Ctenophora clade
is not supported by SSU data (Collins 1998, Kim et al. 1999, Podar et al. 2001), LSU
data (Medina et al. 2001), morphology (Eernisse et al. 1992), or combined analyses(Zrzavy et al. 1998, Peterson & Eernisse 2001). However, the hypothesized position of Ctenophora varies depending on which data are analyzed. Morphologicalanalyses place ctenophores closer to bilaterians (Schram 1991, Eernisse et al. 1992,
Zrzavy et al. 1998, Peterson & Eernisse 2001) because of sperm morphology andmuscle cells, among other characters. In contrast, SSU data support sponges andctenophores as basal lineages of Metazoa (Collins 1998, Kim et al. 1999, Podar
et al. 2001, Medina et al. 2001), leaving cnidarians as sister to bilaterians. Available
evidence from Hox genes (reviewed in Martindale et al. 2002), as well as SSU
secondary structure (Aleshin & Petrov 2002), also supports the Cnidaria/Bilateria
relationship.
The traditional dogma concerning lack of bilaterial symmetry and mesoderm
in cnidarians and ctenophores is problematic. The issue of symmetry is reallyan issue of body axis evolution. How many are there? Evolution of developmental mechanisms research has largely focused on how body axes are set up and31 Oct 2004 12:33

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maintained during ontogeny. Thus, our understanding and definitions of symmetry
are being reshaped by a growing body of evidence that demonstrates that mechanisms used in axial pattern can be found in nonbilaterian animals (Martindale et al.
2002, Brooke & Holland 2003, Wikramanayake et al. 2003, Finnerty et al. 2004).
Similarly, we are beginning to appreciate that mesoderm, or mesodermal precursors, may be present in ctenopohores and cnidarians (e.g., Martindale & Henry
1999, Spring et al. 2002, Muller et al. 2003, and references therein). Information
on relationships within Cnidaria may be found in Bridge et al. (1995) and Collins(2000, 2002). Podar et al. (2001) and Harbison (1985) offer views on molecularand morphological ctenophore phylogeny, respectively.

Placozoa
Placozoans are simple organisms of great interest for understanding very early evolution in animals. As with sponges, the use of placozoans in morphological cladistic
analyses can be problematic because they cannot be scored for most characters.
Every conceivable placement of placozoans among nonbilaterian metazoans has
been proposed. Studies including SSU data variably place placozoans within orsister to the Cnidaria (Bridge et al. 1995, Siddall et al. 1995, Kim et al. 1999,
Cavalier-Smith & Chao 2003; but see Zrzavy et al. 1998, Peterson & Eernisse
2001). Reports of a placozoan/cnidarian clade seem less likely based on the circular morphology of the placozoan mtDNA molecule (most cnidarians have a linear
mtDNA genome) and secondary structure of the mitochondrial LSU (Ender &Schierwater 2003). Although the exact placement of placozoans is not clear, they
are near the base of Metazoa (just before or after the sponge lineages) and are
currently receiving considerable attention via genomic tools (e.g., Martinelli &Spring 2003, Jakob et al. 2004).

BILATERIA
Bilateria consists of three main clades that predate the Precambrian/Cambrianboundary, 540 million years ago (Mya) (Balavoine & Adoutte 1998). Unfortunately, the events that led to the last bilaterian ancestor and subsequent diversification into deuterostomes, lophotrochozoans, and ecdysozoans are not wellunderstood. As such, there is considerable interest in determining which extant
taxon is the most basal bilaterian lineage. Currently, there are two possible candidates, acoelomorphs and myxozoans (small parasitic group). Very recent data
for the chaetognaths, traditionally considered deuterostomes, suggest a fairly basal
position. However, arrow worms are discussed in the deuterostome section becauseof the relevancy of published data.
The placement of acoelomorphs is a controversial topic that highlights someof the potential problems with both morphological and SSU rDNA data. Early
SSU analyses suggested Platyhelminthes was polyphyletic, with Acoela being

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the most basal bilaterian lineage and separate from other flatworms (Ruiz-Trillo
et al. 1999). However, the acoel in question had long-branch lengths owing tohigh nucleotide substitution rates, a problem that randomizes signal in data andcauses long-branched taxa to be artificially placed basal in a tree reconstruction(Felsenstein 1988, Wheeler 1990). Thus, researchers were concerned that the SSU
acoel result was an artifact. This long-branch problem was best illustrated in Peterson & Eernisse (2001), who graphically demonstrated that acoel branches for
SSU data were so long that they effectively acted as random sequences and were
probably rooting the Bilateria incorrectly (see also Giribet et al. 2000). Acoel
morphology was not that helpful for higher-level phylogenetic considerations because of their simplified bodies, but within Platyhelminthes morphology supported
Acoelomorpha (Acoela and Nemertodermatida) as a distinct clade considerably
different from other flatworms (reviewed in Giribet et al. 2000, Ruiz-Trillo et al.
2002). Subsequent work on acoel placement with an independent marker, elongation factor (EF)–1α, supported platyhelminth monophyly (Berney et al. 2000), but
this work soon came under fire because of sequence alignment issues and limited
taxon sampling (Littlewood et al. 2001). Recent findings with myosin II heavy
chain (Ruiz-Trillo et al. 2002) and combined SSU and LSU data (Telford et al.
2003) have independently confirmed that the Acoelomorpha are a basal lineage of
Bilateria. The remaining platyhelminthes appear to be within Lophotrochozoa.
Myxozoans are small enigmatic parasites with a very simple body plan. Thus,
even if they are basal bilaterians, their highly derived morphology may limit
their utility for understanding the last bilaterian ancestor. Myxozoans were previously considered protozoans, but molecular data demonstrated their metazoan
nature (Smothers et al. 1994). Combined SSU and morphology placed them within
Cnidaria (Siddall et al. 1995), but other molecular studies placed them at or near
the bilaterian root (Schlegel et al. 1996, Kim et al. 1999, Ferrier & Holland 2001).
Another mysterious organism, Buddenbrockia, has a simple body plan and has
vexed scientist since its discovery in 1850. This nondescript worm-like organism
is a myxozoan (Monteiro et al. 2002).

DEUTEROSTOMIA
Before the mid-1990s, Deuterostomia was generally considered to consist of threecore phyla (Echinodermata, Hemichordata, and Chordata), plus Chaetognatha andlophophorate taxa (Brachiopoda, Phoronoida, and Bryozoa2). Lophophorates havetypically been regarded as having a mix of traditional protostome and deuterostome characters, but Zimmer (1973), among others, made convincing arguments
based on developmental and nervous features (e.g., body regionalization, cleavage
2

Technically, the term Bryozoa refers to a clade that includes Ectoprocta and Entoprocta(or Kamptozoa). The terms Ectoprocta and Bryozoa are equated here because one would
rather be a bryozologist than an ectoproctologist!

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program, intraepidermal nervous system) for deuterostome affinities. Thus, many
considered some or all of them as basal to Deuterostomia sensu stricto (Willmer
1990, Nielsen 2001). Building on earlier studies that had included molecular data
for a brachiopod (Field et al. 1988, Lake 1990), Halanych et al. (1995) included
SSU data from all three major lophophorate lineages and formally proposed thatbryozoans, brachiopods, and phoronids were derived protostomes allied to annelids and mollusks. They proposed the node-based clade Lophotrochozoa. The
placement of lophophorate taxa and support for Lophotrochozoa are discussed
below.
Chaetognatha has also been removed from Deuterostomia. Two independent
SSU papers reported that chaetognaths were not deuterostomes, but their exact
placement in animal phylogeny remained elusive (Telford & Holland 1993, Wada
& Satoh 1994). Further analyses with a broader range of taxa supported a nematodechaetognath relationship, but the issue of long-branch attraction in SSU data could
not be completely ruled out (Halanych 1996b, Peterson & Eernisse 2001). The
uncertainty of chaetognath’s position is echoed in combined studies that placethem within Ecdysozoa (Zrzavy et al. 1998, Peterson & Eernisse 2001, Eernisse &Peterson 2004) or as basal bilaterians (Giribet et al. 2000). Papillon et al. (2003) surveyed Hox genes and reported that chaetognaths are basal in metazoan phylogeny
because of the presence of a chimera medial/posterior Hox orthologs. Additional
posterior Hox genes have been found, supporting chaetognaths as basal protostomes (D.Q. Matus, K.M. Halanych & M.Q. Martindale, unpublished results),
consistent with mtDNA gene order (Helfenbein et al. 2004). Thus, many of thedeuterostome-like features of chaetognaths (enterocoelous development, tripartite body, radial cleavage, etc.) are likely bilaterian symplesiomophies rather thanderived features.

Ambulacraria
Hemichordates were once placed within Chordata, but they were removed becausesome but not all the chordate-like features were present. Perhaps surprisingly these“half-chordates” are much more closely allied to echinoderms than to chordates(e.g., for morphology and SSU data, see Turbeville et al. 1994, Giribet et al.
2000, Peterson & Eernisse 2001; for SSU, see Halanych 1995; for changes intRNA coding, see Telford et al. 2000; for multigene, see Cameron et al. 2000,
Furlong & Holland 2002). Metschnikoff (1881), focusing on similarities between
the larvae of echinoderms and enteropnuests (also known as acorn worms), referredto the echinoderm-hemichordate group as Ambulacraria, which Halanych (1995)
formalized as a node-based name. Morphology supporting this grouping includes
characters pertaining to the tripartite larval coeloms (absent in chordates).
Ambulacraria has profound implications for understanding chordate origins
by altering interpretation of the evolution of gill slits, the nervous system, andpossibly the notochord. Such chordate features may have been present in the lastcommon ancestor of the Deuterostomia. Now we must address the possibility thatechinoderms lack gill slits and a notochord-like structure because these features

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were lost during the evolution to a pentaradial body plan. Similarly, Bather’s (1913)
and later Jefferies’s (1986) assertions that primitive echinoderms possessed ciliatedgill slits may be true. However, objective cladistic analyses of morphology and/or
molecules do not support Jefferies’s notion that chordates are direct descendentsof echinoderms.
Noteworthy is the large amount of genomic data coming to bear on the issue of
deuterostome relationships. For example, an impressive survey of hemichordate
genes with orthologs involved in chordate nervous system development demonstrates an amazing amount of conservation in expression domains despite thenoncentralized nature of the hemichordate nervous system (Lowe et al. 2003). Additionally, shortly after this publication, completely sequenced genome for eachmajor deuterostome lineage should be available in GenBank.

Tunicata
The tadpole larva is used to unify Tunicata (also known as Urochordata) with
Cephalochordata and Craniata. Perhaps the most convincing characters are thenotochord and neural development. Except for Larvacea (Appendicularia), commonalities between the adult body form of tunicates, cephalochordates, and craniates are lacking to the point that their inclusion in the same phylum is questioned(Nielsen 2001). Interestingly, as pointed out by Swalla and colleagues (Swalla
et al. 2000, Cameron et al. 2000, Winchell et al. 2002), the phylogenetic signal
supporting a monophyletic Chordata (including tunicates) clade is weak. In fact,
Ambulacraria is repeatedly much more robustly supported than Chordata (e.g.,
Winchell et al. 2002, Bourlat et al. 2003). The placement of Tunicata is variable:
sister to Craniata/Cephalochordata clade (Cameron et al. 2000, SSU of Winchell
et al. 2002), sister to Craniata (Giribet et al. 2000), sister to Ambulacraria (Wada& Satoh 1994, Swalla et al. 2000), or the basal deuterostome lineage (LSU ofWinchell et al. 2002, Bourlat et al. 2003). Tunicates often display long branches
relative to other deuterostomes, making their placement difficult. Despite the consensus that Tunicata, Cephalochordata, and Craniata form a monophyletic clade,this issue deserves more attention. The vast differences between tunicates and otherchordates suggest that they possess an evolutionarily distinct body plan. Hence,
the term Tunicata is preferred over Urochordata.
Paleontological work of Shu and collaborators (1999, 2001a, 2001b, 2003)
is revising our understanding of the early evolution of chordates. They have discovered ascidian (e.g., Cheungkongella), cephalochordate-like yunnanozoan (e.g.,
Haikouella), and agnathan (e.g., Myllokunmingia) fossils that push the origins ofthese lineages at least into the Lower Cambrian (approximately 530–540 Mya)and provide evidence of their complexity early in their evolution.

Xenoturbella
Xenoturbella is a small, morphologically nondescript flatworm-like organism that
feeds on bivalve eggs and larvae, whose phylogenetic affinities have long been a

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mystery. Although the first available molecular data on Xenoturbella suggested
molluscan affinities (Norén & Jondelius 1997), it appears to be a deuterostomebasal to the Ambulacraria. Bourlat et al. (2003) assert that in addition to their SSU,
cytochrome oxidase c subunit I (CO I) and CO II data, mitochondrial gene order,and more tentatively, codon usage support this placement. Because of its basal
position, questions arise as to whether Xenoturbella’s simplified body plan is theresult of strong selective constraints on an ancestral body form or the product of
secondary simplification. Xenoturbella clearly illustrates that many exciting andinteresting findings about animal evolution await discovery.

PROTOSTOMIA
Within Bilateria, Lophotrochozoa and Ecdysozoa form a monophyletic clade, typically called Protostomia, supported by SSU and LSU data (Halanych et al. 1995,
Mallat & Winchell 2002), combined analyses (Giribet et al. 2000), and Hox genes(de Rosa et al. 1999). In cases where conflicting topologies (e.g., Ecdysozoa with
Deuterostomia) have been reported (Ruiz-Trillo et al. 2002), support is weak. Continued use of the term Protostomia is less than ideal but admittedly familiar. Froma Hyman-like mindset, the term implies that the ultimate fate of the blastoporeis phylogenetically conservative and has traditionally been applied to coelomate
animals (to the exclusion of pseudocoelomates and acoelomates). In our current
understanding, blastopore fate is irrelevant for many ecdysozoans because theblastopore is usually not retained. Also, both protostome clades contain several
former acoelomate or pseudocoelomate taxa. Lastly, lophotrochozoans, ecdysozoans, and deuterostomes were probably all present in Precambrian times and all
experienced some degree of a rapid radiation around 580–520 Mya. Thus, it seems
more natural to think about bilaterians as having three main clades, given the importance of the Cambrian explosion in metazoan history (Balavoine & Adoutte1998).

LOPHOTROCHOZOA
Lophotrochozoa is a clade originally identified by SSU data and defined as thelast common ancestor of annelids, mollusks, the three lophophorate phyla (Brachiopoda, Phoronida, and Bryozoa), and all the descendants of that ancestor(Halanych et al. 1995). The name of the clade refers to the inclusion of animals thathave either a trochophore or a lophophore feeding apparatus. The major implication of this hypothesis is that lophophorate taxa are not allied to the deuterostomes
but are highly derived protostomes near annelids, mollusks, and their allies, calling into question many of the classical characters used to split protostomes anddeuterostomes.
The Lophotrochozoa hypothesis was contentious at first because analyses of
nonmolecular data still grouped some or all lophophorate taxa with deuterostomes

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239(Schram 1991, Eernisse et al. 1992, Zrzavy et al. 1998, Sørensen et al. 2000, Nielsen2001). In solely molecular analyses, brachiopods, phoronids, and bryozoans havenever been strongly supported with deuterostomes. Moreover, the Lophotrochozoa
hypothesis has received strong support from multiple sources of molecular data,
including SSU data (Halanych et al. 1995, Mackey et al. 1996, Eernisse 1997), LSU
data (Mallat & Winchell 2002; Y.J. Passamaneck & K.M. Halanych, unpublishedresults), Hox gene data (de Rosa et al. 1999, Passamaneck & Halanych 2004),
mitochondrial sequence and gene arrangement data (Stechmann & Schlegle 1999,
Helfenbein et al. 2001, Helfenbein & Boore 2004), myosin II heavy chain sequence
data (Ruiz-Trillo et al. 2002), and intermediate filament sequences (Erber et al.
1998). In particular, five Hox genes (lox2, lox4, lox5, post1, and post2) havebeen characterized as having lophotrochozoan-specific peptide signatures (de Rosa
et al. 1999, Balavoine et al. 2002). Not surprisingly, taxonomic sampling of theabove studies varies greatly, and only a few studies include all major (putative)
lophotrochozoan taxa. For example, bryozoans seem to be a key taxon for defining
Lophotrochozoa but have only recently been examined for data other then the SSU(see below).
Relationships within Lophotrochozoa are not well understood, and short-branch
lengths between recognized phyla are a typical result. This lack of phylogenetic
signal could be due to a rapid radiation of the taxa (i.e., Cambrian explosion) or
indicative of the data in question. As genes other than the SSU and broader taxon
sampling have been employed, lophotrochozoan interphyletic relationships havebecome more apparent, but support via bootstrap analyses or hypothesis testing
methods (e.g., likelihood ratio tests) is often limited. For example, the terms Eutrochozoa and Trochozoa have been used to describe subsets of lophotrochozoan
taxa (see Peterson & Eernisse 2001), but their weak nodal support precludes detailed discussion here. Nonetheless, within Lophotrochozoa several subclades are
emerging (Figure 2).

Annelida
Annelida encompasses a greater diversity of animal body plans than traditionallyrecognized (McHugh 2000, Halanych et al. 2002). Both McHugh (1997) andKojima (1998) used EF-1α data to suggest that “Polychaeta” is not monophyletic.
Specifically, Vestimentifera, Pogonophora, and Echuira, which were all consideredseparate phyla, are within the annelid radiation. SSU (Halanych et al. 2001), CO
I (Black et al. 1997), and mitochondrial genome data (Boore & Brown 2000;
R.M. Jennings & K.M. Halanych, unpublished data) corroborated placement ofvestimentiferans and pogonophorans within annelids. This placement has long
been argued by some on the basis of morphology (van der Land & Nørrevang 1977,
Southward 1988) and has been supported in a morphological cladistic analysis(Rouse & Fauchald 1997). Furthermore, Vestimentifera is clearly a clade within
the recognized Pogonophora (or Frenulata) (Southward 1988; Halanych et al.
1998, 2001; Rouse 2001). McHugh (1997), and Rouse & Fauchald (1997) argue31 Oct 2004 12:33

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that the pogonophoran/vestimentiferan clade should revert to its original nomen
Siboglinidae (Caullery 1914). Additionally, Clitellata (Oligochaeta and Hirudinea)
are derived polychaetes (McHugh 2000, Rota et al. 2001, Struck et al. 2002).
McHugh’s (1997) EF-1α data also placed Echiura within annelids, which was
subsequently supported by morphological work on the larval nervous system(Hessling 2002) and by SSU data (Bleidorn et al. 2003). Another group thatdeserves brief mention is Myzostomida, commensals/parasites on echinoderms
that have often been placed with annelids (Westheide & Rieger 1996, Rouse &Fauchald 1997). Available combined EF-1α and SSU data suggest an affinity
to flatworms (Eeckhaut et al. 2000), but nervous system morphology (Müller &Westheide 2000) as well as larval morphology (Eeckhaut et al. 2003) are annelidlike. A recent combined analysis of SSU and morphology suggests this organism
is outside the annelid radiation (Zrzavy et al. 2001). This group will receive future
attention because its placement bears on issues of homology for nervous and larval
characters within Lophotrochozoa.

Platyzoa
Platyzoa consists of Platyhelminthes (hereafter referred to as excluding Acoelomorpha), Rotifera, Acanthocephala, Gastrotricha, and Gnathostomulida, as recognized by Garey & Schmidt-Rhaesa (1998) and Cavalier-Smith (1998) and further
supported by Giribet et al. (2000). Molecular evidence suggests Platyhelminthes
are within the lophotrochozoan clade (Balavoine & Telford 1995, Balavoine 1997,de Rosa et al. 1999, Ruiz-Trillo et al. 2002), and Garey and colleagues (Garey et al.
1996b, Garey & Schmidt-Rhaesa 1998) provided strong support for acanthocephalans within rotifers, the Syndermata. The placement of gnathostomulids together
with Syndermata has received support (Ahlrichs 1997, Giribet et al. 2000). Members of this group have an internal set of chitinous jaws and are therefore called theGnathifera. Although molecular data are still wanting, the curious Micrognathozoa
is likely to be in the Gnathifera (Kristensen & Funch 2000, Sørensen et al. 2000).
However, recent molecular data (Giribet et al. 2004) are ambiguous, with SSU andvery small fragments of LSU and Histone 3, placing Micrognathozoa near syndermatans and cycliophorans, whereas CO I placed it near entoprocts. Interestingly,
the first report of Gnathostomulid SSU data (Littlewood et al. 1998) placed themnext to a chaetognath-nematode clade, whereas in Giribet et al.’s (2000) analyses they clustered with platyhelminthes and gastrotrichs. Peterson & Eernisse(2001) noticed the potential long-branch issues of this group and subsequently removed the acoels, gnathostomulids, and gastrotrichs from their analyses. The LSU
data support the grouping of rotifers and acanthocephalans with platyhelminthes(gnathostomulids were not included; Y.J. Passamaneck & K.M. Halanych, unpublished observations). The morphological evidence does provide support for the
Platyzoa (see Giribet et al. 2000).
One key issue with Platyzoa is its placement relative to Lophotrochozoa. Although some analyses assert that it is the sister clade to Lophotrochozoa (Garey &Schmidt-Rhaesa 1998, Giribet et al. 2000), others support placing Platyzoa within
Lophotrochozoa (Peterson & Eernisse 2001; Eernisse & Peterson 2004; Y.J.

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Passamaneck & K.M. Halanych, unpublished observations). Given that Lophotrochozoa is a node-based name, the inclusiveness of the group is determined by the
position of its basal lineages, in this case Bryozoa. Thus, to determine if Platyzoa
is within Lophotrochozoa, we must know its position relative to Bryozoa. The
placement of Platyzoa remains an important issue because the position of platyhelminthes, with their simple body plans, shapes perceptions on the evolution oforganismal complexity.

Brachipoda, Phoronida, Bryozoa
Another consistent result is that “Lophophorata” is not a monophyletic taxon,
as long advocated on the basis of morphology (Nielsen 1985, 1987, 2001). Brachiopods and phoronids form a monophyletic entity, with bryozoans considerably
removed. This result has been supported by SSU (Halanych et al. 1995, Mackey
et al. 1996, Eernisse 1997), morphology and SSU (Zrzavy et al. 1998, Giribet et al.
2000, Peterson & Eernisse 2001), and morphology (Nielsen et al. 1996, Nielsen2001). Lophophorate monophyly can be significantly rejected on the basis ofcombined SSU and LSU data (Y.J. Passamaneck & K.M. Halanych, unpublishedresults). In these analyses, brachiopods and phoronids tend to be placed near eutrochozoan taxa (e.g., annelids, mollusks; see de Rosa 2001, Eernisse 1997), andbryozoans are the most basal lineage of Lophotrochozoa. Whereas Giribet et al.
(2000) suggested that bryozoans were basal protostomes, Hox data from bryozoans
confirm their placement in Lophotrochozoa, probably as basal (Passamaneck &Halanych 2004). Cohen and coworkers (Cohen et al. 1998, Cohen 2000) suggested,on the basis of SSU data, that phoronids are derived brachiopods, but subsequent
analysis suggests that they are sister taxa (Peterson & Eernisse 2001). Proposals
have been put forth to recognize the new clade as either Brachiozoa (CavalierSmith et al. 1998), Phoronozoa (Zrzavy et al. 1998), or Lophophorata (Peterson &Eernisse 2001). The first two options represent two sides of the proverbial coin, but
the last option is problematic because the term “lophophore” has a long history of
being applied to brachiopods, phoronids, bryozoans, and even pterobranch hemichordates (Halanych 1996a). As such, the change in definition of Lophophorata
will introduce confusion into the literature.

Other Taxa
Several other taxa deserve attention in the context of the Lophotrochozoa. As
with annelids, within mollusks we do not have a good understanding of major
relationships (see Haszprunar 2000, Steiner & Dreyer 2003, Medina & Collins
2003, Passamaneck et al. 2004). Although most analyses tend to place annelids
and mollusks close to each other (e.g., Zrzavy et al. 1998, Giribet et al. 2000,
Peterson & Eernisse 2001), we do not know how several other taxa fit in, forexample scipunculans, nemerteans, and the brachiopod/phoronid clade. Examining
SSU data alone in this region of the tree is problematic because they do not recoverrecognized phyla as monophyletic (e.g., mollusks, brachiopods, nemerteans). Thissituation is highlighted in Eernisse’s (1997) work, which discusses the positive31 Oct 2004 12:33

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influence of more robust taxon sampling. A combined analysis of SSU and LSU
recovers most “phyla” as monophyletic, but interphylum relationships are basedon very short-branch lengths (Y.J. Passamaneck & K.M. Halanych, unpublishedresults). These short-branch lengths would be expected in the case of a rapid
radiation such as the Cambrian explosion.
Nemerteans are also lophotrochozoans (Turbeville et al. 1992, Kmita-Cunisse
et al. 1998, de Rosa et al. 1999, Balavoine et al. 2002), consistent with embryology and morphology. Sipunculans appear close to mollusks morphologically(Scheltema 1993), but recent mitochondrial gene order data place them near annelids (Boore & Staton 2002). SSU and combined analyses do not provide strong
support for a sipunculid placement other than that they are within Lophotrochozoa(Zrzavy et al. 1998, Giribet et al. 2000, Peterson & Eernisse 2001). Dicymids
and Orthonectids (also known as Mesozoa) were once thought of as intermediates
between protists and metazoans. However, molecular evidence suggests that thesetwo (likely independent) groups are degenerate triploblast animals (Katayama et al.
1995, Hanelt et al. 1996, Pawlowski et al. 1996). Dicymids were shown to containthe lophotrochozoan-specific peptide motif in their lox5 homolog (Kobayashi et al.
1999). However, the position of orthonectids is less certain and may be basal in
Bilateria (Hanelt et al. 1996). Entoprocts and cycliophorans also present a bit of amystery. The placement of Entoprocta is variable but consistently within Lophotrochozoa (Mackey et al. 1996, Eernisse 1997, Giribet et al. 2000, Peterson & Eernisse
2001). Cycliophorans were first proposed to be close to entoprocts on the basis ofmorphological similarities (Funch & Kristensen 1995), but preliminary SSU data
placed them close to rotifers (Winnepenninckx et al. 1998). This result has been
supported by one combined evidence analysis (Peterson & Eernisse 2001) but refuted by two others (Zrzavy et al. 1998, Giribet et al. 2000). LSU data support the
Cycliophora/Entoprocta clade (Y.J. Passamaneck & K.M. Halanych, unpublishedobservations), as does morphological cladistic analysis (Sørensen et al. 2000).
Noteworthy lophotrochozoan analyses using solely molecular data have notsupported a clade with spiral cleavage sensu stricto (i.e., Spiralia).3 This result ispartly due to the lack of resolution currently in this region of the tree, yet we must be
open to the possibility that spiral cleavage is not strictly evolutionarily conserved.
In particular, phoronids and brachiopods seemed to be allied with annelids andmollusks to the exclusion of, at least, platyhelminths (as generally judged bymolecules). Given that phoronids and brachiopods have radial or biradial cleavage(Zimmer 1997), we must accept that spiral cleavage, at least, has been lost insome lineages. Thus, there is no monophyletic lineage that includes all spiralcleavers to the exclusion of other cleavage patterns. Recent cell lineage work
further demonstrated that phoronids show no vestiges of 4d mesoderm specification
expected in spiral cleavage (Freeman & Martindale 2002). For a critical evaluationof spiral cleavage as a phylogenetic character, see Jenner (2004).

3

In fact, because of the placement of platyhelminthes, most traditional treatments also do
not have a monophyletic Spiralia.

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ECDYSOZOAThe clade Ecdysozoa circumscribes those animals that have a cuticle shed throughmolting (i.e., ecdysis). Aguinaldo et al. (1997) formally proposed this clade, on
the basis of SSU rDNA results, to include the last common ancestor of arthropods,
tardigrades, onychorans, nematodes, nematomorphs, kinorhynchs, and priapulids,
and all the descendants of that last common ancestor. Previous SSU analyses
including nematodes typically found round worms clustering at the base of Bilateria (e.g., Winnepenninckx et al. 1995). Aguinaldo et al. (1997) assessed theposition of nematodes using a more slowly evolving nematode sequence (in thiscase Trichinella), eliminating the potential problem of long-branch attraction. Interestingly, a previous cladistic morphological study (Eernisse et al. 1992) had
also recovered the same clade of molting animals (with the exception that Priapulida was part of a basal polytomy). Initial acceptance of this radical revision
was slow because it was based on a single nematode sequence. However, it has
been subsequently supported by independent data sets, most notably Hox genes(Ubx, abd-A, and Abd-B have ecdysozoan-specific peptides; de Rosa et al. 1999,
Balavoine et al. 2002), LSU rDNA data (Mallat & Winchell 2002, Mallat et al.
2004), and combined morphology and SSU (Zrzavy et al. 1998, Giribet et al. 2000,
Peterson & Eernisse 2001). Additionally, Haase et al. (2001) report that Ecdysozoa
show neural expression of horseradish peroxidase (HRP) immunoreactivity thatis absent in other animals. They suggest that the presence of anti-HRP-reactive
glycoprotein(s) is a synapomorphy for Ecdysozoa.
The presence of a multimeric form of β-thyomosin that was hypothesized as
an ecdysozoan synapomorphy (Manuel et al. 2000) has been shown to be present
in other metazoans (Telford 2004a). Also, genome-scale analyses have claimed torefute the Ecdysozoa hypothesis (e.g., Blair et al. 2002, Wolf et al. 2004), but unfortunately these analyses are flawed owing to limited taxon sampling (containing
only three or four metazoan taxa total) and the inability to correct adequately forhighly derived Caenorhabditis elegans sequences (i.e., long-branch issues). Wolfet al. (2004) did try to address the long-branch issue, but their effort was hampered by their limited number of metazoan taxa, three. For additional discussion
concerning the problems of these papers, see Telford (2004b).
The Ecdysozoa hypothesis has had perhaps the most far-reaching effects oncomparative biology because of the large amount of work on Drosophila andCaenorhabditis. Before the Ecdysozoa hypothesis, if a common genetic mechanism was found in both flies and round worms, it was presumed to be present
throughout Bilateria. With the placement of these two taxa as members of the same
lineage, the common machinery may be representative of only the ecdysozoan lineage, thereby limiting the inferences drawn from these model organisms.

Scalidophora and Nematoida
Researchers have limited knowledge of interrelationships within Ecdysozoa because many of the taxa are poorly studied. For example, in early 2004, only 1

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GenBank entry existed for Kinorhyncha, 19 for Nematomorpha, and 26 for Priapulida. Nonetheless, there seems to be a general consensus which awaits further
conformation. The Priapulida/Kinorhyncha/Loricifera clade should be referred
to as Scalidophora (Lemburg 1995, Schmidt-Rhaesa 1996, Ehlers et al. 1996).
Nielsen (2001) has used the name Cephalorhyncha for this clade, but previous
usage of this term included the Nematomorpha (Malakhov 1980). Within thisgroup, loriciferans are most likely sister taxon to kinorhynchs (Schram 1991,
Sørensen et al. 2000, Peterson & Eernisse 2001), but no loriciferan molecular
data have been collected because of difficulty in obtaining tissue. When loriciferans are not considered, priapulids and kinorhynchs form a monophyletic clade(Aguinaldo et al. 1997, Aleshin et al. 1998, Giribet et al. 2000, Peterson & Eernisse
2001).
The horsehair worms, Nematomorpha, are allied with Nematoda. This group,
termed Nematoida (Schmidt-Rhaesa et al. 1998), has been supported in some analyses (Zrzavy et al. 1998; Giribet et al. 2000, combined data; Garey 2001) but notothers (Giribet et al. 2000, SSU only; Peterson & Eernisse 2001). Using combined
SSU and LSU data, Mallat et al. (2004) found strong support for Nematoida. The
combined group of Scalidophora and Nematoida has been referred to as either
the Introverta or Cycloneuralia (Nielsen 2001), but it is refuted by available data
(Zrzavy et al. 1998, Peterson & Eernisse 2001, Mallat et al. 2004; but see Giribet
et al. 2000). Instead, the Scalidophora is the most basal branch in the Ecdysozoa,
with Nematoida and Panarthropoda (Tardigrada, Onychophora, and Arthropoda)
as sister clades.

Panarthropoda
Within the Panarthropoda, the placement of tardigrades, onychophorans, andarthropods relative to each other has generated considerable debate. Early mitochondrial SSU data suggested that Onychophora were inside the Arthropoda(Ballard et al. 1992), and papers that reported a Tardigrada/Arthropoda relationship did not include an onychophoran (Garey et al. 1996a, Giribet et al. 1996).
The rDNA analyses of Mallat et al. (2004) suggested an onychophoran/tardigrade
clade, but the authors were tentative about this result because onychophoran rDNA
appears very derived, and nodal support is weak. This result was also recoveredby Giribet et al.’s (2000) combined morphology and SSU analyses.
Although of great interest, I do not discuss the relationships within the arthropods in detail. Recent work on the subject has used a variety of molecular markers (rDNA, Hox genes, mtDNA arrangement), and these are discussed elsewhere(Giribet & Ribera 2000, Giribet et al. 2001, Hwang et al. 2001, Cook et al. 2001,
Mallett et al. 2004). The most notable change in arthropod phylogeny is the placement of Hexapoda within Crustacea to form Pancrustacea. This hypothesis wasconvincingly put forth by Regier & Shultz (1997) on the basis of EF-1α and hasreceived considerable support (e.g., Cook et al. 2001, Mallett et al. 2004). Also thepreviously recognized phylum Pentastomida, parasites on vertebrates, is a derived
crustacean clade (Abele et al. 1989, Lavrov et al. 2004).

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Dis-Articulating
One reason many were resistant to the Lophotrochozoa and Ecdysozoa hypothesesis that they contradicted the Articulata (Arthropoda and Annelida) as a real clade.
Despite the overwhelming evidence that annelids are much more closely related tomollusks than to arthropods (based on morphology as well at least five independent
molecular markers), there are still attempts to maintain an Articulata-like clade(e.g., Nielsen 2003). The segmented nature of annelids and arthropods has a long
history of being used to unite these taxa (Willmer 1990). Although genes involvedin the segmentation program in arthropods (e.g., Drosophila) are well studied (fora general review, see Carroll et al. 2001), very little is known about segmentationin annelids. What we do know is that segmentation-related genes (e.g., engrailed
and hunchback) in Drosophila appear to be doing something different in annelids(Seaver et al. 2001, Werbrock et al. 2001, but see Prud’homme et al. 2003). Seaver(2003) reviews the possibilities of independent origins of segmentation in annelids,
arthropods, and chordates. As she points out, all these taxa are nested within several
nonsegmented taxa. Thus, any attempt to infer that an ancestor deep in the bilateriantree was segmented also required multiple losses of segmentation in numerous
different lineages. Given that genetic machinery for segmentation does not appear
to be the same, a segmented protostome or bilaterian ancestor is not likely.
Proponents of the Articulata hypothesis assert that segmentation is a very strong
morphological character and thus a good phylogenetic indicator. Yet from an objective point of view there is no reason segmentation should be a better indicatorof phylogenetic history than molting (in ecdysozoans) or a trochophore larva (in asubset of lophotrochozoans). The Articulata hypothesis also suggests that cleavage
patterns are not immutable, as arthropods lack spiral cleavage. All these characters
are intricately tied to constraints in functional morphology for which we have little
understanding of the selective forces or evolutionary plasticity.

CAMBRIAN EXPLOSIONAs should be clear from the previous discussion, understanding the early evolutionary events of animal history is difficult. This situation has not been made any
easier by the lack of a substantial fossil record before about 570 Mya. At roughly
543 Mya, the fossil record shows a sudden diversity of animal forms that represent
most of the major lineages, with some taxa displaying great diversity and derived
body plans (reviewed in Grotzinger et al. 1995, Knoll & Carroll 1999, Erwin &Davidson 2002). This sudden appearance of diversity in the fossil record is called
the Cambrian explosion.
Recent finds for the Lower Cambrian Chengjiang and Sirius Passet faunas(approximately 520 Mya) have provided exquisitely preserved samples of animals(Conway Morris & Peel 1995, Chen & Zhou 1997, Bengston & Zhao 1997, Shu
et al. 1999). Older fossils from the Ediacaran and Doushantuo formations (upto 570 Mya) predate the Cambrian boundary and show that some animal lineages
were present well before the Cambrian (Xiao et al. 1998). For the period before the31 Oct 2004 12:33

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Doushantuo formation (which yielded sponges and fossil embryos; Li et al. 1998,
Xiao et al. 1998), fossils for animals are generally lacking, despite the presencein the fossil record of several other eukaryotic crown groups dating back to 1200
Mya (Erwin & Davidson 2002). [The report by Seilacher et al. (1998) of ancient
worm trace fossils was erroneous (Rai & Gautam 1999, Rasmussen et al. 2002).]
In contrast to the fossil data, several recent works have reported using a molecular clock to date animal diversification (Wray et al. 1996, Nikoh et al. 1997, Ayala
et al. 1998, Gu 1998, Bromham et al. 1998, Lynch 1999). These works report thatbilaterians diverged between 630 and 1200 Mya. Several workers (e.g., Philippe
et al. 1994, Smith & Peterson, 2002; see Graur & Martin 2004 for a particularlycolorful discussion) have highlighted some of the problems with using a molecular
clock to date deep divergences. In particular, clock studies have been plagued byassumptions of rate homogeneity in nucleotide substitution patterns. Even when
nucleotide substitution models can correct for rate variation across different positions in the same gene, available molecular tools are not sophisticated enough (yet)to deal adequately with rate variation across lineages within the same tree. Furthermore, many molecular clock analyses made the mistake of overgeneralizing theirresults. Specifically, they used only a limited number (3–5) of fossil calibration
points, typically within craniates or other deuterostomes, whereas the Cambrian
explosion was mainly lophotrochozoan and ecdysozoan in nature and involved
numerous lineages (although we must recognize the diversity of echinoderms andpresence of early chordates).
On the positive side, studies of molecular clocks have called our attention toa hidden history of early animal evolution. Although the fossil data suggested
this hidden history was very short in nature (∼30 My), molecular clock analyses
in general suggested a much longer hidden history (up to 700 My; see Erwin &Davidson 2002). This last scenario seems unlikely because fossils of other crowneukaryotes are known from this period, necessitating ad hoc hypotheses to accountfor the dearth of animal fossils in particular.
The fact that there is any hidden history, regardless of duration, suggests thatearly animals were very small organisms, likely meiofaunal or small epibenthic
dwellers. Such organisms would not fossilize easily (but the Chengjiang, Sirius
Passet, and Doushantuo formations have proven the exception) and were probably
direct developers. Another argument against a segmented last common bilaterianancestor is that miniaturization can apparently reduce segmentation (Westheide
1997).

CONCLUSIONSOur understanding of metazoan phylogeny is far from complete. However, in thepast 15 years we have made tremendous progress toward understanding the general framework of animal evolution. Relationships among the most basal lineagesof animals are not entirely clear, but poriferans are likely a paraphyletic gradethat led to a Cnidarian/Bilaterian clade. Within Bilateria, we have three major
clades. Lophotrochozoa is the most diverse clade in terms of body plans, and31 Oct 2004 12:33

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understanding their internal relationships will take considerable work. How Platyzoa fit into this group also remains to be seen. Ecdysozoa groups nematodes andarthropods and has implications for how we extrapolate information from model
systems. Chaetognaths are likely to be basal to Ecdysozoa and Lophotrochozoa.
Deuterostomia only contains a limited number of lineages, but the presence of
the Ambulacraria (echinoderms and hemichordates) suggests that several chordate features evolved earlier than traditionally believed. At the base of Bilateria,
we have the Acoelomorpha and possibly Myxozoa.
Compared with the Hyman-like concept of animal phylogeny, this new view
underscores the evolutionary plasticity of embryology and functional morphology.
Many of the dogmatic concepts in invertebrate biology must be questioned (e.g.,cleavage patterns are immutable, evolution proceeds from simple to complex,
segmentation is highly conserved).
Clearly, several relationships still need to be worked out. To promote additional research on metazoan evolution, below are ten provocative hypotheses thatare likely to provide considerable insight into animal evolution when tested in arigorous manner:
1. Placozoans branched off from the main animal lineage before sponges.
2. Mesoderm first arose in ctenophores.
3. Acoelomorphs are secondarily simplified animals.
4. Chaetognatha is the sister to the Lophotrochozoa/Ecdysozoa clade.
5. Spiral cleavers do not form a monophyletic clade exclusive of other cleavage
patterns.
6. Genetic mechanisms controlling annelid segmentation are different than inarthropods.
7. The Brachiopoda/Phoronida clade is sister to Mollusca.
8. Panarthopoda evolved from a small infaunal organism.
9. Platyzoa is a derived subclade of Lophotrochozoa.
10. The hidden history of early bilaterian evolution was less than 50 My.
NOTE ADDED IN PROOF
While this work was in press, Anderson et al. (2004) published datafrom the sodium-potassium ATPase α-subunit gene, which also supports the
Lophotrochozoa and Ecdysozoa hypotheses, but did not recover deuterostomes
or Arthropods as monophyletic.
ACKNOWLEDGMENTS
I thank all those who over the years have provided fruitful discussions concerning
animal evolution, including those at the Lambert residence at Friday Harbor Laboratories. Drew Harvell’s support of this review is most appreciated. Comments
by T. Struck and J.H. Halanych are most appreciated. C.N. Halanych and J.M.

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Halanych freely shared time to support this work. H. Blasczyk assisted with figures. This work was supported by the National Science Foundation (DEB-0075618,
EAR-0120646, and IBN-0333843).
The Annual Review of Ecology, Evolution, and Systematics is online at
http://ecolsys.annualreviews.org

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Figure 1 Traditional synthesis. The understanding of metazoan evolution prior to
Field et al. (1988). This tree is drawn to illustrate major concepts. The tree is color
coded to match the clades consistent with our current understanding as shown in
Figure 2: Brown is Metazoa, gray is Bilateria, green is Deuterostomia, dark green isAmbulacraria, red is Ecdysozoa, blue is Lophotrochozoa, magenta is Platyzoa, andblack is nonmetazoan. Researchers have proposed many variations of this generalhypothesis. For example, many viewed Bryozoa, Brachiopoda, and Phoronida as
forming a monophyletic Lophophorata. Also, it was widely recognized that the
Aschelminthes was probably not a natural group. Note that, for illustrative purposes, not all taxa shown in Figure 2 are shown here. Filled circles correspond tolabeled nodes. Dashed vertical lines indicate groups that are not monophyletic.

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HALANYCH

Figure 2 Modern synthesis. The new view of animal phylogeny based largely on
molecular data. Details and support for various clades are discussed in the text. This
figure is intended to be slightly conservative in nature, as poorly resolved issues areshown as polytomies. The tree is color coded: Brown is Metazoa, gray is Bilateria,
green is Deuterostomia, dark green is Ambulacraria, red is Ecdysozoa, blue is
Lophotrochozoa, magenta is Platyzoa, and black is nonmetazoan. Nested clades of
one color may be inside a more inclusive clade of another color. For example,
Echinodermata is dark green because it is within Ambrulacraria, but it is also adeuterostome (green), bilaterian (gray), and metazoan (brown). Note that
Siboglinidae is the preferred name for the pogonophoran/vestimentiferan lineage,
and the position of Orthonectida as a basal bilaterian needs confirmation. Filled circles correspond to labeled nodes. Dashed vertical lines indicate groups that are notmonophyletic.

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CONTENTS
VERTEBRATE DISPERSAL OF SEED PLANTS THROUGH TIME,
Bruce H. Tiffney

1

ARE DISEASES INCREASING IN THE OCEAN? Kevin D. Lafferty,
James W. Porter, and Susan E. Ford

31

BIRD SONG: THE INTERFACE OF EVOLUTION AND MECHANISM,
Jeffrey Podos, Sarah K. Huber, and Benjamin Taft

55

APPLICATION OF ECOLOGICAL INDICATORS, Gerald J. Niemi
and Michael E. McDonald

89

ECOLOGICAL IMPACTS OF DEER OVERABUNDANCE, Steeve D. Côté,
Thomas P. Rooney, Jean-Pierre Tremblay, Christian Dussault,
and Donald M. Waller

113

ECOLOGICAL EFFECTS OF TRANSGENIC CROPS AND THE ESCAPE
OF TRANSGENES INTO WILD POPULATIONS, Diana Pilson
and Holly R. Prendeville

149

MUTUALISMS AND AQUATIC COMMUNITY STRUCTURE: THE ENEMY
OF MY ENEMY IS MY FRIEND, Mark E. Hay, John D. Parker,
Deron E. Burkepile, Christopher C. Caudill, Alan E. Wilson,
Zachary P. Hallinan, and Alexander D. Chequer

175

OPERATIONAL CRITERIA FOR DELIMITING SPECIES, Jack W. Sites, Jr.,and Jonathon C. Marshall199

THE NEW VIEW OF ANIMAL PHYLOGENY, Kenneth M. Halanych
LANDSCAPES AND RIVERSCAPES: THE INFLUENCE OF LAND USE ON
STREAM ECOSYSTEMS, J. David Allan
LONG-TERM STASIS IN ECOLOGICAL ASSEMBLAGES: EVIDENCE FROM
THE FOSSIL RECORD, W.A. DiMichele, A.K. Behrensmeyer,

257

T.D. Olszewski, C.C. Labandeira, J.M. Pandolfi, S.L. Wing, and R. Bobe

285

229

AVIAN EXTINCTIONS FROM TROPICAL AND SUBTROPICAL FORESTS,
Navjot S. Sodhi, L.H. Liow, and F.A. Bazzaz

EVOLUTIONARY BIOLOGY OF ANIMAL COGNITION, Reuven Dukas
POLLINATION SYNDROMES AND FLORAL SPECIALIZATION,
Charles B. Fenster, W. Scott Armbruster, Paul Wilson,
Michele R. Dudash, and James D. Thomson

323
347

375
v

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vi

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CONTENTS

ON THE ECOLOGICAL ROLES OF SALAMANDERS, Robert D. Davicand Hartwell H. Welsh, Jr.

ECOLOGICAL AND EVOLUTIONARY CONSEQUENCES OF MULTISPECIESPLANT-ANIMAL INTERACTIONS, Sharon Y. Strauss and Rebecca E. Irwin
SPATIAL SYNCHRONY IN POPULATION DYNAMICS, Andrew Liebhold,
Walter D. Koenig, and Ottar N. Bjørnstad

405
435
467

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ECOLOGICAL RESPONSES TO HABITAT EDGES: MECHANISMS,
MODELS, AND VARIABILITY EXPLAINED, Leslie Ries,
Robert J. Fletcher, Jr., James Battin, and Thomas D. Sisk

491

EVOLUTIONARY TRAJECTORIES AND BIOGEOCHEMICAL IMPACTS OF
MARINE EUKARYOTIC PHYTOPLANKTON, Miriam E. Katz,
Zoe V. Finkel, Daniel Grzebyk, Andrew H. Knoll, and Paul G. Falkowski

523

REGIME SHIFTS, RESILIENCE, AND BIODIVERSITY IN ECOSYSTEMMANAGEMENT, Carl Folke, Steve Carpenter, Brian Walker,
Marten Scheffer, Thomas Elmqvist, Lance Gunderson, and C.S. Holling

557

ECOLOGY OF WOODLAND HERBS IN TEMPERATE DECIDUOUS FORESTS,
Dennis F. Whigham

583

THE SOUTHWEST AUSTRALIAN FLORISTIC REGION: EVOLUTION ANDCONSERVATION OF A GLOBAL HOT SPOT OF BIODIVERSITY,
Stephen D. Hopper and Paul Gioia

PREDATOR-INDUCED PHENOTYPIC PLASTICITY IN ORGANISMS WITHCOMPLEX LIFE HISTORIES, Michael F. Benard
THE EVOLUTIONARY ECOLOGY OF NOVEL PLANT-PATHOGEN
INTERACTIONS, Ingrid M. Parker and Gregory S. Gilbert

623
651
675

INDEXES
Subject Index
Cumulative Index of Contributing Authors, Volumes 31–35
Cumulative Index of Chapter Titles, Volumes 31–35

ERRATA
An online log of corrections to Annual Review of Ecology,
Evolution, and Systematics chapters may be found at
http://ecolsys.annualreviews.org/errata.shtml

701
721
724