DIVERSITY OF LIFE

DESCRIPTION OF THE KINGDOM ANIMALIA (LINNAEUS 1758)

EUKARYA>UNIKONTA>OPISTHOKONTA>ANIMALIA
Animalia (ah-nee-MAH-lee-uh) is derived from the Latin word, Animalis, which means a living thing.  It also can refer to things that breathe or have a soul.  

INTRODUCTION TO THE KINGDOM ANIMALIA

Animalia is the most speciose and morphologically-diverse kingdom of eukaryotes.  We interpret the kingdom as having two unequal subkingdoms: a unicellular-colonial group [Choanozoa (Cavalier-Smith 1993)] and a multicellular group [Metazoa (Haeckel 1866)].  Table 1 compares the two subkingdoms according to  characters that are distinctive of animals and supported by a full genome analysis of a unicellular choanozoan (King et al. 2008).  Sorensen et al. (2000) and Eernisse and Peterson (2004) consider Choanozoa to be the sister group of the Metazoa within the kingdom Animalia.  If Choanozoa were not considered to be animals, then they would have to be raised to a rank equivalent to Metazoa (=Animalia).  We feel that the addition of another kingdom is not warranted especially since the attributes of Table 1 generally overlap between the two taxa.  Those characters in the Choanozoa related to sexual reproduction are unknown because a sexual life history has never been observed.

 

 

TABLE 1. Characters of Metazoa and comparisons with those of the Choanozoa.  The information was taken from Nielsen (2008), King et al. (2008), and Blackstone (2009).

CHARACTER

CHOANOZOA

METAZOA

COLLAGEN

YES

YES

EXTRACELLULAR MATRIX

YES

YES

CELL ADHESION MOLECULES

YES

YES

DEVELOP FROM A BLASTULA

NO

YES

HOX & TRANSCRIPTION FACTOR GENES

YES, BUT NO HOX GENES

YES

GAMETIC MEIOSIS

?

YES

OOGAMOUS SEXUAL REPRODUCTION

?

YES

SPERM WITH A SINGLE POSTERIOR FLAGELLUM

?

YES

SPERM WITH ACROSOME

?

YES

CELLULAR DIFFERENTIATION

NO

YES

 

 

Collagen is a structural protein that occurs in animal cells and in the extracellular matrix (Wolfe 1993).  It is very common in connective tissue and muscle and can be the most abundant protein in humans and other mammals (Di Lullo et al. 2002).  In addition to collagen and other fibrous proteins, the extracellular matrix has proteoglycans, which together fill the spaces between the cells and keep them hydrated.  Animal cells also have adhesion molecules that help form tight junctions between cells making impermeable boundaries between cells.  Thus, tissues of cells may form chambers within which controlled extracellular actions, like digestion, can occur.  Furthermore, the connections between animal cells permit the movement of nutrients through tissues and make the compartmentalization possible in the formation of large, multicellular bodies with many cell types, tissues, and organs.

The development of a typical metazoan follows a relatively simple pattern in the sexual life history (see Figure 1A).  Meiosis occurs in the steps leading to the production of gametes (gametic meiosis), and the gametes are eggs and sperm (oogamy).  Animal sperm have a single posteriorly-directed flagellum, and the head of the sperm usually contains an acrosome, a specialized organelle that digests its way through the membranes of the egg.  Though the sexual life history is somewhat simple compared to other eukaryotes, the developmental cycle is remarkably complex and stylized leading to the formation of differentiated cells in tissues and organs.  The zygote, the first cell following syngamy, undergoes an initial cleavage (see Figure 1B), which usually is radial, but in one line of Bilateria (Hatscheck 1888) is spiral.  The initial divisions lead to a hollow ball of cells, the blastula (see Figure 1C).  This stage is so characteristic that Margulis and Schwartz (1998) defined Animalia as a kingdom of organisms that developed from a blastula.  The blastula polarizes and a region of cells begins to invaginate.  The resulting structure is the gastrula (see Figure 1D) that has an outer layer of ectoderm and an inner layer of endoderm, which forms the archenteron, and communicates to the outside by the blastopore.  The two layers differentiate into a covering and much of the nerve tissue (ectoderm derivatives) and the digestive layer.  Among the radiates, the archenteron is persistent and remains with a single opening for the digestive system.  A major innovation of the bilaterians is the formation of a secondary pore which makes a complete digestive tube.  The bilaterians, and perhaps also the Ctenophores, have a third developmental germ cell layer, the mesoderm, that forms between the endoderm and ectoderm.  From this layer develops much of the muscle and connective tissue of most animals.

The development of a relatively complex animal body from a fertilized egg requires a sequence of delicately-controlled gene expressions.  This is accomplished through a coordinated series of transcription factors that modulate the expression of genes in given cells.  Pirez-daSilva and Sommer (2003) suggest that the extraordinary diversity of cell form and type can be accounted for by just a few signaling pathways (e.g. Hedgehog, Wnt, Notch, JAK/STAT, and nuclear transforming pathways), most of which are activated by the communication of one cell with another during development.  Some of the most interesting control genes are the homeobox or Hox genes, which seem to be associated with the anterior-posterior gradient that becomes established during the developmental history of an animal.  Clusters of Hox genes function to provide a regional identity to the axis, which is well illustrated in the segmentation of insects or chordates (Gellon and McGinnis 1998, Pearson et al. 2005, and Pratihar et al. 2010).  Thus, cellular diversity and specific structures along the anterior-posterior axis are determined by finely-tuned cascades of regulatory genes and signaling pathways in animals.

 
 
A.
B.
C.
D.
FIGURE 1. THE UNIVERSAL STAGES IN THE LIFE CYCLE OF A METAZOAN ANIMAL.  A. Stages of the sexual life history of the typical animal.  Black arrows indicate diploid changes and the striped arrows indicate the short-lived haploid stages.  B. Two of the common types of cleavage to the 8-cell stage.  Spiral cleavage forms a ball of cells in which the daughter mitotic products are alternating.  Radial cleavage forms a ball of cells in which the daughter cells overly each other.  C.  The blastula is formed by repeated divisions that give rise to a hollow ball of cells.  D. The gastrula is formed when a region on the blastula infolds to form a blastopore and an archenteron.  Thus the outer cell layer becomes the ectoderm and the inner layer is the endoderm.

 

 
Origins of the Metazoa

All metazoan groups have taxa that produce bilaterally-symmetrical larvae.  Even sponges, which appear to be so simple that they seem to be the most unlikely candidates for the Metazoa, produce larvae that resemble free-swimming blastulae or gastrulae (see Figure 2).   Radially-symmetrical groups like Cnidaria (Hatschek 1888) and Ctenophora (Eschscholtz 1829), also produce free-swimming bilaterally-symmetrical larvae that resemble small ciliated flatworms (e.g. planulae and cydippids, respectively).  Even Darwin (1859) suggested that affinities between taxa should be determined by looking at the larval stages.  Thus, very disparate mature forms can have strikingly similar early developmental stages.  Nielsen (2008) proposed that the sponge larval form was the foundation of the rest of the Metazoa and suggested a six stage series from the typical swimming blastula-like larva of the Demospongiae (Sollas 1885) to a gastrula-type.  In Nielsen's theory, the sponge larval form became sexually mature with the loss of the adult form in an event called paedomorphosis.  The gastrula then developed a ring of sensory tissue around the blastopore.  A Hox cluster appeared and became more complex forming a bilaterally-symmetrical elongated form that developed a complete food tube (with a mouth and an anus) and a compartmented body.  This scenario is consistent with developmental histories of both diplobalstic and triploblastic organisms.  Also, it is consistent with a scenario in which sponges are reduced metazoans (Mann 2010).  

Phylogenomic studies (e.g. Dunn et al. 2008; Hejnol et al. 2009; Nosenko et al. 2013; Ryan et al. 2013; Moroz et al. 2014; Whelan et al. 2015) show Ctenophora as the sister to all other Metazoa.  The ctenophores or comb jellies have been kicked about in the stem region of the animal tree.  Such a ctenophore-sister position would mean the the last common ancestor of the Metazoa was quite complex with organs and tissues such as muscles and nervous systems, which were lost in the parazoan line (Jekely et al. 2015).  Figure 3 A-D illustrates how the ctenophores and sponges occupy different basal positions with each of the four hypotheses: Porifera-Sister Hypothesis (Figure 3A after Salchian-Tabrizi et al. 2008; Edgecombe et al. 2011; Nosenko et al. 2013; Zhang et al. 2013; Pisani et al. 2015), Ctenophore-Sister Hypothesis (Figure 3B after Dunn et al. 2008; Hejnol et al. 2009; Ryan et al. 2013; Moroz et al. 2014; Whelan et al. 2015), Ctenophore + Porifera-Sister Hypothesis (Figure 3C after Ryan et al. 2013) and the traditional Morphology-Phylogeny Based Hypothesis (Figure 3D after Telford et al. 2015).


FIGURE 2

 

 

THE ANIMAL KINGDOM

Hz = Holozoa

Fz = Filozoa

An = Animalia

Mz = Metazoa

Em = Eumetazoa

Co = Coelenterata

Tr = Transitional Eumetazoa

FIGURE 3. Competing theories regarding the sister relationship within the Metazoa. Specifically, the theories focus on the sponges and ctenophores and their sister relationships relative to the rest of the Metazoa.  A. The Porifera-Sister Hypothesis (after Salchian-Tabrizi et al. 2008; Edgecombe et al. 2011; Nosenko et al. 2013; Zhang et al. 2013; Pisani et al. 2015)  B. The Ctenophora-Sister Hypothesis (after Dunn et al. 2008; Hejnol et al. 2009; Ryan et al. 2013; Moroz et al. 2014; Whelan et al. 2015).  C. The Porifera + Ctenophora Hypothesis (after Ryan et al. 2013).  D. The Traditional Morphology-Based Hypothesis (after Telford et al. 2015).  Porifera and Ctenophora have been highlighted to illustrate their changing positions in each hypothesis.

 

 

Pisani et al. (2015) and Simion et al. (2017) demonstrate convincingly that the proposed basal or ctenophore-sister position of the Ctenophora is an artifact of improperly applied molecular phylogenetic methods.  For example, they claim that methods used in the analyses did not attempt to compensate for long-branch attraction, an artifact of phylogenetic analysis that tends to group distantly-related taxa if the comparisons are from rapidly evolving portions of the genome.  They also site the early authors for using improper evolutionary models and inappropriate outgroups.  Pisani et al. (2015) and Simion et al. (2017) used the genomic data sets of the earlier studies and came up with a clear parazoa-sister signal as indicated in Figure 3A.  We used this argument and evidence to construct the cladogram in Figure 4.

Such scenarios using living animals as models can lead to misinterpretation of the evidence.  Fossil evidence suggests that the last common ancestor of the Metazoa lived in the upper Precambrian.  Phosphatized remains of small bilaterian animals with a coelom and complete food tube have been found in China (Chen et al. 2004), which implies that the bilaterian form may have been similar to the last common ancestor.  Furthermore, trace fossils of animals interpreted as triploblastic burrowing worms from rock more than a billion years old have been found in India (Seilacher et al. 1998) and similar fossils occur in rock more than 1.2 billion years old in southwestern Australia (Rasmussen et al. 2002).  Thus, the bilaterians need not be interpreted as derived from the basal metazoan taxa, but could represent the basal group from which the others sprang.

In the late Precambrian, during a period called the Cryoginian (720-635 mya), the earth underwent a series of global glaciation events punctuated by periods of greenhouse warming (Hoffman et al. 1998; Hoffman and Schrag 2000).  The last glaciation ended around 635 million years ago, which is remarkably close to the postulated time of the last common ancestor of the Metazoa.  Soon after that, a strange, flattened fauna, the Ediacaran fauna (from the Ediacaran period, 635-541 mya), appeared and diversified in the later Precambrian seas.  They appeared to be bilaterally or radially-symmetrical, usually were quilted in a way that appeared to be segmented, and had a clear anterior-posterior axis (see Figure 5).  Narbonne (2005) suggests that the ediacarans were mixtures of basal animals like ctenophores, cnidarians and bilaterians together with groups that have become extinct; however, (Dzik 2003) argues that ediacarans were outside of the mainstream of metazoan evolution.  Typical pleated animals such as Dickinsonia (Figure 3) likely fed on the pervasive near shore photosynthetic microbial mats.  Before the advent of large microbial predators, photosynthesis occurred without control, which may have removed enough atmospheric carbon to cause the snowball earth glaciations, which, in turn, cut off most photosynthesis allowing for a buildup of greenhouse gasses.  These snowball-greenhouse swings between 720 and 636 million years ago may have been the evolutionary cauldron in which animals were forged.  With the development of more diverse animal faunas following the late precambrian, a rapid increase in animal diversity gave rise to the Cambrian Explosion in which almost all existing animal phyla appeared.

Despite problems with the stem taxa of the animal kingdom and nature of the Ediacaran faunas, the Animal Kingdom  is a natural, though highly diverse group of organisms, most of which are multicellular and develop from a blastula (Margulis and Schwartz 1998).  At a deeper level, the Animal Kingdom (metazoans + choanoflagellates) is a sister group of the fungi (Bauldauf and Palmer 1993), and together they form a group called the Opisthokonts (Cavalier-Smith and Chao 1995; Cavalier-Smith et al. 1996; and Patterson 1999).  This relationship has been confirmed also by supergroup analyses (Baldauf 2003a and Keeling 2004) which suggest a sister group relationship between the Opisthokonts and the Amoebozoa forming a larger group called the Unikonta.


FIGURE 5

 

THE ANIMAL KINGDOM

Hz = Holozoa

Fz = Filozoa

An = Animalia

Mz = Metazoa

Em = Eumetazoa

Bi = Bilateria

Du = Deuterostomata

Pr = Protostomata

Ec = Ecdysozoa

Sp = Spiralia

FIGURE 4.  The kingdom Animalia and its basal sister-groups.  The topology is a consensus of Salchian-Tabrizi et al. (2008), Edgecombe et al. (2011), Nosenko et al. (2013), Zhang et al. (2013), and Pisani et al. (2015).  This figure follows the Porifera-Sister hypothesis (see Figure 4A).  The animal kingdom is contained within the open box.  Taxa in the colored box form a paraphyletic diploblastic group that we call Transitional Eumetazoa or Diploblastea.

 

 
Holozoa: Animalia + Basal Sister Groups

Holozoa (Lang et al. 2002) includes Animalia plus two basal sister groups: Ichthyosporea (Cavalier-Smith 1998) and Filasterea (Cavalier-Smith 2008) (see the consensus topology in Figure 3A-D and Figure 4).  Both groups were recognized to emerge near the separation of the fungus and animal lines (Shalchian-Tabrizi et al. 2008).

Ichthyosporea is a group of unicellular taxa, many of which are intracellular animal parasites.  Ragan et al. (1996) identified them as a group that emerges near the root of the fungus-animal tree and called them the DRIPs clade (an acronym that incorporated the taxa identified in the group: Dermocystidium, Rosette agent, Ichthyophonus, and Psorospermium).  Cavalier-Smith (1998) defined them as a class, which was later expanded and renamed Mesomycetozoea (meaning between animals and fungi) by Mendoza et al. (2002), who claim that since the group contains many species that are not fish parasites, the former name was misleading.  The intermediate position of this group is supported by the occurrence of chitin in the spore walls.  We have retained the former name due to the rules of priority.

Members of this group invade host cells and grow asexually ultimately forming walled uninucleate spores.  Within the same host, the released spores can infect other cells or be released into the environment where some species form uniflagellate zoospores.  Others develop amoeboid cells on release in the environment.  They might be adventitious parasites that generally live a saprotrophic existence.  Rosette agent (Sphaerothecum destruens) is particularly destructive of salmonid fish in which infective zoospores are spread from fish to fish through urine and other fluids (Arkush et al. 2003).  At least one (Rhinosporidium seeberi) infects humans, other mammals, and some birds causing rhinosporidiosis, which in humans forms growths and lesions of the mucosa (mainly mouth and nasal passages) that are filled with spores.  These seem to be adventitious infections by cells that naturally occur in ponded water.

Filasterea (meaning filament star) is made up of free-living unicellular, uninucleate marine protists (Shalchian-Tabrizi et al. 2008).  They have axopod-like tentacles that radiate around the spherical cell (see Figure 6; Suga et al. 2013).  The tentacles are supported internally by microtubules in the same way that rods of choanocytes which make up the filtering basket of choanocytes are constructed.  The genomic study by Suga et al. (2013) uncovered sets of proteins involved in cell adhesion and regulation typical of animals.


FIGURE 6

Choanozoa: The Unicellular Animals

The choanoflagellates are unicellular or colonial organisms that are identical to sponge choanocytes in structure.  This relationship is more than superficial in that it has been confirmed by molecular evidence (Wainright et al. 1993; Cavalier-Smith et al. 1996; Carr et al. 2008; King et al. 2008).  Thus, the case for choanoflagellates as animals seems quite secure (Sorensen et al. 2000; Eernisse and Peterson 2004) .  Indeed, Brusca and Brusca (2003), Nielsen (2001), and Tudge (2000) all indicate that the choanoflagellates are (at the very least) sister groups to the animal kingdom.  If the choanozoans are animals, then the Animal Kingdom grades from unicellular (Choanozoa) to multicellular (Metazoa) levels of structure.

 

Metazoa (Mz, Figures 4 and 5): The Multicellular Animals

The Metazoa have cells organized into tissues and develop with an abbreviated life history (with a few derived exceptions) in which gonads produce gametes (eggs and sperm), the only haploid cells.   Nevertheless, some go through elaborate life cycles in which the individual may pass through a series of larval stages, some of which do not resemble the adult.  According to Adoutte et al. (2000), Conway Morris (1993), Nielsen (2001), Raff (2001), Anderson (2001a), Brusca and Brusca (2003), and Tudge (2000), the Metazoa has three somewhat unequal clades which we treat as grades that are defined according to their fundamental levels of cellular construction: the Parazoa (tissue grade), the Diploblastic Animals (animals with organs and two cell layers), and the Bilateria (Protostomata and Deuterostomata; triploblastic level of construction).  

 

Parazoa: The Tissue-Grade Animals

Parazoa includes the sponges (Porifera), animals are asymmetrical as mature adults and develop through simple life histories.  Sponges can show a remarkable degree of cellular independence and survive and reassemble after separation of the cells (Huxley 1911).  Their construction as tissues of several cell-types, one of which is the choanocyte, makes them the simplest of the metazoa and connects them with the choanozoans.  Nielsen (2008) suggested that the higher-level complexities in the animal kingdom developed from the structure of a larval sponge that became sexually mature.  However, Adl et al. (2005) in an attempt to classify the Eukaryotes based on cladistic rules, separate Porifera together with Placozoa (see Diploblastic Animals) and Mesozoa (see Spiralia in the Bilateria) and elevate all of them to the same rank.  Such a change goes against a long tradition of taxonomy and would require much more support to convince us at this point.  Furthermore, we are very skeptical about the separate or primitive natures of the the Mesozoa.  Indeed, the groups within the Mesozoa likely only bear superficial resemblance and have become secondarily simplified from a higher level of organization. Mann (2010) also suggests that the sponges are not basal, but became secondarily simplified from animals with more complex forms.

 

Eumetazoa (Em, Figures 4 and 5): Animals with Defined Organs and Symmetry

Eumetazoa (Buetschli 1910) includes all animals with tissues organized into organs and organ systems, which include reproductive, muscular, and nervous systems. Furthermore, the organ-level animals tend to have determinate growth and develop along the prescribed lines of symmetry.  The cladistic presentation by Adl et al. (2005) concludes, among other things, that this is the base of the Animal Clade and that Parazoa and Choanozoa are sister groups to the animals.  Edgecombe et al. (2011) are cautious about these groups and have them emerge as stem lines forming a large polytomy.

 

Diploblastea (Tr, Figure 4): Transitional Animals

This is an artificial paraphyletic grouping of animal taxa that share the character of diploblasty, (a body made of two cell layers: ectoderm and endoderm).  Endoderm is the layer that lines the gut while the ectoderm is the cellular layer on the outside of the animal.  These layers also have developmental derivatives like the gonads.  Cnidarians (jellyfish, corals, and hydrozoans) and crenophores (comb jellies) have been interpreted as having radial symmetry and formerly joined in a taxon called Radiata.  They do superficially resemble jellyfish and even have a gut with a single opening.  Indeed, Nielsen (2001), Philippe et al. (2005) and Telford (2015) associate the Cnidaria and Ctenophora into a monophyletic group, sometimes called Coelenterata (see Figure 4D).  Halanych et al. (2004) support this view by asserting that both phyla have mesoderm.  If so, they also are triploblastic taxa.  

A remarkable and fairly old hypothesis (Weil 1938, cited in Lom 1990) places the traditional “sporozoan” protozoa called the myxosporozoans (here called the Myxozoa) into the metazoans.  Weil suggested that the myxozoans evolved from free-living cnidarians and became extremely simplified as intracellular parasites (as have the narcomedusae, a group of parasitic cnidarians).  Indeed, the capsules of the myxosporidians bear a striking structural resemblance to the nematocysts of the cnidarians.  This view has slowly gained acceptance (e.g. Lom 1990; Smothers et al. 1994; and Foox and Siddall 2015).  Smothers et al. (1994) confirm the structural association with molecular evidence that the myxosporidians are metazoans.  Genomic evidence (Chang et al. 2015) places Myxozoa firmly within the Hydrozoa of the Cnidaria.

Placozoa (Trichoplax is the only identified genus), is a phylum which may represent an early metazoan body plan that appears to be a free-living gastrula with a fully open blastopore such that the endoderm is in contact with the substrate and the ectoderm is on the dorsum.  Schierwater et al. (2008) consider them to be the appropriate model organism to study the origin of the Metazoa and interpret the molecular and morphological evidence to suggest that the placozoans are sisters to the other diploblastic organisms (cnidarians and ctenophores) while the triploblastic bilaterians form a sister group to the diploblastic taxa (Schierwater et al. 2009a & 2009b).  

The ctenophores or comb jellies are diploblastic animals with nervous and muscular systems (Jekely et al. 2015). Despite that, Halanych (2015) argues that the ctenophores are older than the sponges, and phylogenomic analyses (e.g. Dunn et al. 2008; Hejnol et al. 2009; and Ryan et al. 2013) tend to place them at the base of the metazoans.  The basal position of the ctenophores has become highly contested.  Arguing from morphology and development (e.g. Telford et al. 2015) and genomic evidence (e.g. Pisani et al. 2015), sponges are the basal metazoans.  Pisani et al. (2015) used the former genomic data sets and performed cladistic analyses using more biologically relevant evolutionary models and more appropriate outgroups to demonstrate basal nature of the sponges.  The multiple theories regarding the positions of Porifera and Ctenophora are illustrated in Figure 4 A-D.

 

Bilateria (Bi, Figures 4 and 5): The Triploblastic Animals

The bilaterians are, as the name implies, bilaterally symmetrical.  As they develop from the gastrula, a third cell layer, the mesoderm, develops between the ectoderm and endoderm.  Derivatives of the mesoderm provide much of the complexity seen in triploblastic animals.  For example, among vertebrates, the mesoderm develops into most of the bone, muscle, mesentaries, blood, etc.  Most of the vertebrate nervous system, as well as certain bones and other structures develop from the ectoderm.

The origin of the bilaterians is somewhat controversial, but the growing body of molecular and developmental evidence suggests that the acoel flatworms are not members of the Platyhelminthes (e.g. Baguña and Riutort 2004; Dunn et al. 2008; Egger et al. 2009; Hejnol et al. 2009).  Furthermore, they are basal to bilaterians (Hejnol et al. 2008; Ruiz-Trillo et al. 1999).  Boero et al. (2007) suggest that the cnidarians gave rise to the bilaterians by paedomorphogenesis in which the bilaterally-symmetrical planula cnidarian larva, which bears a striking resemblance to the acoel flatworms, became sexually mature. The acoels are sisters to the rest of the bilaterians, collectively referred to as the Nephrozoa because they all share an ancestor that produced nephridia (Edgecombe et al. 2011).

Within the subkingdom Bilateria, we have kept the Protostome - Deuterostome dichotomy (these are approximately at the superphylum level).  The two groups differ fundamentally in how the gastrula develops.  The blastopore of a deuterostome (Du, Figures 4 and 5) becomes the anus while the blastopore of a protostome (Pr, Figures 4 and 5) becomes the mouth.  Also, the protostomes develop by spiral cleavage and form a schizocoelic coelom.  The deuterostomes tend to develop by radial cleavage and form an endocoelic coelom.  

Dunn et al. (2008) and Edgecombe et al. (2011) have standardized the bilaterians and terminologies for taxa above the level of phylum.  The Deuterostomes separate into two major clades: Chordata (including vertebrates, tunicates, and cephalochordates) and the Ambulacraria (echinoderms and hemichordates.  The topology of the protostomes is much more complex.  

Traditional taxonomic systems divide the bilaterian animals according to grades of body structure, especially within the Protostomata which is separated according to type of body cavity (i.e. the Acoelomates, the Pseudocoelomates, and the Eucoelomates).  Such a view can be seen in many pre-cladistic texts (e.g. Storer and Usinger, 1965) and even persist in more recent texts like Margulis and Schwartz (1998) and Nielsen (1995).  In a systematic sense, we have abandoned the old view of dividing the protostomes according to type of body cavity.  Cladistic analyses based on morphology and development (e.g. Brusca and Brusca, 2003; Nielsen, 2001) have led to the integration of acoelomate and pseudocoelomate taxa into the bilaterian clades.  

The deuterostomes and most of the protostomes are eucoelomate in structure, but some groups do not show clear developmental or morphological affinities (i.e. the chaetognaths and lophophorates).  Brusca and Brusca (2003), Nielsen (2001), and Margulis and Schwartz (1998) interpret the "lophophorates" as deuterostomes (although Nielsen says that the "bryozoans" are not related to the lophophorates and occupy a clade with the rotifers and gnathostomulids within the protostomes).  Furthermore, Nielsen (2001) and Brusca and Brusca (2003) placed the Annelida as a sister group to the panarthropods.  Other than the question of the position of the "bryozoan" phyla, they differ as to the position of the Chaetognatha.  Nielsen (2001) interprets chaetognath development and adult structure as being protostomal while Brusca and Brusca (2003) interpret the Chaetognatha as deuterostomal.  Halanych and Passamaneck (2001), through molecular analysis, confirmed that the chaetognaths are protostomes with deuterostomic features (e.g. they produce a secondary mouth, they have coelomic pouches that are more like those of deuterostomes).  Philippe et al. (2007) resolved the problem by placing the chaetognaths at the base of the Protostome clade so that they retain many of the deuterostome features.

Molecular phylogenetic trees suggest a very different organization of the bilaterians than those generated by morphology and development.  Giribet (2008) and Edgecombe et al. (2011) summarize current results of molecular phylogenetics in which they place the lophophorates in the protostomes and separate the protostomes into two fundamentally different lines: Ecdysozoa and Lophotrochozoa (here called the Spiralia).  Ecdysozoa grow by casting the external cuticle/exoskeleton and have similar introvert-like feeding organs (synapomorphies in this system).  Spiralia includes animals with lophophores or trochophore larvae as synapomorphies.  Besides the relationship implied by the molecular trees, some of the protostomes, particularly the Platyzoa (a subgroup of the Spiralia) appear to have no structural synapomorphies.

The topology of bilaterians in Figure 5 reflects current interpretations of developmental, anatomical, and molecular studies (summarized by Shalchian-Tabrizi et al. 2008; Telford et al. 2015; Pisani et al. 2015).  Acoelomorpha is sister to the Protostomes + Deuterostomes.  Within the protostomes, the differentiation between Ecdysozoa and Spiralia (Lophotrochozoa) is now generally accepted.  

 

MAJOR GROUPS OF THE ANIMAL KINGDOM

 

 

CHOANOZOA (Cavalier-Smith 1993)
METAZOA (Haeckel 1866)

 

 

PARAZOA (Sollas 1884)

EUMETAZOA (Buetschli 1910)

 

DIPLOBLASTEA*

BILATERIA (Hatscheck 1888)

 

ACOELOMORPHA (Ehlers 1986)

DEUTEROSTOMATA (MacAlister 1876)

PROTOSTOMATA (MacAlister 1879)

 

ECDYSOZOA (Aguinaldo et al. 1997)

SPIRALIA (Giribet 2002) [=LOPHOTROCHOZOA (Halanych et al. 1995)]

 

 
* Diploblastea is a term that we created to include the transitional Metazoa, all of which contain two cell layers but have little else in common.  

LITERATURE CITED

Adl, S. M., A. G. B. Simpson, M. A. Farmer, R. A. Andersen, O. R. Anderson, J. R. Barta, S. S. Bowser, G. Brugerolle, R. A. Fensome, S. Fredericq, T. Y. James, S. Karpov, P. Kugrens, J. Krug, C. E. Lane, L. A. Lewis, J. Lodge, D. H. Lynn, D. G. Mann, R. M. McCourt, L. Mendoza, O. Moestrup, S. E. Mozley-Standridge, T. A. Nerad, C. A. Shearer, A. V. Smirnov, F. W. Spiegel, and M. F. J. R. Taylor. 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. Journal of Eukaryotic Microbiology. 52(5):399-451. 

Adoutte, A., G. Balavoine, N. Lartillot, O. Lespinet, B. Prud'homme, and R. de Rosa. 2000. The new animal phylogeny: reliability and implications. Proceedings of the National Academy of Sciences. U.S.A. 97:4453-4456. 

Anderson, D. T. 2001a. The Invertebrate Phyla. In: Anderson, D.T., ed. Invertebrate Zoology. Oxford University Press. Oxford, UK. pp. 1-9.

Arkush, K. D., L. Mendoza, M. A. Adkison, and R. P. Hedrick. 2003. Observations on the life stages of Sphaerothecum destruens n.g., n. sp., a mesomycetozoan fish pathogen formally referred to as the rosette agent. The Journal of Eukaryotic Microbiology. 50(6): 430-438.

Baguña, J. and M. Riutort. 2004. The dawn of bilaterian animals: the case of acoelomorph flatworms. BioEssays. 26: 1046-1057.

Baldauf, S. L. 2003. The deep roots of eukaryotes. Science. 300 (5626): 1701-1703. 

Blackstone, N. W. 2009. A new look at some old animals. PLoS Biol. 7(1): e1000007. doi:10.1371/journal.pbio.1000007.

Boero, F., B. Schierwater, and S. Piraino. 2007. Cnidarian milestones in metazoan evolution. Integrative and Comparative Biology. 47(5): 693-700.

Brusca, R. C. and G. J. Brusca. 2003. Invertebrates. 2nd Edition. Sinauer Associates. Sunderland, MA.

Bütschli, O. 1910. Einleitung, vergleichende Anatomie der Protozoen, Integument und Skelet der Metazoen...: Einleitung, vergleichende Anatomie der Protozoen, Integument und Skelet der Metazoen. Springer Verlag. Berlin.

Carr, M., B. S. C. Leadbeater, R. Hassan, M. Nelson, and S. L. Baldauf. 2008. Molecular phylogeny of choanoflagellates, the sister group to Metazoa. Proceedings of the National Academy of Sciences. U.S.A. 105(43): 16641-16646.

Cavalier-Smith, T., M. T. E. P. Allsopp, E. E. Chao, N. Boury-Esnault, and J. Vacelet. 1996. Sponge phylogeny, animal monophyly, and the origin of the nervous system: 18S rRNA evidence. Canadian Journal of Zoology. 74:2031-2045.

Cavalier-Smith, T. and E. E. Chao. 1995. The opalozoan Apusomonas is related to the common ancestor of animals, fungi, and choanoflagellates. Proceedings of the Royal Society of London B. 261:1-6.

Chang, E. S., M. Neuhof, N. M. Rubenstein, A. Diamant, H. Philippe, D. Huchon, and P. Cartwright. 2015. Genomic insights into the evolutionary origin on Myxozoa within Cnidaria. Proceedings of the National Academy of Sciences (USA). 112(48): 14912-14917.

Chen, J-Y., D. J. Bottjer, P. Oliveri, S. Q. Dornbos, F. Gao, S. Ruffins, H. Chi, C-W Li, and E. H. Davidson. 2004. Small bilaterian fossils from 40 to 55 million years before the Cambrian. Science. 305: 218-222.

Conway Morris, S. 1993. The fossil record and the early evolution of the Metazoa. Nature. 361:219-225.

Di Lullo, G. A., S. M. Sweeney, J. Korkko, L. Ala-Kokko, and J. D. San Antonio. 2002. Mapping the ligand-binding sites and disease-associated mutations on the most abundant protein in the human, type I collagen. The Journal of Biological Chemistry. 277(6): 4223-4231. 

Dunn, C. W., A. Hejnol, D. Q. Matus, K. Pang, W. E. Browne, S. A. Smith, E. Seaver, G. W. Rouse, M. Obst, G. Edgecomb, M. V. Sorensen, S. H. D. Haddock, A. Schmidt-Rhaesa, A. Okusu, R. Mobjerg-Kristensen, W. C. Wheeler, M. Q. Martindale, and G. Giribet. 2008. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature. 452: 745-749.

Dzik, J. 2003. Anatomical information content in the ediacaran fossils and their possible zoological affinities. Integr. Comp. Biol. 43: 114-126.

Edgecombe, G. D., G. Giribet, C. W. Dunn, A. Hejnol, R. M. Kristensen, R. C. Neves, G. W. Rouse, K. Worsaae, and M. V. Sorensen. 2011. Higher-level metazoan relationships: recent progress and remaining questions. Organisms Diversity and Evolution.  DOI 10.1007/s13127-011-0044-4. [C]

Egger, B., D. Steinke, H. Tarui, K. de Mulder, D. Arendt, G. Borgonie, N. Funayama, R. Gschwentner, V. Hartenstein, B. Hobmayer, M. Hooge, M. Hrouda, S. Ishida, C. Kobayshi, G. Kuales, O. Nishimura, D. Pfister, R. Rieger, W. Salvenmoser, J. Smith, U. Technau, S. Tyler, K. Agata, W. Salzburger, and P. Ladurner. 2009. To be or not to be a flatworm: The acoel controversy. PLoS ONE. 4(5): e5502. doi:10.1371/journal.pone.0005502.

Ehlers, U. 1986. Comments on a phylogenetic system of the Platyhelminthes. Hydrobiologia. 132: 1-12.

Eschscholtz, J. F. 1829-1833. Zoologischer Atlas. Vol. 1-5. Reimer. Berlin.

Gellon, G. and W. McGinnis. 1998. Shaping animal body plans in development and evolution by modulation of Hox expression patterns. BioEssays. 20(2): 116-125.

Giribet, G. 2002. Current advances in the phylogenetic reconstruction of metazoan evolution.  A new paradigm for the Cambrian explosion? Mol. Phylogenet. Evol. 24: 345-357.

Giribet, G., D. L. Distel, M. Polz, W. Sterrer and W. Wheeler. 2000. Triploblastic relationships with emphasis on the acoelomates and the position of Gnathostomulida, Cycliophora, Plathelminthes, and Chaetognatha: a combined approach of 18S rDNA sequences and morphology. Systematic Biology. 49:539-562.

Haeckel, E. 1866. Generelle Morphologie der Organismen. Reimer. Berlin.

Halanych, K. M. 2015. The ctenophore lineage is older than sponges? That cannot be right! Or can it? The Journal of Experimental Biology. 218: 592-597.

Hatschek, B. 1888. Lehrbuch der Zoologie, 1. Lieferung. Gustav Fischer. Jena. pp. 1—144. 

Hejnol, A. and M. Q. Martindale. 2008. Acoel development supports a simple planula-like urbilaterian. Philosophical Transactions of the Royal Society. B. 363: 1493-1501.

Hejnol, A., M. Obst, A. Stamatakis, M. Ott, G. W. Rouse, G. D. Edgecombe, P. Martinez, J. Baguña, X. Bailly, U. Jondelius, M. Wiens, W. E. G. Müller, E. Seaver, W. C. Wheeler, M. Q. Martindale, G. Giribet, and C. W. Dunn. 2009. Assessing the root of bilaterian animals with scalable phylogenomic methods. Proceedings of the Royal Society. B. 276: 4261-4270.

Hofmann, H. J., G. M. Narbonne, and J. D. Aitken. 1990. Ediacaran remains from intertillite beds in northwestern Canada. Geology. 18: 1199-1202.

Huxley, J. S. 1911. Some phenomena of regeneration in Sycon; with a note on the structure of its collar cells. Philosophical Transactions of the Royal Society of London B. 202: 165-189.

Jekely, G., J. Paps, and C. Nielsen. 2015. The phylogenetic position of ctenophores and origin(s) of nervous systems. EvoDevo. 6(1): http://evodevojournal.com/content/6/1/1

Keeling P. J. 2004 The diversity and evolutionary history of plastids and their hosts. American Journal of Botany. 91(10): 1481-1493. 

King, N., M. J. Westbrook, S. L. Young, A. Kuo, M. Abedin, J. Chapman, S. Fairclough, U. Hellsten, Y. Isogai, I. Letunic, M. Marr, D. Pincus, N. Putnam, A. Rokas, K. J. Wright, R. Zuzow, W. Dirls, M. Good, D. Goodstein, D. Lemons, W. Li, J. B. Lyons, A. Morris, S. Nichols, D. J. Richter, A. Salamov, JGI Sequencing, P. Bork, W. A. Lim, G. Manning, W. T. Miller, W. McGinnis, H. Shapiro, R. Tijan, I. V. Grigoriev, and D. Rokhsar. 2008. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature. 451: 783-788.

Linnaeus, C. 1758. Systema Naturae per Regna Tria Naturae. Regnum Animale. Laurentii Salvii. Stockholm.

Lom, J. 1990. Myxozoa. In: Margulis, L., J. O. Corliss, M. Melkonian, and D. J. Chapman, eds. 1990. Handbook of the Protoctista; the structure, cultivation, habits and life histories of the eukaryotic microorganisms and their descendants exclusive of animals, plants and fungi. Jones and Bartlett Publishers. Boston. pp. 36-52.

Margulis, L. and K. Schwartz. 1998. Five kingdoms, an illustrated guide to the phyla of life on earth. 3rd Edition. W. H. Freeman and Company.  New York. 

Narbonne, G. M. 2005. The Ediacara biota: Neoproterozoic origin of animals and their ecosystems. Annu. Rev. Earth Planet. Sci. 33: 421-442.

Nielsen, C. 1995. Animal Evolution: Interrelationships of the Living Phyla. 1st Edition. Oxford University Press. Oxford.

Nielsen, C. 2001. Animal Evolution: Interrelationships of the Living Phyla. 2nd Edition. Oxford University Press. Oxford.

Nielsen, C. 2008. Six major steps in animal evolution: Are we derived sponge larvae? Evolution and Development. 10(2): 241-257.

Nosenko, T., F. Schreiber, M. Adamska, M. Adamski, M. Eitel, J. Hammel, M. Maldonado, W. E. G. Muller, M. Nickel, B. Schierwater, J. Vacelet, M. Wiens, and G. Worheide. 2013. Deep metazoan phylogeny: When different genes tell different stories. Molecular Phylogenetics and Evolution. 67: 223-233.

Patterson, D. J. 1999. The diversity of eukaryotes. American Naturalist. 154 (Suppl.): S96–S124. 

Pearson, J. C., D. Lemons, and W. McGinnis. 2005. Modulating Hox gene functions during animal body patterning. Nature Rev. Genet. 6: 893-904.

Pires-daSilva, A. and R. J. Sommer. 2003. The evolution of signaling pathways in animal development. Nature Reviews Genetics. 4: 39-49.

Pisani, D., W. Pett, M. Dohrmann, R. Feuda, O. Rota-Stabelli, H. Philippe, N. Lartillot, and G. Wörheide. 2015. Genomic data do not support comb jellies as the sister group to all other animals. Proceedings of the National Academy of Sciences (USA). 112(50): 15402-15407.

Pratihar, S., R. P. Nath, and J. K. Kundu. 2010. Hox genes and its role in animal development. International Journal of Science and Nature. 1(2): 101-103. 

Raff, R. A. 2001. Metazoan phylogeny. In: Anderson, D.T., ed. Invertebrate Zoology. Oxford University Press. Oxford, UK . pp. 424-446.

Rasmussen, B., S. Bengtson, I. R. Fletcher, and N. J. McNaughton. 2002. Discoidal impressions and trace-like fossils more than 1200 million years old. Science. 296: 1112-1115. [L, C]

Ruiz-Trillo, I., M. Ruitort, D. T. J. Littlewood. E. A. Herniou, and J. Baguña. 1999. Acoel flatworms: earliest extant bilaterian metazoans, not members of Platyhelminthes. Science. 283. 1919-1923.

Ryan, J. F., K. Pang, C. E. Schnitzler, A-D. Nguyen, R. T. Moreland, D. K. Simmons, B. J. Koch, W. R. Francis, P. Havlak, NISC Comparative Sequencing Program, S. A. Smith, N. H. Putnam, S. H. D. Haddock, C. W. Dunn, T. G. Wolfsberg, J. C. Mullikin, M. Q. Martindale, and A. D. Baxevanis. 2013. The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science. 342: DOI: 10.1126/science:1242592

Schierwater, B., M. Eitel, W. Jakob, H-J. Osigus, H. Hadrys, S. L. Delaporta, S-O. Kolokotronis, and R. DeSalle. 2009a. Concatenated analysis sheds light on early metazoan evolution and fuels a modern "Urmetazoon" hypothesis. PLoS Biol. 7(1): e1000020. doi:10.1371/journal.pbio.1000020.

Schierwater, B. S-O. Kolokotronis, M. Eitel, and R. DeSalle. 2009b. The diploblast-bilateria sister hypothesis. Communicative and Integrative Biology. 2(5): 1-3.

Schierwater, B., D. de Jong, R. DeSalle. 2009c. Placozoa and the evolution of Metazoa and intrasomatic cell differentiation.  International Journal of Biochemistry and Cell Biology. 4: 370-379.

Seilacher, A., P. K. Bose, and F. Pflüger. 1998. Triploblastic animals more than 1 billion years ago: trace fossil evidence from India. Science. 282: 80-83.

Simion, P., H. Philippe, D. Baurain, M. Jagar, D. J. Richter, A. D. Franco, B. Roure, N. Satoh, E. Queinnec, A. Ereskovsky, P. Lapebie, E. Corre, F. Delsuc, N. King, G. Worheide, and M. Manuel. 2017. A large and consistent phylogenomic dataset supports sponges as the sister group to all other animals. Current Biology. 27: 958-967.

Smothers, J. F., C. D. von Dohlen, L. H. Smith, Jr., and R. D. Spall. 1994. Molecular evidence that the myxozoan protists are metazoans. Science. 265:1719-1721. 

Srivastava, M. O. Simakov, J. Chapman, B. Fahey, M. E. A. Gauthier, T. Mitros, G. S. Richards, C. Conaco, M. Dacre, U. Hellsten, C. Larroux, N. H. Putnam, M. Stanke, M. Adamska, A. Darling, S. M. Degnan, T. H. Oakley, D. C. Plachetzki, Y. Zai, M. Adamski, A. Calcino, S. F. Cummins, D. M. Goodstein, C. Harris, D. J. Jackson, S. P. Leys, S. Shu, B. J. Woodcroft, M. Vervoort, K. S. Kosik, G. Manning, B. M. Degnan, and D. S. Rokhsar. 2010. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature. 466: 720-727. 

Storer, T. I. and R. L. Usinger. 1965. General Zoology. 4th Edition. McGraw-Hill Book Company. New York.

Suga, H., Z. Chen, A. de Mendoza, A. Sebe-Pedros, M. W. Brown, E. Kramer, M. Carr, P. Kerner, M. Vervoort, N. Sanchez-Pons, G. Torruella, R. Derelle, G. Manning, B. F. Lang, C. Russ, B. J. Haas, A. J. Roger, C. Nusbaum, and I. Ruiz-Trillo. 2013. The Capsaspora genome reveals a complex unicellular prehistory of animals.  Nature Communications. DOI: 10.1038/ncomms3325

Telford, M. J., G. E. Budd, and H. Philippe. 2015. Phylogenomic insights into animal evolution. Current Biology. 25: R876-R887.

Tudge, C. 2000. The Variety of Life, A Survey and a Celebration of All the Creatures That Have Ever Lived. Oxford University Press. New York. 

Valentine, J. W. 2004. The Origin of Phyla. University of Chicago Press. Chicago.  614 pp.

Wainright, P. O., G. Hinkle, M. L. Sogin, and S. K. Stickel. 1993. Monophyletic origins of the Metazoa: an evolutionary link with Fungi. Science. 260: 340-342. 

Weill, R. 1938. L'interpretation des Cnidosporides et la valeur taxinomique de leur cnidome. Leur cycle compare a la phase larvaire des Narcomeduses Cuninides. Travaux de la Station Zoologique de Wimereux. 13:727-744.

Wolfe, S. L. 1993. Molecular and Cellular Biology. Wadsworth Publishing Co. Belmont, California.

 

By Jack R. Holt & Carlos A. Iudica.  Last revised: 05/14/2018