II. Testing the Validity of Traditional Morphological Characters by Seeing Whether They Are Consistent With Molecular Trees

To be consistent with a given phylogenetic tree, a character must map onto the tree with few changes in character state.

For example, bilateral symmetry is consistent with the traditional morphology-based cladogram for the Big Nine phyla (those with more than 5,000 named species), since it can be mapped onto the cladogram with only one change in character state.

  • The basic phylogenetic outline shown in Figure 14 has been standard since the publication of The Invertebrates by Hyman. Hyman's original tree had a "primitive acoel flatworm" as the base of the Bilateria, with Platyhelminthes and Nematoda in the Protostomia. Many authors now make the latter two phyla separate branches basal to the other Bilateria.

Figure 14. The traditional morphology-based phylogeny of the major animal phyla, based on the "hypothetical diagram" by Hyman (1940, vol. 1, p. 38). Bilateral symmetry is consistent with this phylogeny because it requires only one change in character state to account for its distribution among the phyla.

Segmentation, however, is less consistent with traditional morphology based phylogenetic trees, because it requires at least two changes in character state: one for annelids and arthropods and one for chordates (Fig. 15).

Figure 15. Traditional phylogeny of the Big Nine showing that segmentation is less consistent, because it requires at least two changes in character state to account for its distribution.

Lack of consistency implies that either the character is not synapomorphic (homologous), or the phylogenetic tree is incorrect.

  • Similar characters can evolve convergently more than once, as segmentation apparently did in Arthropoda and Chordata. Convergent evolution results in analogous characters that are not indicative of phylogeny. In the language of cladistics, such an evolutionary convergent character is a homoplasy. A homoplasy is not a synapomorphy (shared, derived, homologous character), which is the only kind of character that is useful in cladistics.
  • If analysis indicates that an incharacter is nevertheless a synapomorphy, the tree is less likely to be correct, because it does not provide a parsimonious explanation for the evolution of the character. A different tree should be tried.
  • These same principles apply to molecular characters as well as to morphological characters.

A character that is consistent with both a morphological and a molecular phylogeny is more likely to be phylogenetically informative.

  • A morphological character is not likely to be useful if it is not consistent with either a tree based on other morphological characters or one based on molecules.

Morphological characters have not led to a consensus phylogeny.

  • The use of different characters and methods of analysis have also resulted in numerous dif-ferent proposed phylogenies (Jenner and Schram 1999). For example, Willmer (1990), like Hyman, used a noncladistic approach in which one or a few striking characters, such as the fate of the blastopore, were heavily weighted. Nielsen (1995) and other cladists give equal weight to a larger number of characters. Pechenik (2000, pp. 18-20) provides a sampling of different trees, and Eernisse et al. (1992) show a dozen variations gleaned from textbooks.
  • Hyman's (1940, vol. 1, pp. 37-38) phylogenetic tree of Animalia has a trunk from which Pro-tozoa, Mesozoa, Porifera, and Radiata sprout before giving rise to the Bilateria, as outlined in Figures 14 and 15. She recognized 22 phyla (listed below in bold face with some spellings changed) and arranged them in order of complexity:

    Subkingdom Protozoa
          Protozoa
    Subkingdom Metazoa
          Branch A. Mesozoa
               Mesozoa
          Branch B. Parazoa
              
    Porifera
          Branch C. Eumet
    azoa
               Grade I. Radiata
                   
    Cnidaria
                    Ctenophora

               Grade II. Bilateria
                    A. Acoelomata
                         Platyhelminthes
                         Nemertea

                    B. Pseudocoelomata
                         Aschelminthes (Rotifera, Gastrotricha, Kinorhyncha, Nematoda,                          Nematomorpha, Acanthocephala)
                         Entoprocta
                    C. Eucoelomata
                         1. Schizocoela
                             Ectoprocta
                             Phoronida
                             Brachiopoda
                             Mollusca
                             Sipuncula
                             Priapulida
                             Echiurida
                             Annelida
                             Arthropoda

                         2. Enterocoela
                             Chaetognatha
                             Echinodermata
                             Hemichordata
                             Chordata

  • Willmer (1990, p. 361) presented a morphology-based tree that she characterized as "undoubtedly wrong" but a useful summary of her conclusions from the morphological evidence. Her summary tree could be shown in a cladogram of the Big Nine phyla that differs from Figures 14 and 15 mainly in that each of four lineages for Nematoda, Mollusca, Annelida, and Echinodermata plus Chordata diverges from a flat-worm-like ancestor. In addition, she divided Arthropoda into three phyla, with only Uniramia allied to Annelida. Her tree for the 36 phyla that she recognized can be summarized as follows:

    Descendants of "planulas"
         Porifera
         Placozoa
         Mesozoa
         Cnidaria
         Ctenophora

         "Acoelomate Platyhelminthes" (polyphyletic)
    Lines of descent from "acoelomate Platyhelminthes"
         Gastrotricha, Nematoda, Nematomorpha
         Rotifera, Acanthocephala
         Entoprocta
         Nemertea
         Mollusca
         Sipuncula
         Pentastomida
         Tardigrada
         Echiura, Pogonophora, Onychophora, Annelida, Uniramia
         Pycnogonida
         Chelicerata
         Crustacea
         Loricifera
         Kinorhyncha
         Priapulida
         Ectoprocta, Phoronida, Brachiopoda
         Hemichordata, Echinodermata, Chordata
         Chaetognatha
         Gnathostomulida

  • A morphology-based cladogram for the Big Nine phyla derived from Nielsen's (1995, p. 6) summary cladogram is similar to Figures 14 and 15 except that Nematoda is in a separate line from the one in which Platyhelminthes then Mollusca, Annelida, and Arthropoda branch. His cladogram showing the 31 phyla he recognized (in boldface) is summarized in the following slightly simplified indented list:

    Animalia
          Porifera
              
    Placozoa
              
    Eumetazoa
                    Cnidaria
                   
    Bilateria
                         Protostomia
                              Aschelminthes
                                   Rotifera, Acanthocephala
                                   Chaetognatha
                                   Cycloneuralia
                                        Gastrotricha
                                        Nematoda, Nematomorpha
                                        Priapulida
                                        Kinorhyncha
                                        Loricifera

                              Spiralia
                                   Parenchymia
                                        Platyhelminthes
                                        Nemertea

                                   Bryozoa
                                        Entoprocta
                                        Ectoprocta

                                   Teloblastica
                                        Sipuncula
                                        Mollusca
                                        Annelida
                                        Onychophora
                                        Arthropoda
                                        Tardigrada

                         Protornaeozoa
                              Ctenophora
                              Deuterostomia
                                   Phoronida, Brachiopoda
                                   Pterobranchia, Echinodermata

                                   Cyrtotreta
                                        Enteropneusta
                                        Chordata
                                              Urochordata
                                              Cephalochordata
                                              Vertebrata

The following morphological characters traditionally used in phylogenetics are also consistent with the widely accepted molecular phylogenetic tree of the Big Nine Phyla: bilateral symmetry and triploblasty, deuterostomy, and spiral cleavage pattern.

  • Figure 16 summarizes the currently accepted molecular phylogeny for the Big Nine phyla. It differs from the traditional phylogeny in Figures 14 and 15 mainly in dividing the protosomes into two distinct clades, with one including Platyhelminthes, Mollusca, and Annelida, and the other including Nematoda and Arthropoda.

Figure 16. Bilateral symmetry and triploblasty, deuterostomy, and spiral cleavage pattern are consistent with the molecular phylogenetic tree of the Big Nine Phyla.

Bilateral symmetry and triploblasty are also consistent with a molecular phylogenetic tree that includes all animal phyla.

  • HISTORY: In the first volume of The Invertebrates (1940, pp. 32-39), Hyman placed the Bilateria in a grade above the Radiata (Cnidaria and Ctenophora), which were in turn above the Porifera. She eschewed the term "diploblast," noting that sponges do not develop from two germ layers and that all except Hydrozoa have a middle layer of cells that could be called tissue.
  • RECENT MORPHOLOGICAL STUDIES: Willmer (1990) rejected not only the dip-loblast/triploblast dichotomy, but also the Radiata/Bilateria distinction, noting that most sponges and placozoans are asymmetric, and many cnidarians and especially ctenophorans tend toward bilateral symmetry. Nevertheless, she (1990, p. 361) placed Porifera, Cnidaria, and other traditional "Radiata" or "Diploblasts" below a flatworm-like ancestor of the bilaterally symmetric animals. Nielsen (1995, p. 64) also concluded that bilateral symmetry is "a highly questionable synapomorphy of the bilaterians," but for different reasons he (p. 72) considered it "reasonable to regard the Bilateria as a monophyletic group and as the sister group of the Cnidaria." His Bilateria includes Ctenophora as the sister group of Deuterostomia (p. 307).
  • As shown in Figure 17 (next page), a tree based mainly on 18S rDNA supports the traditional view that "diploblasts" or "radiata" are basal to the bilateria.
  • This molecular phylogenetic tree is a composite of many separate studies, some of which will be discussed in Part III. It recognizes 30 phyla. Mesozoa are included within Platyhelminthes, and Echiurida and Pogonophora are included within Annelida. See Figure 1.B of Adoutte et al. (2000) and Figure 2 of Zrzavý et al. (1998) for somewhat different molecular phylogenetic trees of all phyla. It may prove convenient to print a copy of Figure 17 for reference in later discussion.
  • The Bilateria are also recovered as a monophyletic clade in molecular phylogenies based on 5S rDNA (Hori and Osawa 1987) and 28S rDNA (Christen et al. 1991).

Deuterostomy in Echinodermata, Hemichordata, and Chordata is also consistent in a molecular phylogenetic tree of all animal phyla.

  • HISTORY: Hyman (1951, vol. 2, p. 5) accepted the then-prevailing view that deuterostomes (Chaetognatha, Echinodermata, Hemichordata, and Chordata) were a heterologous assemblage of groups that were not closely related. She considered the lophophorates (Ectoprocta, Phoronida, and Brachiopoda) to be intermediate between protostomes and deuterostomes.
  • RECENT MORPHOLOGICAL STUDIES: Willmer (1990, p. 349) rejected the protostome/deuterostome dichotomy, but she agreed that Hemichordata, Echinodermata, and Chordata (branching in that order) represented a monophyletic lineage that did not include the lophophorates. Nielsen (1995, pp. 76-77) regarded the fate of the blastopore as an unreliable character, but using other characters, he (p. 62) divided the Bilateria into the two clades Protostomia and Protornaeozoa (Ctenophora plus Deuterostomia). His Deuterostomia clade included hemichordates, echinoderms, chordates, Phoronida, and Brachiopoda, but not Ectoprocta (p. 333).
  • If the problematic Chaetognatha are excluded, the molecular tree based on 18S rDNA (Fig. 17) suggests that the traditional deuterostomates are in fact monophyletic. Chaetognaths, as well as lophophorates, will be discussed in more detail later in Part III.

Figure 17. Summary tree from molecular phylogenetic studies of animal phyla. (There are no molecular data for Loricifera.)

The spiral-cleavage pattern is somewhat consistent with a molecular phylogenetic tree that includes all animal phyla.

  • HISTORY: Hyman recognized the importance of the cleavage pattern, but she gave more weight to the schizocoelous versus enterocoelous origin of the coelom. She appears not to have regarded "Spiralia" as a distinct group.
  • RECENT MORPHOLOGICAL STUDIES: Willmer (1990, pp. 128-129) cautiously recognized a "core group of spiralians… including certain polyclads, nemerteans, annelids, uniramian arthropods, pogonophorans, echiurans, sipunculans and molluscs." However, she (p. 268) regarded the molluscs as pseudocoelomates with little in common with other phyla. Nielsen (1995, p. 96) considered it best to treat the Spiralia as the sister clade of Aschelminthes within Protostomia. His Spiralia comprised Sipuncula, Mollusca, Annelida, Onychophora, Arthropoda, Tardigrada, Entoprocta, Platyhelminthes, and Nemertea.
  • Molecular phylogenetics (Fig. 17) supports the existence of a clade in which the spiral cleavage pattern may be plesiomorphic (primitive). However, this clade also includes lophophorates, which generally have radial cleavage. It also includes flatworms, which have spiral cleavage but are often not included with coelomate spiralians. It does not include onychophorans, tardigrades, or arthropods. These groups will be discussed in more detail in Part III.

The lophophore by itself is not consistent with the molecular phylogenetic tree, and it may not be a homology.

  • HISTORY: Hyman (1959, vol. 5, p. 229) defined the lophophore as "a tentaculated extension of the mesosome that embraces the mouth but not the anus and has a coelomic lumen." She considered it a homologous character uniting Ectoprocta, Phoronida, and Brachiopoda as lophophorates.
  • RECENT MORPHOLOGICAL STUDIES: Willmer (1990, p. 349) considered the lophophor-ates to be a "rather close-knit assemblage." Nielsen (1995, p. 183) found no synapomorphy uniting the ectoprocts with the phoronids and brachiopods. He dismissed the lophophore as nonsynapomorphic, because numerous other characters linked Ectoprocta to Spiralia and Phoronida and Brachiopoda to Deuterostomia.
  • Molecular studies (Fig. 17) place the "lophophorates" in the clade of protostomates that includes Platyhelminthes, Mollusca, and Annelida. The lophophorates do not appear to be monophyletic within that clade, however, because Phoronida and Brachiopoda may be more closely related to each other than to Ectoprocta.

The occurrence and type of body cavity (whether the animal is acoelomate, pseudocoelomate, or coelomate) is not consistent with the molecular phylogenetic tree and is not homologous.

  • HISTORY: Hyman (1940, vol. 1, p. 35), following Schimkevitch (1891), was primarily responsible for the distinction among acoelomates, pseudocoelomates, and coelomates. "Such a division," she wrote, "stands firmly on a realistic anatomical basis and eschews all theoretical vaporizings…." She dismissed the once-common view that acoelomates and pseudocoelomates originated from coelomates. This "Archecoelomate Theory" has been revived in recent times, but it is not widely accepted or even familiar among American zoologists. (See Willmer 1990, pp. 33-37 for discussion.) Support for it comes from the fact that the pseudocoel can form by loss of the peritoneum or part of the mesoderm enclosing a coelom, among other ways (Maggenti 1976). In addition, some nematodes, all leeches, and some other presump-tive coelomates and pseudocoelomates have secondarily become acoelomate, showing that a coelomate-to-pseudocoelomate or coelomate-to-acoelomate evolutionary sequence is at least conceivable. All of this casts doubt on the homology of the acoelomate and pseudocoelomate conditions.
  • RECENT MORPHOLOGICAL STUDIES: Willmer's (1990, p. 22-38) review of body cavities led her to the conclusion that "it may well be that--contrary to most of the simple invertebrate textbooks--the body cavities of animals are amongst the most misleading of all possible characters." She (p. 246) concluded that the pseudocoelomates (including molluscs; p. 268) were polyphyletic derivatives of several acoelomate lines. Nielsen (1995) saw "nothing to indicate that the acoelomate condition is ancestral" or "that the various coeloms are homologous" (p. 65), and he opined that the pseudocoelomate versus coelomate distinction had been "strongly overemphasized" (p. 235). He rejected, however, the idea that the acoelomate and pseudocoelomate conditions were derived from coelomate ancestors (p. 236). A cladistic analysis by Wallace et al. (1996) also indicated that pseudocoelomates were polyphyletic, with one clade comprising Rotifera and Acanthocephala and another comprising two lesser clades: (Nematoda + Nematomorpha) and (Kinorhyncha + Loricifera + Priapulida).
  • Molecular phylogenetic studies (Fig. 17) support the nontraditional view that the pseudocoel is apomorphic (derived) with respect to the coelom. The traditional pseudocoelomates (including Nematoda, Nematomorpha, Priapulida, Kinorhyncha, Rotifera, and Entoprocta) are scattered in two distinct clades, each of which also includes coelomates. In addition, the out-group of these two clades, Deuterostomia, is coelomate. Thus the most parsimonious hy-pothesis is that the coelom is plesiomorphic in all Bilateria, and the pseudocoel is derived from it.
  • Molecular phylogenetic studies also suggest that the acoelomates are derived from coelomates. "Acoelomates" (including Platyhelminthes and Gnathostomulida) occur within a clade that mostly comprises coelomates. The most parsimonious hypothesis is that the acoelomate condition evolved from a coelomate, not that coeloms evolved from acoelomates many times in these other phyla.
  • Acoelomates may, however, be monophyletic within this clade (Giribet et al. 2000).
  •