The Evolutionary Relationships of Rotifers and Acanthocephalans

James R. Garey,  Andreas Schmidt-Rhaesa, Thomas J. Near & Steven A. Nadler

From the Sixth Rotifer Symposium at Saint John's University, in press in Hydrobiologia

Summary
 Advances in morphological and molecular studies of metazoan evolution have led to  a better understanding of the relationships among  rotifers (Monogononta, Bdelloidea and Seisonidea) and acanthocephalans, and their relationships to other bilateral animals.  The most accepted morphological analysis places Acanthocephala as a sister group to Rotifera, although other studies have placed Acanthocephala as a sister taxon to Bdelloidea or Seisonidea.  Molecular analyses using nuclear 18S rRNA and mitochondrial 16S rRNA genes support Acanthocephala as a sister taxon to Bdelloidea, although no molecular data is available for Seisonidea.  Combining molecular and morphological analyses of Bilateria leads to a tree with Platyhelminthes, Rotifera, Acanthocephala and Gnathostomulida (and probably Gastrotricha) as a sister group to the annelid-mollusc lineage of the Spiralia (Lophotrochozoa).


 

Figure 1.  Possible relationships between Seisonidea (S), Monogononta (M) and Bdelloidea (B).  1: Clefts but no pores in terminal organ of the protonephridia; rotatory organ; unpaired retrocerebral glands; salivary glands integrated into the mastax (Ahlrichs, 1997); vitellarium (Wallace & Colburn, 1989).  2: Paired ovaries, ramate mastax, absence of secreted tube (Pennak, 1989).  3: Males present, no bladder, cellular stomach with microvilli (Ricci et al., 1993), similarities of internal layer in their syncytial integument (Clement, 1993).



Figure 2.  Proposed relationships between Seisonidea (S), Monogononta (M), Bdelloidea (B) and Acanthocephala (A).  1: Internal layer of syncytial epidermis.  2: Lemnisci and proboscis present (Lorenzen, 1985).  3: Pseudocoel present, syncytial epidermis, monociliated pit absent, hermaphorditism absent, acrosome present, anteriorly inserting flagellum on sperm (Wallace et al., 1996), internal layer in the syncytial epidermis (Nielsen, 1995). 4: Parthenogenesis, hypodermic impregnation, collagen absent (Wallace et al., 1996), toes with adhesive glands (Nielsen 1995).  5: Internal layer in the syncytial epidermis, anteriorly inserted flagellum on sperm cell, outer epidermal cell membrane intrusions with bulbs.  6: Dense bodies within spermatozoa, epidermis with filament bundles (Ahlrichs, 1997).
 

Figure 3.  Molecular phylogeny of Bilateria based on the 18S rRNA gene.  The tree shown is a strict consensus of NJ, MP, and ML analyses (modified after Garey et al., 1996a).  Numbers above and below each fork represent the percentage of 1,000 bootstrap replicates that support the branch in the MP and NJ trees respectively. Numbers to the right of each fork are CP values from the NJ tree.  Values are shown only when greater than 50. The Rotifera + Acanthocephala clade, Bdellodea + Acanthocephala clade, and the Acanthocephala clade were all supported by decay indices greater than 20.
 



Figure 4. Molecular phylogeny of Bilateria based on a 600 bp fragment of the mitochondrial 16S rRNA gene.  The tree shown is a NJ tree.  Bootstrap values for Kimura distances with gamma correction ( =0.72) are shown above the forks, values for Tamura & Nei distances are below  and numbers to the right are CP values for Kimura distances.



Figure 5.  Proposed position of Rotifera within the Bilateria based on morphological and molecular data. The annelid-mollusc lineage refers to the bulk of the non-ecdysozoan protostomes, but not necessarily all of them.  Only a few key characters are given. 1: Blastopore becomes the anus. 2: Ventral lateral nerve chord (Ahlrichs, 1995).  3: Molting by ecdysis (Aguinaldo et al., 1997). 4: Spiral cleavage. 5: Filiform sperm without accessory centriole (Ahlrichs, 1995).  6. Biciliary terminal cell in the protonephridia (Ax, 1996).  7: Jaws composed of rods imbedded in a cuticular matrix (Ahlrichs, 1997).  8: Internal layer in the syncytial epidermis (Storch & Welsch 1969).