The phylogenetic position of the Arthropoda
Schmidt-Rhaesa, A., Ehlers, U. Bartolomaeus, T, Lemburg, C. and Garey, J.R. (1998)


 Traditionally, Panarthropoda (Euarthropoda, Onychophora, Tardigrada) are regarded as being closely related to Annelida in a taxon Articulata, but this is not supported by molecular analyses.  comparisons of gene sequences suggest that all molting taxa (Panarthropoda, Nematoda, Nematomorpha, Priapulida, Kinorhyncha, Loricifera) are related in a monophyletic taxon Ecdysozoa. An examination of the characters supporting Articulata reveals that only segmentation with a teloblastic segment formation and the existence of segmental coelomic cavities with nephridia support the Articulata while all other characters are modified or reduced in the panarthropod lineage. Another set of characters is presented that supports the monophyly of Ecdysozoa: molting under influence of ecdysteroid hormones, loss of locomotory cilia, trilayered cuticle and the formation of the epicuticle from the tips of epidermal microvilli. Comparative morphology suggests Gastrotricha as the sister group of Ecdysozoa with the synapomorphies: triradiate muscular sucking pharynx and terminal mouth opening. Thus there are morphological characters which support Articulata but molecular as well as morphological data advocates Ecdysozoa. Comparison of both hypotheses should prompt further thorough and targeted investigations.

Figure 1.  Concurring hypotheses:  Panarthropoda are either the sister taxon of Annelida within the Articulata (A) or of Cycloneuralia within Ecdysozoa.

Figure 2.  Resulting cladogram of the analysis of 18S rRNA gene sequences from Aguinaldo et al. (1997).  Protostomia (Gastroneuralia), Ecdysozoa and Spiralia (bold lines) are strongly supported groups.  The branching patterns within Ecdysozoa and Spiralia are not always well supported and are therefore not necessarily representative.

Figure 3.  Character evolution under the Articulata hypothesis.  Several plesiomorphic (1) or probable synapomorphic (2) characters of the stem lineage of Articulata are reduced or modified in the panarthropod stem lineage.  Characters of (3) are probable synapomorphies of Annelida and Panarthropoda.  Characters are: 1. Collagenous cuticle, trochophore-like larva, spiral cleavage.  2. One pair of coelomic cavities per segment, one pair of metanephridia per segment, ventral nerve cord with one pair of ganglia per segment, one pair of appendages per segment, one pair of palps (?).  3. Metameric organization, teloblastic segment formation, the general existence of coelomic cavities and nephridia.  4. Autoapomorphies of Panarthropoda:  chitinous cuticle, ecdysis.  5.  Probable autapomorphies of Annelida:  one pair of palps?, nuchal organs?, parapodia?, arrangement of setae?

Figure 4.  Proposed relationships under the Ecdysozoa hypothesis:  Panarthropoda and Cycloneuralia are sister taxa, the closest sister group of Ecdysozoa is Gastrotricha.  Characters are: 1. Protostomia (Gastroneuralia): dorsofrontal cerebral ganglion with inner neuropil, longitudinal nerve cords including one pair of ventrolateral nerves.  2. (Gastrotricha + Ecdysozoa): muscular sucking pharynx, terminal mouth opening, bilayered cuticle including a trilaminate epicuticle.  3. Ecdysozoa:  molting of cuticle by ecdysteroid hormones, loss of locomotory ciliachitinous endocuticle, secretion of epicuticle by the tips of epidermal microvilli.  4.  Panarthropoda: segmental organization, segmental locomotory appendages.  5. Cycloneuralia:  circumpharyngeal brain with an equally thick ring, brain with antero-posterior sequence of pericarya - neuropil - pericarya.  6.   Nematoida:  reduction of circular musculature.  7.  Scalidophora:  introvert with scalids.

Figure 5.  Ultrastructural cross section through an early embryo (coiled stage) of Epiperipatus biolleyi (Onychophora).  coe, embronic coelomic cavity lined by undifferentiated cells with rudimentary cilia; ect, ectoderm; int, embryonic intestine.

Figure 6.  Molting in euarthropods (A), tardigrades (B) and nematodes (C).  A after Foelix (1982); B after Marcus, redrawn from Ruppert and Barnes (1994); C after Ruppert and Barnes (1994).

Figure 7.  A. Molting in Nectonema munidae (Nematomorpha): the larval cuticle (lc) is replaced by the adult cuticle (ac).  ep, epidermis.  B. Trilayered cuticle of the larva of Halicryptus spinulosis (Priapulida) in the neck region.  epi, epicuticle; exo, exocuticle; endo, endocuticle; ep, epidermis.  C:  Trilayered cuticle of Epiperipatus biolleyi (Onychophora).  Note the trilaminate character of the epicuticle.  D:  Molting in Macrobiotus hufelandi (Tardigrada).  A new epicuticle is formed by secretion of numerous separate patches (arrows).  E:  Formation of a new epicuticle by the tips of epidermal microvilli in a scalid of a larval Halicryptus spinulosus (Priapulida).  Note that the epicuticle is secreted in separate patches (arrows).  C by B. Walz, Potsdam with kind permission of Springer Verlag, Berlin.

Figure 8.  Triradiate pharyngeal lumina in onychophorans and nematodes.  In an early (B) and slightly older (A) embryo of Opisthopatus blainvillei (Onychophora) at the level of the brain (A) and further posterior (B).  b, brain; pe, pharyngeal epithelium; sag, duct of salivary gland; slg, duct of slime gland; vnc, ventral nerve cords; vo, ventral organ.  C.  In Enoploides spiculohamatus (Enopida, Nematoda).  pg, pharyngeal gland.  D: In an undetermined freshwater nematode.  C by M. Stohr, Gottingen.