Nature, V413, 157
MORPHOLOGICAL CHARACTERS
Edgecombe et al. (2000) described 211 characters for Panarthropoda, most of which are used here. Characters in that work that pertained to Annelida or which are invariant in the ingroup for this study (synapomorphies of Panarthropoda) are excluded in the present analysis.
For embryological characters 1-10, Halobiotus (Eibye-Jacobsen, 1997) is used for Eutardigrada; Glomeris (Dohle, 1964) is coded as a proxy for Sphaereotheriidae; Polyxenus is coded after Seifert (1960); Pauropodinae is based on Pauropus (Tiegs, 1947); Hanseniella is coded from Tiegs (1940); data for Chilopoda are coded for Scolopendra (Heymons, 1901), Scutigera (Dohle, 1970) and Lithobius (Hertzel, 1984); Campodea is based on Uzel (1898) and Tiegs (1942) with observations on the confamilial Lepidocampa by Ikeda and Machida (1998); japygids are scored based on Japyx (Silvestri, 1933), as interpreted by Ikeda and Machida (1998); Petrobius (Larink, 1969) and Pedetontus (Machida et al., 1990, 1994) are used for Machilidae; Lepisma (Heymons, 1897; Larink, 1983), Ctenolepisma and Therombia (Woodland, 1957) are used for Lepismatidae (summarised by Anderson, 1973); Baetis (Böhle, 1969) is coded as a proxy for Callibaetis (Baetidae); Blatta (Wheeler, 1889, summarised by Anderson, 1973) is coded for Blattodea; Locusta migratoria is coded from Roonwal (1936). Codings for Crustacea are based primarily on syntheses by Anderson (1973, 1982) and Weygoldt (1994). Opilio is the only taxon coded for Opiliones, using data from several other genera of Phalangioidea (e.g., Moritz, 1957; Juberthie, 1961, 1964).
1. Non-migratory gastrulation: 0, absent; 1, present. Anderson (1973) described a unique pattern of gastrulation in peripatopsid Onychophora, which has been regarded as an autapomorphy for Onychophora (Monge-Nájera, 1995).
2. Early cleavage: 0, total cleavage with radially oriented position of cleavage products; 1, intralecithal cleavage. A wide range of euarthropods share early total cleavage without oblique spindles, which Scholtz (1998) suggested is an autapomorphy of Euarthropoda. Tardigrades are described as having total cleavage, but the orientation is uncertain (Eibye-Jacobsen, 1997). Onychophora is coded from Anderson (1973, 1979), and Pycnogonida coded from Dogiel (1913). Edgecombe et al. (2000) coded Insecta as having complete superficial cleavage, but this is restricted to Dicondylia, Archaeognatha (Machilidae) having early total cleavage (Larink, 1997). The development of several species of Pycnogonida belonging to the families Ammotheidae, Callipallenidae, Endeidae and Phoxihilidiidae (Morgan, 1891; Meisenheimer, 1902; Sanchez, 1959) shows variation in the type of cleavage depending on the egg size. Species with small eggs have total cleavage with radially oriented position of cleavage cells (e.g. Endeis spinosa [Sanchez, 1959]), however different species of the family Ammotheidae are variable (Morgan, 1891; Meisenheimer, 1902; Sanchez, 1959).
- Blastokinesis with amnioserosal fold: 0, absent; 1, amniotic cavity open; 2, amniotic cavity closed (amnioserosal fold fuses beneath the embryo). Insect embryology is uniquely characterised by the division of the dorsal extra-embryonic ectoderm into an amnion and a serosa (Anderson, 1973; Machida and Ando, 1998). We follow Whiting et al. (1997) in regarding the closed amniotic cavity of Dicondylia as a modification of the open (Larink, 1983) amniotic cavity of Archaeognatha (i.e., the character is ordered). Aspects of the archaeognathan amnion, notably the yolk folds that encompass the embryo (Machida et al., 1994), may present unique characters for that group.
- Blastoderm cuticle (cuticular egg envelope): 0, absent; 1, present. Anderson (1973) identified a thin, highly resistant blastoderm cuticle beneath the chorion as shared by Progoneata, and lacking in Chilopoda, the latter largely based on Heymons’ (1901) work on Scolopendra. Machida and Ando (1998), however, cited Knoll’s (1974) study of Scutigera as indicating its presence within Chilopoda. Blastoderm cuticle is also present in Collembola and Diplura and, as in myriapods, is formed by the embryo and presumptive serosa (Machida and Ando, 1998). In Archaeognatha and Zygentoma, the cuticular egg envelope is formed by the serosa alone (without a contribution by the embryo) (Machida and Ando, 1998), whereas it is lacking in some pterygotes (e.g., Drosophila: Machida and Ando, 1998). Distinction from so-called blastoderm cuticle in Xiphosura (Anderson, 1973:370) is required.
- Dorsal closure of embryo: 0, definitive dorsal closure (dorsal covering of embryo participates in the definitive dorsal closure); 1, provisional dorsal closure (embryonic dorsal covering degenerates without participating in the definitve closure, which is exclusively derived from the embryo). Definitive and provisional dorsal closure of the embryo are as defined by Machida and Ando (1998) to describe the cover of the embryo and hatching in myriapods (Pauropoda, Symphyla, Chilopoda) and hexapods (Collembola, Diplura, Insecta), respectively. Provisional closure in insects was summarised by Johannsen and Butt (1941:56-57).
- Ectoteloblasts forming part of metanaupliar/egg-naupliar region of germ band: 0, absent; 1, present, at anterior border of blastopore. Ectoteloblasts are specialised stem cells that give rise to the ectoderm of most postnaupliar segments in Malacostraca (Gerberding, 1997). They are absent in branchiopods [Daphnia based on the cladoceran Leptodora kindti (Gerberding, 1997)], and are lacking only in Amphipoda among the Malacostraca (Dohle and Scholtz, 1988; Weygoldt, 1994). Ectoteloblasts in leptostracans, stomatopods, syncarids and decapods are characterised by their circular or semi-circular arrangement at the anterior border of the blastopore, whilst those of peracarids are arranged in a single row (Weygoldt, 1994). Cells that form the early ectodermal material of the germ band in Cirripedia have been called ectotelobasts (Anderson, 1969, 1973), but Dohle (1972) considered morphological differences from the ectoteloblasts of Malacostraca to rule out homology (Gerberding, 1997). Scholtz (2000) summarised evidence for precise homologies in malacostracan teloblasts, with most groups sharing 19 ectoteloblasts and 8 mesoteloblasts. The latter share detailed similarities in their arrangement (one median pair and three lateral pairs).
- Caudal papilla: 0, absent; 1, present. Scholtz (2000) identified an anteroventrally folded caudal papilla as unique to Malacostraca. The caudal papilla is a ventrally-pointing tube derived from the preanal growth zone, containing the proctodaeum. It is folded anteroventrally in egg-nauplii. A caudal papilla is lacking in some peracarid groups (Tanaidacea, Isopoda, Cumacea, Mictacea).
- Fat Body: 0, absent; 1, fat body cells develop from vitellophages in yolk; 2, fat body cells develop from walls of mesodermal somites. The presence of a cephalic storage organ, the fat body, has been identified as an atelocerate synapomorphy (Boudreaux, 1979). Anderson (1973) made a distinction between vitellophagal fat body cells (Symphyla + Pauropoda + Diplopoda) and an origin of the fat body in the mesoderm (Chilopoda + Hexapoda). Dohle (1980) upheld this distinction, and employed the former condition as evidence for monophyly of the progoneate myriapods. A partial uncertainty coding (states 1 or 2, but not 0) is employed for several taxa in which a fat body is present but its embryological origin is unknown.
- Fate map ordering of embryonic tissues: 0, presumptive mesoderm posterior to presumptive midgut; 1, presumptive mesoderm anterior to midgut; 2, mesoderm midventral, cells sink and proliferate, midgut internalises during cleavage; 3, mesoderm diffuse through the ectoderm; 4, midgut develops from anterior and posterior rudiments at each end of midventral mesoderm band. Fate map patterns follow Anderson (1973, 1979) and Schram (1978). The phylogenetic value of fate maps has been criticised (Weygoldt, 1979), but Anderson (1982) reiterated the similarity of patterns across some major groups (e.g., all Crustacea can be uniquely characterised by state 1 above fideAnderson, 1982).
- Embryological development: 0, with a growth zone giving rise to both the prosoma and opisthosoma; 1, with a growth zone giving rise to the opisthosoma (Anderson, 1973; Dunlop and Webster, 1999). A growth zone giving rise to the ambulatory segments of the prosoma and the opisthosoma is found in scorpions (Euscorpius: Yoshikura, 1975) and xiphosurans, while in other arachnids this growth zone gives rise to the opisthosoma only, the prosoma developing directly from the blastoderm. Based on the latter observation, we code Mastigoproctus as described for Typopeltis (Anderson, 1973).
- Engrailed expressed in mesoderm patterning: 0, present; 1, absent. Zrzavý and Štys (1995) surveyed "compartment-like patterning" in the mesoderm of annelids and arthropods, as marked by engrailed expression. Limited data are available to indicate the absence of such mesodermal patterning in some insects and crustaceans (Artemia, peracarids and decapods: see Dohle, 1997) versus its presence in at least some chilopods, onychophorans and annelids. Dohle (1997) characterised the difference between myriapods (Ethmostigmus: Whitington et al., 1991) and hexapods/crustaceans as the former having engrailed staining in mesoderm and in the cytoplasm whereas the latter have en-product confined to the nuclei of ectodermal cells.
- Epimorphic development: 0, absent; 1, present. Several arthropod groups have been diagnosed by epimorphosis, hatching with the complete complement of segments (e.g., Epimorpha within Chilopoda; Diplura + Insecta fide Kraus, 1998).
- Nauplius larva or egg-nauplius: 0, absent; 1, present. Edgecombe et al. (2000) coded the nauplius (a swimming larva) as inapplicable for terrestrial taxa. Within Entomostraca, the nauplius is lacking only in Cladocera (Gerberding, 1997). Most malacostracan exemplars considered here have direct development (e.g., Leptostraca and Peracarida), but can be scored for the presence of an egg-nauplius. Some peracarids (Amphipoda, Tanaidacea, Cumacea, Isopoda), however, lack an egg-nauplius (Scholtz, 2000). Dahms (2000) summarised specific details of the naupliar apparatus that imply a single origin for this larval type, but Scholtz (2000) argued that a free-living nauplius evolved from an egg-nauplius within Malacostraca.
- Bivalved secondary shield grows from tergite of maxillary segment during larval development (heliophora stage): 0, absent; 1, present. Walossek (1995) and Walossek and Müller (1998a) used a unique secondary shield during larval development as a synapomorphy for Onychura (= Conchostraca + Cladocera).
- Pupoid stage (motionless stage after hatching, pupoid remains encased in embryonic cuticle): 0, absent; 1, present. Anderson (1973) summarised evidence for a pupoid stage in Chilopoda, Diplopoda and Pauropoda. Dohle (1998), however, identified a pupoid stage as confined to diplopods and pauropods, and Enghoff et al. (1993) recognised the pupoid as a so-called hexapod stage. We recognise the peripatoid and foetoid stages of Epimorpha (Chilopoda) as character 255. Glomeris is coded as a proxy for Sphaerotheriidae.
- Sclerotisation of cuticle into hard, articulated tergal exoskeleton: 0, absent; 1, present.
- Cuticle calcification: 0, absent; 1, present. Enghoff (1984) regarded a calcified cuticle as a synapomorphy of Chilognatha. Calcium carbonate impregnation of the cuticle is also coded for Reptantia but not for the shell of Cirripedia (coding is based on the cuticle).
- Cilia in photoreceptors: 0, present; 1, absent. Wheeler et al. (1993) coded for a reduction in cilia in onychophorans and euarthropods relative to annelids. We modify the coding of Edgecombe et al. (2000: character 17), which coded the euarthropod state with reference to cilia being present only in sperm (versus also present in the photoreceptors in Onychophora). A phylum-level groundplan has been adopted.
- Tendon cells with tonofilaments penetrating epidermis: 0, absent; 1, present. Boudreaux (1979) and Wägele (1993) acknowledged tonofilaments as a euarthropod synapomorphy, and Dewel and Dewel (1997) confirmed their absence in onychophorans and tardigrades. A phylum-level groundplan has been adopted.
- Dorsal longitudinal ecdysial suture with forking on head: 0, absent; 1, present. Edgecombe et al. (2000: character 20) coded variation in ecdysial suture patterns in Panarthropoda as a multistate character. Their coding for myriapods and hexapods followed Boudreaux (1979), who regarded ecdysis involving transverse rupture between the head and trunk to be diagnostic of Myriapoda. While a head-trunk split is reasonably regarded as the groundplan state for Myriapoda, details of ecdysial patterns in various taxa complicate coding. For example, within Chilopoda, Lithobiomorpha moult at the transverse suture on the head shield (Lewis, 1981), and it is probable that Craterostigmus has the same ecdysial pattern, having identical sutures on the head shield (see character 21). In Geophilomorpha, Lewis (1961) described ecdysial rupture across the anterior part of the head shield in Strigamia. These deviations lead us to abandon coding head-trunk rupture across Myriapoda. Likewise, within Crustacea group-specific ecdysial patterns can be identified (e.g., biphasic moult with the break between pereionites 4 and 5 in Isopoda: Brusca and Wilson, 1991), but coding states that can be homologised across Panarthropoda is complicated. We have thus restricted coding of ecdysial patterns. Boudreaux (1979) claimed dorsal longitudinal ecdysis to be diagnostic for Hexapoda, but Snodgrass (1952:269) specified that the latter pertained to Insecta in particular, whereas Collembola and Protura have a head-trunk ecdysial split (Kaufman, 1967:16). Though Onychophora also have a dorsal longitudinal rupture of the cuticle, the insect pattern possesses details, such as dorsal forking (frontal line) on the head that permit distinction. In japygids the Y-shaped frontal line is lacking, but the posterior cornonal suture is present.
- Transverse and antenocellar sutures on head shield: 0, absent; 1, present. Edgecombe et al. (1999: character 7) coded an ecdysial complex of transverse and antenocellar sutures (sensu Crabill, 1960) as shared by Craterostigmus and Lithobiomorpha. The frontal line in some Geophilomorpha may be homologous with the transverse suture, but the antennocellar suture is lacking.
- Resilin protein: 0, absent; 1, present. Weygoldt (1986) indicated that the spiral protein resilin is known only from euarthropods (summarised by Hackman, 1984) and onychophorans. Nielsen (1995), however, mapped resilin onto the tree as a euarthropod synapomorphy, indicating its absence in tardigrades and onychophorans. We follow the phylum-level groundplan assigned by Nielsen (1995).
- Moulting gland: 0, absent; 1, present. Wägele (1993) cited a moulting gland as a diagnostic character of Mandibulata. This was based on a proposed homology between the Y-organ of Malacostraca (Fingerman, 1987) and the prothoracic gland of insects. Wägele noted that such moulting glands in insects and crustaceans are hypodermal derivations of the second maxilla, and are absent in chelicerates. An alleged ecdysial gland in some chilopods (Lithobiomorpha: Seifert and Rosenberg, 1974; glandula capitis in Scutigeromorpha: Seifert, 1979) may be homologous. Evidence for an ecdysial gland has not been found in other myriapods (Tombes, 1979) except for polyxenid millipedes (glandula perioesophagealis; Seifert, 1979). Studies of branchiopods have not discovered similar moulting glands although moulting hormones appear to be present (Martin, 1992).
- Bismuth staining of Golgi complex beads: 0, not staining; 1, staining. Locke and Huie (1977) observed Golgi beads to stain with bismuth (also judged by the reaction with interchromatin and perichromatin granules present in most nuclei) in various euarthropods and tardigrades, but not in Onychophora (Epiperipatus), Annelida, Mollusca, Nematoda, or Platyhelminthes. Bismouth staining was observed for Limulus, an undetermined isopod, Orconectes (coding for Reptantia) and Locusta for the terminals here coded. However this pattern seems to be a putative synapomorphy for Arthropoda, since it has also been recorded in other chelicerates, millipedes and several neopteran insects. The three exemplars of Pycnogonida are here coded based on the undetermined pycnogonid of Locke and Huie (1977).
- Metanephridia with sacculus with podocytes: 0, absent; 1, present. While metanephridia are probably plesiomorphic for arthropods (Fauchald and Rouse, 1997), the sacculus and podocytes are novel nephridial structures for onychophorans and euarthropods, lacking in tardigrades (Nielsen, 1998; Schmidt-Rhaesa et al., 1998) and pycnogonids (King, 1973). A groundplan coding has been adopted.
- Distribution of segmental glands: 0, on many segments; 1, in at most last four cephalic segments and first two post-cephalic segments; 2, on second antennal and maxillary segments only. Definition of the basic euarthropod distribution of segmental glands, a reduction from that in Onychophora, follows Weygoldt (1986). We have not attempted to define all variants of segmental gland distribution within Euarthropoda, and state 1 above is an artificial grouping. A more advanced reduction in Crustacea, restricted to the antennal and maxillary segments, has been regarded as a crustacean synapomorphy (Lauterbach, 1983, 1986). Walossek and Müller (1990:410) considered remipedes (Schram and Lewis, 1989) and anostracans to deviate from this state in possessing additional cephalic segmental glands, but Wägele (1993) dismissed these as integumental glands and embryonic mesodermal cells, respectively.
- Tömösváry organ ("temporal organs" at side of head behind insertion of antenna): 0, absent; 1, present. Homology of Tömösváry organs across the Myriapoda has been widely accepted (Snodgrass, 1952), but relationships to similarly positioned structures in hexapods are contentious. François (1969), for example, homologised the pseudocellus of Protura with Tömösváry organs, whereas Tuxen (1959) regarded them as antennal vestiges on the basis of musculation. The postantennal organs of Collembola may also be homologous (Haupt, 1979), and as such have been coded here. We have scored the temporal organs of Ellipura as homologous with those of Myriapoda, following Haupt (1979) and Bitsch and Bitsch (1998, 2000), though Dohle (1997) questioned the likelihood of this homology. The homologue of the Tömösváry organ in Craterostigmus is a ringed organ on the cephalic pleurite (Shear and Bonamo, 1988, fig. 50; Dohle, 1990, fig. 2), in a similar position as in Lithobiomorpha. Despite arguments that the organ could be non-functional in Craterostigmus (Borucki, 1996), it is unambiguously present. Štys and Zrzavý (1994) refer to the possibility of a Tömösváry organ in Diplura (Japygina), but this homology has not been substantiated.
- Salivary gland reservoir: 0, absent; 1, present. Monge-Nájera (1995) identified a salivary gland reservoir as an onychophoran autapomorphy.
- Malpighian tubules formed as endodermal extensions of the midgut: 0, absent, 1, present. Shultz (1990) claimed that endodermal Malpighian tubules are unique to Arachnida and, despite their absence in some ingroup taxa (such as Opiliones), resolved them as an arachnid autapomorphy. Hexapod and myriapod Malpighian tubules, in contrast, are extensions of the ectodermal hindgut (see character 30). The non-homology of these structures is generally recognised, and we have accordingly coded them as separate characters.
- Malpighian tubules formed as ectodermal extensions of the hindgut: 0, absent; 1, single pair of Malpighian tubules at juncture of midgut and hindgut; 2, multiple pairs of tubules at anterior end of hindgut. The presence of Malpighian tubules in Collembola is dubious (Clarke, 1979; Bitsch and Bitsch, 1998; here coded as absent), while Protura have several pairs of papillae behind the midgut-hindgut junction (see character 31). Distinct conditions can be recognised within the myriapods and the ectognath hexapods, and serve as the basis for states 1 and 2 above. The homology of insect Malpighian tubules (whether ectodermal or entodermal) is controversial, but an ectodermal origin is best supported (Dohle, 1997). One or a small pair of supernumerary Malpighian tubules is present in some chilopods (Prunescu and Prunescu, 1996). The so-called Malpighian tubules of eutardigrades are not in contact with cuticle and as such do not appear to be ectodermal in origin (Møbjerg and Dahl, 1996).
- Form of ectodermal Malpighian tubules: 0, elongate; 1, papillate.