http://www.collembola.org/publicat/ordo.htm - Last updated on 2017.01.04 by Frans Janssens
Checklist of the Collembola: Note on the Ordinal Morphogenetic Relationships of Collembola

Frans Janssens, Department of Biology, University of Antwerp, Antwerp, B-2020, Belgium

Abstract.
The Collembola evolved into two main groups: in Poduromorpha, with small furca, a furcula, and in Neocollembola, with well developed furca. The Neocollembola evolved according to 2 schemes: 1. tomoceromorph forms, with enlarged third abdominal segment, and 2. panentomobryomorph forms, with enlarged fourth abdominal segment. The Neelipleona, small subglobular forms with reduced abdomen and enlarged thorax, is considered as basal remnant group of Neocollembola. The Panentomobryomorpha specialised further into 1. Euentomobryomorpha, linear comma-shaped forms, 2. Coenaletidae, linear comma-shaped forms with enlarged abdominal segments, and 3. Symphypleona, subglobular forms with enlarged abdomen.
Some Poduromorpha, such as Neanuridae, Onychiuridae and Tullbergiidae, with vestigial furcula, Euentomobryomorpha, such as Microfalculidae and some Isotomidae, and Symphypleona, such as Mackenziellidae, with a furcula are secondarely regressive forms.

Introduction

The furca is the most prominent feature that is characteristic to the Collembola in general, although it can be secondarely reduced completely. The development of the furca has played a prominent role in the development of the overall body shape of the Collembola. The furca-bearing fourth abdominal segment is the most variable abdominal segment, morphologically (Massoud, 1971:196). Even in some Poduromorpha, it is also developed larger then the other segments. In many Entomobryomorpha s.l., the fourth abdominal segment is the largest of all. And in most Symphypleona, it is the fourth abdominal segment that contributes most to the enlargement of the trunk. The ordinal phylogeny that is proposed here is based on a dichotomic morphogeny induced by the progressively increasing function of the furca.

Ordinal Phylogenetic Relationships

Fig.1. Tentative ordinal phylogenetic relationships
	  +----------- "protoCollembola" (+)
     +----+
     |    +------------ Poduromorpha
<-pC-+
     |    +------------ Neelipleona
     |    |
     +-Nc-+    +------- Tomoceromorpha
	  +-Pt-+
	       |  +---- Euentomobryomorpha 
	       +Pe+
		  |  +- Coenaletidae
		  +2-+
		     +- Symphypleona

This ordinal tree (Fig.1) is a compromise compilation of the views of relationships among orders of Collembola based on phylogenies proposed by Cassagnau (1971), Massoud (1971, 1976) Moen & Ellis (1984), Bretfeld (1986), Fjellberg (1994), Soto-Adames (1996), D'Haese (2002, 2003), Park (2002), Deharveng (2004), Gao & al. (2008), Xiong & al. (2008), Schneider & al. (2011) and Yu & al. (2016). Traditionally, the Collembola have been divided into five groups (Poduromorpha, Metaxypleona, Neelipleona, Entomobryomorpha, and Symphypleona) which different authors have considered to represent orders, sections or every category in between these two. D'Haese (2002) and Xiong & al. (2008) considered Entomobryomorpha as paraphyletic and D'Haese (2002:1148) proposed Tomoceromorpha as a new basic group of Collembola. Schneider & al. (2011) confirmed 1. the monophyly of Neelipleona and 2. that Neelipleona are not closely related to Symphypleona. Yu & al. (2016) consider Neelipleona and Poduromorpha closely related. We consider Neelipleona as basal apomorph group of the Neocollembola (fig.1:Nc). We propose Coenaletidae (= Entomobryomorpha with grasping antennae) as extant representatives of transient forms between Entomobryomorpha and Symphypleona (via Sminthuridoidea = Mackenziellidae + Sminthurididae (= Symphypleona with grasping antennae)).

Description of basic groups of Collembola

Protocollembola. The hypothetical ancestors of all Collembola, the protoCollembola, are characterised by 1. the protergite being distinctly present, and 2. the furcal precursor muscles of the third abdominal segment being present. The protoCollembola and the direct plesiomorph descendants are extinct.

Fig.Neo. Tentative tree
       pT+     pT+     pT+
       f3+     f3+     f3+
<--pC--o--pC'--o--pC"--o protoCollembola (+)
       |       |
       |       |       pT+
       |       |       f3-
       |       +-------o Poduromorpha
       |
       |       pT-
       |       f3+
       +-------o Neocollembola (Nc)
Poduromorpha. The Poduromorpha are characterised by: 1. the protergite being distinctly present, and 2. an elongated and segmented habitus. These characters are assumed to be plesiomorphies (after Thibaud, Schulz & da Gama Assalino, 2004:3).
In the Poduromorpha, the apomorph descendants of the protoCollembola', the furcal precursor muscles of the third abdominal segment are absent (f3-). In the plesiomorph descendants of the protoCollembola', the protoCollembola", the furcal precursor muscles of the third abdominal segment remain present (f3+). These plesiomorph descendants are all extinct (+).
The combination of characters present in members of the Isotogastruridae seem to represent a transitional stage between the orders Poduromorpha and Entomobryomorpha. The ordinal position of Isotogastruridae is resolved by D'Haese (2003:577,578) as sister group of Tullbergiidae. To avoid breaking the taxonomic hierarchy, it is here tentatively placed as a 'familia incertae sedis' in Onychiuroidea, close to Tullbergiidae.

Metaxypleona. Contrary to Moen & Ellis (1984) and Stebaeva (1988, cited from D'Haese, 2003:564), but more in line with Soto-Adames (1996), Carpenter & Wheeler (1999), D'Haese (2002, 2003), Park (2002) and Deharveng (2004), Metaxypleona is here not maintained to give Podura an ordinal taxonomic status. We do not agree with Börner (1906), who pointed out that Podura has some synapomorphies with Symphypleona: in particular the hypognath head and the long curved dentes of the furca. We believe that these characters developed independently in both groups and are simply the result of homoplasy. Handschin (1929:19) suggested to place Podura inbetween the Arthropleona (Poduromorpha and Entomobryomorpha s.l.) and Symphypleona. Salmon (1964:100) defined Metaxypleona1 for Podura and Actaletes as a sister group of Symphypleona. This author saw Podura as a very early stage in the morphological processes of specialisation which lead ultimately to the Symphypleona. Contrary to Salmon's opinion, we will show that Podura and Symphypleona are paraphyletic. Moen & Ellis (1984:202-203) redefined Metaxypleona, by retaining Poduridae as the only member of the order. In addition, the authors described four putative synapomorphies that support a sister group relationship between Metaxypleona and Symphypleona-Neelipleona. However, taken into account the morphological study of Frish (1978) on the heart in Podura, Actaletes and representatives of Poduromorpha, Symphypleona, and Entomobryomorpha, the Metaxypleona is here considered in close relationship with the Poduromorpha. Frish concluded that the heart of poduromorphs, including Podura, has six ostia, while the higher entomobryomorphs have five ostia, and in Symphypleona the ostia are reduced to three. The epicuticular ultrastructural lattice of microtubercles of Podura appears to be more like that of Poduromorpha than of Symphypleona (Dallai & Malatesta, 1973:135-139). According to Hemmer (1990), Podura aquatica has a haploid chromosome number of n=11, the highest of any Collembola (Hopkin, 1997:34). Symphypleona typically have n=5 up to n=7 (Dallai & al., 2000:56). This makes a close relationship between Metaxypleona and Symphypleona questionable (Hopkin, 1997:34). Jordana & Arbea (1997:15) point out that the retrocerebral complex of Podura is identical to that of Hypogastruridae, indicating that Metaxypleona and Poduromorpha are more closely related. Deharveng (2000:in litt.) notes that Podura is very near to Hypogastrura by its chaetotaxy. We agree with D'Haese (2002, 2003), Park (2002) and Xiong & al. (2008) that Podura is well embedded into Poduromorpha. Therefore, Metaxypleona is rejected, and in line with Palacios-Vargas (1994:409), Poduroidea is tentatively reestablished to give Podura superfamiliar status within the Poduromorpha, close to Hypogastruroidea.

Neocollembola. The Neocollembola are characterised by an absent protergite.
The Neelipleona, Entomobryomorpha s.l. and Symphypleona form a monophyletic grouping, the 'higher' Collembola, here called tentatively the Neocollembola (Nc in fig.1, Neo). The Neocollembola are the most ancient apomorph descendants of the protoCollembola.
In the protoCollembola (pC), the protergite is present (pT+) and the furcal precursor muscles of the third abdominal segment are present (f3+). In the Neocollembola, the apomorph descendants of the protoCollembola, the protergite is absent (pT-). In the plesiomorph descendants of the protoCollembola, the protoCollembola', the protergite remains present (pT+).

Neelipleona. The Neelipleona are characterised by: 1. an absent protergite, and 2. a diverticulate midgut (apomorph condition).
Contrary to the morphological phylogeny of D'Haese (2003:571), that supports the traditionally accepted Neelipleona-Symphypleona sister group relationschip, on the basis of two synapomorphies: 1. antennae inserted on the side of the frontal area, without contact with the clypeal area, and 2. a body of globular shape, with fused thoracic and abdominal segments, we support the paraphyly of Neelipleona-Symphypleona as shown by the combined morphological and molecular phylogeny of Robertson (2001).
The globular body shape is a very weak synapomorphy since it is realised in two completely different and even opposite ways. In Neelidae, the thorax makes up the greater part of the trunk, while in Sminthuridae s.l. the abdomen is the largest body region (Christiansen & Bellinger, 1998:1175). In Neelipleona, the globular shape of the body is realised by strongly reduced abdominal segments I-IV, which are fused and strongly curved dorsoventrad, in combination with a relatively enlarged metathoracic segment. In Symphypleona, the globular body shape is realised by enlarged abdominal segments I-IV, blown-up to such an extent that the stretched intersegmental conjuctivae are more or less indistinct.
Xiong & al. (2008) tested the grouping of Neelides with the Symphypleona in a ribosomal RNA phylogeny, and found respectively weak Maximum Likelihood (ML) support (68/0.99), weak Bayesian support (62/0.91), and no Maximum Parsimony (MP) support (<50). Taking into account the MP, ML and Bayesian trees, in average, support of the grouping of Neelides with Symphypleona is < 60, in other words the monophyly of Neelipleona+Symphypleona is not supported. Therefore, we consider the conclusion of Xiong & al. (2008:734) "Neelipleona as the sister group to Symphypleona" not supported.
Christiansen & Bellinger (1998:1175) support the independant convergent derivation of Neelidae and Sminthuridae s.l. from their respective arthropleone ancestors, such as Symphypleona from poduromorph ancestors, and Neelipleona from entomobryomorph ancestors.
Gao et al. (2008:1142) confirmed the close relationship between Entomobryomorpha and Neelipleona in a phylogenetic rDNA study of basal Hexapoda.
But in the molecular phylogeny of the Neelipleona by Schneider & al. (2011), based on 16S rDNA, COX1 and 28S rDNA D1 and D2 regions, the Neelipleona turned out to be more diverse and more ancient than previously thought and an arthropleone relationship of Neelipleona was found. Neelipleona was considered as the sistergroup of Poduromorpha + Entomobryomorpha (= Arthropleona). Although the stability of the clade Poduromorpha + Entomobryomorpha was weak: it was recovered only in 25% of the different parameter sets. Possibly, methodology flaws were involved, given it was found that Entomobryidae, Isotomidae, Hypogastruridae, Neanuridae and Dicyrtomidae were paraphyletic, even with the limited set of taxa used. Based on morphological grounds we do not support Arthropleona. In particular, due to the absence of the protergite in Entomobryomorpha, Neelipleona and Symphypleona which is a synapomorphy of the Neocollembola, while the protergite is present in Poduromorpha, a close relationship between Poduromorpha and Entomobryomorpha is doubthful.
Yu & al. (2016:288) found a close relationship between Neelipleona and Poduromorpha, although weakly supported.
Taking into account the discussion of the globular body shape and in addition that 1. the form of the retinaculum of Neelidae corresponds with that of arthropleone Collembola versus that of Sminthuridae (Börner, 1906:4); 2. abdominal bothriotricha, typical for Sminthuridae s.l., are lacking in Neelidae (Börner, 1906:4), making a close relationship between Neelidae and Sminthuridae s.l. questionable; 3. the anterior setal row of the clypeus, the prelabral setae of Yosii 1976, only has 2+2 setae as in arthropleone Collembola (Bretfeld, 1999:16); 4. the postembryonal development of Neelipleona is more in line with that of the arthropleone collembolans than with the Symphypleona, such as the longer lifetime, the number of adult instars and the alternating productive and non-reproductive instars (Blancquaert & Mertens, 1979:129); 5. the male genital organ of Megalothorax is much simpler than that of Sminthurus due to the abscence of the prolonged deferens channels and the specialised successive regions in the gonads; their structure resembles that of the arthropleone Collembola, with an additional longitudinal condensation (Willem, 1900:67); 6. the peculiar sex-determination mechanism, as well as the consequent aberrant spermatogenesis, is common to all members of the Symphypleona; this process has been demonstrated in seven genera from three different families: Sminthuridae and Dicyrtomidae (Dallai et al. 1999, 2000 cited from Dallai et al. 2001:238) and Bourletiellidae (Dallai et al. 2001:237-238); on the contrary, it has not been found in members of the Neelipleona, nor in other Collembolan species (Dallai et al. 1999 cited from Dallai et al. 2001:238);
we consider Neelipleona as the most ancient and thus basal group of Neocollembola.

Pantomoceromorpha. The sister group of Neelipleona, tentatively called the Pantomoceromorpha (Fig. 1:Pt), is characterised by: 1. an absent protergite, and 2. a non-diverticulate, smooth midgut (plesiomorph condition, given it is also found in Tomoceromorpha and Poduromorpha).

Tomoceromorpha. Tomoceromorpha are characterised by: 1. an absent protergite, 2. a non-diverticulate, smooth midgut, and 3. a muscular springing mechanism mainly situated in the third abdominal segment, making the third abdominal segment larger than the fourth.
Xiong & al. (2008) and Yu & al. (2016) confirm the findings of D'Haese (2002) that the superfamily Tomoceroidea is monophyletic and that Entomobryomorpha is paraphyletic. Unfortunately, the statement by Xiong & al. (2008) "Some special morphological characters of Tomoceroidea have been identified: the third abdominal segment longer than the fourth segment, the body with scales, and the antennae with four segments. These characters are very different from those of the other groups in Entomobryomorpha, but similar to those of some species in Poduromorpha (Hopkin, 1997)." is a misconception. The characters "the body with scales, and the antennae with four segments" are not at all different from those of other groups in Entomobryomorpha. Scales also are present in Entomobryidae and in Paronellidae. On the contrary, scales are absent in Poduromorpha. And in all Collembola the antennae have 4 segments. The monophyly of Tomoceroidea is weakly supported (63.6% in average) (Xiong & al. 2008). The monophyly of Poduromorpha + Tomoceroidea is not supported (<50% in the Bayesian tree) (Xiong & al. 2008).
Therefore, we place the new ordo Tomoceromorpha D'Haese 2002:1148 tentativelly as basal group of the Pantomoceromorpha (Fig.1:Pt).

Panentomobryomorpha. The sistergroup of Tomoceromorpha, (Fig.1:Pe), is characterised by: 1. an absent protergite, 2. a smooth midgut, and 3. a muscular springing mechanism mainly situated in the fourth abdominal segment, making the fourth abdominal segment larger than the third.

Entomobryomorpha. D'Haese (2002:1148) concludes that Entomobryomorpha is paraphyletic. Xiong & al. (2008) have confirmed that Entomobryomorpha is paraphyletic and Tomoceroidea (=Tomoceromorpha) has been proposed as a new basic group of Collembola. Therefore Entomobryomorpha is here rejected.

Euentomobryomorpha. The Euentomobryomorpha are characterised by: 1. an absent protergite, 2. a smooth midgut, 3. a muscular springing mechanism mainly situated in the fourth abdominal segment, making the fourth abdominal segment larger than the third, and 4. third and fourth abdominal segment not united and enlarged, if united, making out less than half the body size.

Group 2. Group 2 (Fig.1:2) is characterised by: 1. an absent protergite, 2. a smooth midgut, 3. a muscular springing mechanism mainly situated in the fourth abdominal segment, making the fourth abdominal segment larger than the third, and 4. third and fourth abdominal segment united and enlarged, making out about half the body size.

Coenaletidae. The Coenaletidae are characterised by: 1. an absent protergite, 2. a smooth midgut, 3. a muscular springing mechanism mainly situated in the fourth abdominal segment, making the fourth abdominal segment larger than the third, 4. third and fourth abdominal segment united and enlarged, making out about half the body size, 5. a ventral tube having two short eversible vesicles, and 6. an elongate habitus, thoracic and anterior abdominal segments not united.
The Coenaletidae are a transient form between Entomobryomorpha and Symphypleona with united third and fourth abdominal segments. Both segments are involved with the springing organ. Due to the union the springing organ may become more powerfull.
Most striking is the highly modified grasping antennae of the male in Coenaletidae, Mackenziellidae and Sminthururididae, suggesting a synapomorph relationship between these families.

Fig.2. Dicyrtomina cf. ornata from the USA
with eversed ventral tube vesicles
2006 © McClarin, J.

Symphypleona. The Symphypleona are characterised by: 1. an absent protergite, 2. a smooth midgut, 3. a muscular springing mechanism mainly situated in the fourth abdominal segment, making the fourth abdominal segment larger than the third, 4. third and fourth abdominal segment united and enlarged, making out about half the body size, 5. a ventral tube having two long eversible vesicles (see Fig.2), and 6. a subglobular habitus, thoracic and anterior abdominal segments united.
Note that the molecular phylogeny of D'Haese (2002:1148) defines Symphypleona as being paraphyletic. Xiong & al. (2008) supported the monophyly of Symphypleona moderately (72.3% in average).

Geometric Bodyplan

Fig.x. Schematic geometric model of the body segmentation
Janssens, F. 2001.
In the following discussion, a schematic geometric model of the body segmentation is used to demonstrate the relationship between the development of the furca that is synchronous with the development of the body shape.
The geometric model is based on a Cartesian coordinate system with
- an x-ordinate, the dextro-sinistral axis,
- a y-ordinate, the ventro-dorsal axis,
- a z-ordinate, the postero-anterior axis.
Three ordinate planes define the three Cartesian body sections:
- the x-y plane defines the vertical transversal section,
- the y-z plane defines the vertical longitudinal section,
- the x-z plane defines the horizontal longitudinal section.
In the schematic drawings of the body segmentation the ordinate planes are represented as glass planes. A glass sphere with a unit radius represents the unit volume. The body segments are represented as spheres with a diameter that corresponds with their length and that is proportional to the radius of the unit volume.

Discussion of Ordinal Morphogenetic Relationships

Fig.x. Schematic geometric model of protocollembolan body segmentation
Janssens, F. 2001.
The protocollembolan body is divided in the head and the trunk with a head/trunk ratio of about 1/3. The trunk itself comprises two tagmata: the thorax and the abdomen with a thorax/abdomen ratio of about 1/1. The thorax is segmented respectively in a pro-, meso- and metathorax with a ratio of 1/1/1. Pragmatically as well as functionally, the abdomen is modeled as three diplosegments: respectively a pro-, meso- and metaabdomen, with a ratio of 2/2/1. The metaabdomen is typically upwards 'rotated' relative to the mesoabdomen. In the protocollembolan body, all three diplosegments are subdivided in two equally sized segments. The mesoabdomen ventrally bears the jumping organ. The anterior mesoabdominal segment bears the retinaculum. The posterior mesoabdominal segment bears the furca.

The hypothetical protocollembolan ancestral body segmentation is modeled according to the segmental proportions as can be observed in juvenile extant Collembola. Additionally, it is presumed that in the Protocollembola
1. the prothorax is partially reduced;
2. the furca is not yet fully developed; initially, it is small: a furcula.
3. the metaabdomen is small compared to the pro- and mesoabdomen.
The smaller size of the metaabdomen is related to the smaller sized hindgut.
The upwards rotated position of the metaabdomen is related to the ventro-posterior insertion of the furcula.

Biomechanical model of the mesoabdominal furcal tension
The development of the furca is closely related with the development of the furcal muscles and the mesoabdomen. The antero-posterior tension caused by the furcal muscles on the mesoabdominal segments eventually result in a dorso-ventrally abdominal curvature. This tension is primarely caused by the flexor muscles of the furca. The furcal muscles of the hypothetical protocollembolan are modelled as three sets of muscles:
1. the flexor furcae inflex the furca underneath the trunk in its resting position,
2. the extensor furcae and
3. the levator furcae extend the furca behind the trunk to effectuate the jump.
The flexor and extensor muscles are derived from muscles that operated the ancestral abdominal legs: respectively the tergal promotor muscles and the tergal remotor muscles. The levator muscles are derived from the tergosternal muscles and intersegmental muscles of the abdominal segments. The levator muscles operate the furca indirectly by creating a hydrostatic pressure in the abdominal and furcal lumen.
There are two sets of flexor furcae, one at each side of the mesoabdomen. Each lateral set can comprise up to two sets of muscles: a primary segmental set and a secondary intersegmental set. Both are attached ventrally to the antero-lateral rim of the furcal base. The segmental set is attached dorsally to the dorso-lateral antecosta of the posterior mesoabdominal tergite. The intersegmental set is attached dorsally to the dorso-lateral antecosta of the anterior mesoabdominal tergite, such as in Orchesella cincta cf. Schaller (1970:32,Fig.50). The intersegmental set develops secondarely and only in case of large furca (such as found in Neocollembola).
There are two sets of extensor furcae, one at each side of the mesoabdomen. The dorso-ventral extensor furcae are attached dorsally to the dorso-lateral antecosta of the posterior mesoabdominal tergite and ventrally to the postero-lateral rim of the furcal base.
There are two sets of dorso-ventral levator furcae. Both sets are attached medio-ventrally at the antecosta of the posterior mesoabdominal sternite. One segmental set is attached medio-dorsally to the center of the posterior mesoabdominal tergite. The intersegmental set is attached medio-dorsally to the antecosta of the anterior metaabdominal tergite.
Only the intersegmental flexor muscles contribute to the mesoabdominal antero-posterior tension. At the moment of docking the furca in the retinaculum, this tension is maximum. The flexor tension creates a downwards momentum on the posterior mesoabdominal segment. Evolutionary, to compensate for this tension, the mesoabdominal terga tend to enlarge while the mesoabdominal sterna tend to reduce. The elongation of the mesoabdominal terga has been realised differently in Tomoceromorpha and Panentomobryomorpha. In Tomoceromorpha, the anterior mesoabdominal tergum, the third abdominal tergum, is enlarged, while in Panentomobryomorpha, the posterior mesoabdominal tergum, the fourth abdominal tergum, is enlarged.

For a discussion on the evolution of the furcal muscles, see Janssens (2008).

The furca itself is modelled in analogy with the sequence of primitive limb articulation of the hexapod ground plan according to Kukalova-Peck (1992, 2008): 1. epicoxa, 2. subcoxa, 3. coxa, 4. trochanter, 5. prefemur, 6. femur, 7. patella, 8. tibia, 9. basitarsus, 10. eutarsus, 11. posttarsus (1992) or pretarsus (2008). Kukalova-Peck claims that "These segments are all unequivocally identified by their own muscle insertions; they occur serially in all limb-derived appendages on the head, thorax, and abdomen."

Table I. Homology between limb and furca articulation
  Ancestral hexapod limb articulation Collembolan limb articulation Collembolan furca articulation
1. epicoxa epicoxa manubrium
2. subcoxa subcoxa
3. coxa coxa
4. trochanter trochanter
5. prefemur femur dens
6. femur
7. patella tibia, with pseudotarsus and unguis mucro
8. tibia
9. basitarsus empodial tubercle with optional unguiculus
10. eutarsus
11. posttarsus or pretarsus

Based on the homology described in Table I, the protocollembolan manubrium is modelled as a syncoxa with 4 pair-wise fused articles. The tergal condyles of the fused epicoxae are modelled as the basal condyles of the manubrium. It is assumed that the sternal epicoxal condyles became redundant due to the epicoxal fusion and therefore are reduced completely. The redundant condyles of the fused subcoxae are reduced completely. The outer condyles of the fused coxae remain functional while the inner ones reduce. The outer condyles of the trochanter reduce due to the fusion with the coxa. The result is a protocollembollan manubrium with a dicondylic basis and apex. Due to the fusion, the sternal remotors and promotors become redundant and are reduced. The dorsal remotors become furcal extensors and the dorsal promotors become furcal flexors. Three sets of extensor and flexor muscles remain functional: the epicoxal, the subcoxal, and the coxal set. The trochanteral set reduces completely. The epicoxal and subcoxal set cooperate to rotate the basal manubrium backward and forward. The coxal set rotates the distal dentes backward and forward. The syncoxal manubrium as well as the dentes can rotate in their respective condyles up to an angle of about 90 degrees. This allows the furca to be extended up to about 180 degrees. Due to the double set of condyles, the epicoxal and coxal condyles, the furca can be extended 180 degrees in the time required to extend the manubrial base 90 degrees. Due to the double set of manubrial condyles, the furca can be extended at such a high speed that is otherwise not possible.

Gigantic Carboniferous Collembola The compact protocollembolan body shape reduces the possibility of ever finding a fossil collembolan of similar proportions to gigantic early millipedes which reached nearly 2m (Hopkin, 1997:26). The furca is the most important factor that constrains the absolute maximum body size. The largest extant Collembola are found among the Tetrodontophora (up to 9 mm), onychiurid poduromorphans with a strongly shortened furca and Holacanthella (up to 17 mm), neanurid poduromorphans with completely vestigial furca. Taken into account the high atmospheric oxygen level (about 80% above current level) in the Carboniferous (359-239 MYA), we may assume Collembola then also reached a relative 'gigantic' size, as Insecta did. Simplified reasoning : the gigantic Carboniferous ancestral dragon-fly Meganeura monyi was about 40 cm in length; common length of extant larger dragon-flies : 5 cm; ratio = 8. Taking into account this ratio and a common size of 2 mm, and larger size of 10 mm in extant Collembola, 'gigantic' Carboniferous Collembola might have measured 16 up to 80 mm.

Fig.P. Schematic geometric model of poduromorphan body segmentation
Janssens, F. 2001.
The direct descendants of the Protocollembola are all extinct. The driving evolutionary character, the gradual enlargement of the furcula, induced the corresponding enlargement of the mesoabdomen to accomodate the larger furcal muscles. This has an effect on the trunk: the abdomen proportionally enlarges: the thorax/abdomen ratio becomes 5/7. In the plesiomorph descendants of the Protocollembola, the elongation of the furcula was still relatively small. But due to the stronger furcal muscles, the springing organ gained in functionality. The jump itself proved to be an effective escape mechanism from predators and the survivability factor of this group improved considerably compared to that of the ancestral group. The plesiomorph descendants of the Protocollembola are characterised by a furcula, a small furca; a condition typically found in the extant Poduromorpha. In some poduromorphan lineages, the furcula does not enlarge further but has a tendency to reduce. In the more derived forms such as the Onychiuridae and many Neanuridae, the furcula has become vestigial up to absent.

Fig.pN. Schematic geometric model of neocollembolan body segmentation
Janssens, F. 2001.
In the apomorph descendants of the Protocollembola, the prothorax continues to reduce while meso- and metathorax proportionally enlarge. This results in a stronger locomotory center and in a greater (soil surface) activity. The protergite is reduced completely. The protocollembolan furcula developed into a furca.
This extinct hypothetical ancestral group is here tentatively called Neocollembola (Nc in Fig. 1). The Neocollembola are here considered as being the ancestral form of the 'higher' Collembola, characterised by a lacking protergite. In addition, following new chaetotactic features were originated in this ancestral group: bothriothricha and the socalled 'neosminthuroid' setae.
For a discussion on the protergal reduction process itself, see Janssens (2001-2005).

Fig.N. Schematic geometric model of neelipleone body segmentation
Janssens, F. 2001.
In the apomorph descendents of the Neocollembola, a proportionally 'weak' proabdomen, which constrained overall body size, in combination with larger antero-posterior tension of the furcal flexor muscles on the abdomen results in a strong dorso-ventrally abdominal curvature. The downwards curvature of the abdomen results in a subglobular lateral habitus.
Note that there is no prominent upwards rotation of the metaabdomen relative to the mesoabdomen (such as occured in the Symphypleona).
These conditions can be recognised in the Neelipleona.
Note the ventrally infolded midgut of Megalothorax minimus, an adaptation required to support the strong downwards curvature of the abdomen (Willem 1900:Pl.XV,Fig.11). The Neelipleona combine a number of primitive characters, such as very short antennae, subdivided dens and 2 + 2 prelabral setae as in arthropleone collembolans (Bretfeld, 1999:15-16). These are an indication that the Neelipleona are early descendants of an ancient group. Robertson (2001) confirms the paraphyletic relationship between Neelipleona and Symphypleona based on morphological and molecular data. Schneider & al. (2011) confirms the monophyly of Neelipleona. Yu & al. (2016) found a close relationship between Neelipleona and Poduromorpha. The small proabdomen constrains the further development of the furca and correspondingly the overal trunk and body size. Neelipleona are typically very small to small Collembola.

The enlargement of the furca developed synchroneous with the enlargement of the furcal muscles and the development of the secondary intersegmental flexor muscles. The larger furcal muscles have a direct impact on the overall shape of the body: to accomodate the larger muscles, the relative size of the abdomen increased. To compensate for the longitudinal strain, caused by the furcal flexor muscles, the mesoabdominal terga tend to elongate while the mesoabdominal sterna tend to shorten.

Fig.pT. Schematic geometric model of tomoceromorphan body segmentation
Janssens, F. 2001.
The Pantomoceromorpha, the plesiomorph descendants of the Neocollembola, developed a larger furca and in line with that enlarged both the pro- and mesoabdomen. The larger furca and associated larger furcal muscles induce enlargement of both the proabdomen and mesoabdomen. The enlargement of the abdomen changed the body segmentation proportionally: the body/abdomen ratio became about 2/1 and the thoracic and abdominal segments became more equally sized. This condition is typically found in the Tomoceromorpha. In the Tomoceromorpha, the elongation of the mesoabdominal terga has been realised by enlargement of the anterior mesoabdominal tergum, the third abdominal tergum.
In the Panentomobryomorpha, the apomorph descendants of the Pantomoceromorpha, the elongation of the mesoabdominal terga has been realised by enlargement of the posterior mesoabdominal tergum, the fourth abdominal tergum.

In the Euentomobryomorpha, the plesiomorph descendents of the Panentomobryomorpha, to compensate for the increased antero-posterior tension of the intersegmental furcal flexor muscles, the proabdomen increases proportionally and the trunk curves slightly dorsoventrad.

Fig.Ess. Schematic geometric model of euentomobryomorph body segmentation
Janssens, F. 2001.

In the Euentomobryomorpha, the plesiomorph descendants of the Panentomobryomorpha, due to the strong proabdomen, the dorsoventrad curvature is relatively small, resulting in a comma-shaped lateral habitus.
Note that as a secondarely derived character, in the Euentomobryomorpha (more in particular, in the Microfalculidae and in some Isotomidae), the furca can be vestigial up to absent, reducing correspondingly the trunk curvature even more.

In the apomorph descendents of the Panentomobryomorpha, group 2, the third and fourth abdominal segments are enlarged, with correspondingly empowered function of the furca.

In the Coenaletidae, the plesiomorph descendents of group 2, due to the united furcal segments, the third and fourth abdominal segment, the furca is well developed. The male has characteristic grasping antennae used during courtship rituals.

Fig.S. Schematic geometric model of symphypleone body segmentation
Janssens, F. 2001.
The apomorph descendents of group 2 continued to develop an even larger furca due to the fusion of more abdominal segments and even thoracic segments. The furca and associated body curvature reaches its maximum development. The antero-posterior tension of the intersegmental flexor muscles and corresponding abdominal curvature becomes that large that the overall body requires a rotation around the dextro-sinistral axis to compensate the abdominal downwards curvature. To compensate for this body rotation the metaabdomen requires a more prominent upwards rotation relative to the mesoabdomen. The 'uplifted' meso- and metathorax in combination with the strongly downwards curved abdominal segments result in an overall body shape that resembles an inverse 'U'. The body length is effectively reduced. This condition is typically found in the Symphypleona.
In both Mackenziellidae and Sminthurididae the male has modified grasping antennae, as in Coenaletidae.
Note that as a secondarely derived character, more in particular, in the Mackenziellidae, the furca is reduced, reducing correspondingly the trunk curvature and reducing also the globular shape of the trunk.
Note that the midgut of e.g., Sminthurides aquaticus is typically curved upwards - dorsally - (Willem 1900:Pl.XI,Fig.3), an indication of the upwards curvature of the pre-symphypleone trunk.
The globular body shape of the Symphypleona is realised in a completely different way than in the Neelipleona: by the strong upwards curvature and the latero-ventral broadening of the trunk segments. The tergal intersegmental conjuctivae get stretched up to such an extend that the segment limits are not recognisable anymore dorsally. The trunk gets the appearance of a blown-up balloon.
Note that the symphypleone trunk segments are not fused, contrary to the long-established taxonomical terminology used with respect to symphypleone trunk segmentation (e.g. D'Haese, 2003:564).
Note that the hypognathy of the head of the Symphypleona is the result of the body rotation around the dextro-sinistral axis. We do not agree with Salmon's phylogeny (Salmon, 1964:99-103), who considered the orientation of the head axis as an early stage in the morphological processes of specialisation which lead to the Symphypleona.

Conclusion

The rather straightforward ordinal phylogeny that is proposed here is based on a dichotomic phylogeny of the progressively increasing function of the furca. It is assumed that in the protocollembola the furca is not well developed. Initially, it is small: a furcula. The Poduromorpha is the oldest group that specialised this small furca. The furcula reduced even further in size in stead of that it developed. In some species it even disappeared. However, others specialised in increasing the furcula: the 'higher' Collembola, the Neocollembola, characterised with a vestigial protergite. The larger furca has an effect on the overall shape of the body: it becomes dorso-ventrally curved due to the large antero-posterior muscles that spring-load the furca. The larger furca is realised according to two different bodyplans. In the first scheme, the larger furcal flexing muscles are accomodated by the third abdominal segment. In these Tomoceromorpha, the body curvature is minimal and the body is almost tubular. In the second scheme, the Panentomobryomorpha, the larger furcal flexing muscles are accomodated by the fourth abdominal segment. The Neelipleona with a strongly curved body are here considered as the most ancient and therefore basal group of the Neocollembola. In the Euentomobryomorpha, the curvature is typically resulting in a comma-shaped lateral habitus. Note that as a derived character, in the Euentomobryomorpha, the furca can be reduced up to absent, reducing correspondingly the body curvature. The Coenaletidae are an intermediate form between the elongate Euentomobryomorpha and the subglobular Symphypleona. In the Symphypleona the body curvature reaches its maximum development: the last thoracic segments and first four abdominal segments are curved upwards to such an extent that they resemble the shape of an inverse 'U', reducing effectively the body length.

Notes
1 From the Greek 'metaxy' meaning 'found in the middle' or 'between'.

References