http://www.collembola.org/publicat/crustacn.htm - Last updated on 2017.02.23 by Frans Janssens
Checklist of the Collembola: Are Collembola terrestrial Crustacea?

Frans Janssens, Department of Biology, University of Antwerp, Antwerp, B-2020, Belgium
Peter Nolan Lawrence, 9 Weald Close, Bromley Common, Kent, BR2 9PD, UK

Introduction

Although morphological features of Collembola do not support a close relationship with Crustacea, the molecular evidence for a 'crustacean-like' ancestor of Collembola and other 'hexapods' is compelling (Hopkin, 1997:21-22).
Traditionally, a semi-aquatic origin of Collembola has been proposed (Shear & Kukalová-Peck 1990, 1991 cited from D'Haese 2002:1143).
Hopkin (1997:26) presents the following random list of events that may have taken place during the evolution of terrestrial Collembola from a hypothetical aquatic, many-segmented, many-legged, crustacean-like ancestor:
- the second antennae were lost as they were no longer needed for swimming (as occured also in oniscidian isopods in their transition to land).
- the number of segments was reduced until only the head and the three thoracic and six abdominal segments remained.
- the legs on the thoracic segments were retained.
- the legs of the fourth abdominal segment were modified to form the furca.
- the legs of the third abdominal segment were reduced and became the tenaculum that holds the furca in rest position.
- the legs of the first abdominal segment developed thiny-walled vesicles and evolved into the ventral tube.
- the legs on the second, fifth and sixth abdominal segments were suppressed.

However, D'Haese (2002:1150) rejects the semi-aquatic origin of Collembola. The semi-aquatic lifestyle is a secondary acquisition that occured several times independently in the evolution of Collembola. An edaphic lifestyle is the ancestral state.

While there is consensus that Arthropoda is monophyletic, there is none on the relationships of its subordinates. Almost every possible alternative has been offered (Giribet & Ribera, 2000:205):
Arthropoda = Chelicerata + Mandibulata (Crustacea + Atelocerata (Myriapoda + Hexapoda)) according to Snodgrass, 1938; Weygoldt, 1979; Wågele, 1993; Wheeler et al., 1993; Wheeler, 1995, 1998 (cited from Giribet & Ribera, 2000:205).
Arthropoda = Chelicerata + Mandibulata (Myriapoda + Pancrustacea (Crustacea + Hexapoda)) according to Giribet et al., 1996; Giribet & Ribera, 1998; Zrzavy et al., 1998 (cited from Giribet & Ribera, 2000:205).
Arthropoda = (Chelicerata + Myriapoda) + Pancrustacea (Crustacea + Hexapoda) according to Turbeville et al., 1991; Friedrich & Tautz, 1995; Giribet et al., 1996 (cited from Giribet & Ribera, 2000:205); Dove & Stollewerk, 2003.
Arthropoda = Schizoramia (Chelicerata + Crustacea) + Atelocerata (Myriapoda + Hexapoda) according to Cisne, 1974; Briggs et al., 1992; Budd, 1993 (cited from Giribet & Ribera, 2000:205).

Many studies unite Crustacea and Atelocerata in the Mandibulata (Snodgrass, 1938; Weygoldt, 1979; Wågele, 1993; Wheeler et al., 1993; Wheeler, 1995,1998; Giribet et al., 1996; Giribet & Ribera, 1998; Zrzavy et al., 1998). Others align Crustacea with Chelicerata in the Schizoramia (Cisne, 1974; Briggs et al., 1992; Budd, 1993). Supporters of Mandibulata do not agree whether Atelocerata is monophyletic and sister of Crustacea (the traditional and majority position), or whether Crustacea is sister of Hexapoda (the Pancrustacea hypothesis). For a comprehensive overview of the rival hypotheses, see Giribet & Ribera (2000:222-225). Given the conflicting morphological (Atelocerata), molecular (Pancrustacea) and paleontological (Schizoramia) hypotheses, only a simultaneous analysis of all data from extinct and extant taxa might offer a solution (Giribet, Edgecombe & Wheeler, 1999:197).
A comprehensive review of the phylogeny of hexapods based on molecular data, the methods of data collection and analysis, and the conflict areas between molecular and morphological phylogenies is given by Carapelli, Nardi, Dallai & Frati (2006:191-204).

Any direct relationship between Hexapoda and Myriapoda is becoming more and more doubtful and therefore the polyphyly of Atelocerata seems increasingly certain (Dove & Stollewerk, 2003). As more nuclear, mitochondrial gene order and protein-encoding gene data have been examined for an ever-wider set of taxa, little or no support has been found for any of the possible groupings alternative to Pancrustacea (Cranston & Gullan, 2003:883). In this paper, we will question whether or not Collembola are Insecta, Hexapoda or Crustacea within the context of the Pancrustacea theory. Hexapody originated at least twice independantly in Arthropoda, making the Hexapoda paraphyletic (Nardi et al., 2003; Cook et al., 2005). We will show that Collembola are not so called primitive apterous insects, but a unique and ancient group of well adapted terrestrial crustaceans. For this reason, Lawrence (2003:I) proposes the nomen novum Gillopoda for the Collembola Lubbock, 1870.

Paleontological considerations

Fig.r. Rhyniella praecursor
After Scourfield (1940).
Fig.r2. Rhyniella praecursor
After Anonymous (2017).
Based on the discovery of the fossil collembolan Rhyniella praecursor (Fig.r, r2) by Hirst & Maulik in the Devonian chert beds in Scotland in 1926, and the striking resemblance it shows with extant species, Tillyard (1928) concludes that Collembola are primary, ancestral, and archaic terrestrial arthropodans and not forms readapted by retrograde evolution as claimed by Handlirsch (1908) (cited from Handschin, 1955:41,49).
Rhyniella praecursor Hirst & Maulik, 1926 has been assigned to different families, respectively to Poduridae (Poduromorpha) by Tillyard (1928), to Entomobryomorpha, possibly Protentomobryidae by Scourfield (1940), to Rhyniellidae by Paclt (1956), to Protentomobryidae by Salmon (1964), to Neanuridae by Massoud (1967), and to Isotomidae by Greenslade & Whalley 1986:320.
Crowson (1985) questioned whether or not the Rhyniella fossils are recent contaminations, because of the finding of a thysanopteran nymph in the deposit which was clearly a later contaminant. However it has been shown that the Collembola are securely embedded in the rock and that there was only a single phase of mineralisation (Whalley & Jarembowski, 1981 cited from Greenslade & Whalley 1986:319). Most recent dating using argon/argon techniques have confirmed the chert as being over 400 million years old (Greenslade & Whalley 1986:319).
Direct fossil evidence of Collembola before the Devonian is lacking (Lehmann & Hillmer, 1983 cited from Hopkin, 1997:23).
The discovery of coprolites (fossil faeces) in Upper Silurian rocks of 412 million years in age, which could be derived from springtails, suggests that Collembola were an important component of the earliest terrestrial ecosystems (Edwards, Selden, Richardson & Axe, 1995 cited from Hopkin, 1997:23).

Fig.Db. Devonohexapodus bocksbergensis
After Haas, Waloszek & Hartenberger (2003) Fig.6B.

Hexapody did not evolve as an adaptation to terrestrial locomotion, but was already developed in the marine habitat, as demonstrated by the ectognathous marine hexapod Devonohexapodus bocksbergensis (Fig.Db) from the Lower Devonian Hunsrück Slates (Haas, Waloszek & Hartenberger, 2003:39,46). This finding demonstrates that stem lineage Insecta coexisted during the Devonian with the more derived Collembola (Haas, Waloszek & Hartenberger, 2003:52). Cambronatus brasseli and Wingertshellicus backesi from the Lower Devonian, are described by Briggs & Bartels (2001) as "crustaceanomorphs", while Haas, Waloszek & Hartenberger (2003:49) suggest a close relationship to Hexapoda. The marine Tesnusocaris goldichi Brooks, 1955, from the Carboniferous, redescribed by Emerson & Schram (1991) as a representative of the Remipedia, is condsidered to be more close to Hexapoda by Haas, Waloszek & Hartenberger (2003:49).

A key problem to the origin of hexapods is the almost complete absence of fossils that connect hexapods to the other major arthropod subphyla, namely Crustacea, Myriapoda, and Chelicerata. The last common ancestor of hexapods and branchiopods may have originated in freshwater during the Late Silurian, giving rise to extant freshwater dwelling branchiopods (fairy shrimps, water fleas, and tadpole shrimps) and insects. This hypothesis accounts for the missing fossil record of branchiopods and hexapods before the Devonian. Crustacean fossils are recorded at least as far back as the Upper Cambrian, about 511 million years ago, where they are found in marine sediments. However, except for the debated Devonohexapodus bocksbergensis specimen, all hexapod remains are found only in freshwater or terrestrial strata no earlier than the Devonian, around 410 million years ago. This leaves a gap of 100 million years to the earliest crustaceans. (Glenner, Thomsen, Hebsgaard & Sorensen, 2006:1883). The early marine ancestor of the hexapods might have appeared more similar to Rehbachiella kinnekullensis, a close marine relative to branchiopods from the Upper Cambrian, than to D. bocksbergensis or other hexapods. (Glenner, Thomsen, Hebsgaard & Sorensen, 2006:1884).

Reinterpretation of a fossil insect fragment Rhyniognatha hirsti Tillyard, 1928 from the early Devonian Rhynie cherts of Scotland indicates that insects originated in the Silurian period (Engel & Grimaldi, 2004:627-630). This is supported by the fossil records of Archaeognatha (= Microcoryphia) that have been listed from the early Devonian of Quebec (Labandeira & al., 1988 cited from Bach de Roca, Gaju-Ricart & Compte-Sart, 1999:387) and from the Devonian of New York (Shear & al., 1984 cited from Bach de Roca, Gaju-Ricart & Compte-Sart, 1999:387), suggesting a parallel evolution of Insecta and Collembola. Rhyniella praecursor Hirst & Maulik, 1926, the oldest known collembolan fossil from the Devonian red sandstone Rhynie chert beds, Scotland, resembles extant Collembola up to such an extent that this might be an indication that Collembola reached their evolutionary climax already 400 million years ago. Therefore, Handschin (1955:49) considers Collembola as living fossils.

In a molecular study of the evolution of the mitochondrial cytochrome oxidase II gene of Collembola was shown that values of genetic distance between congeneric species and between families were remarkably high; in some cases the latter were higher than divergence values between orders of insects. The remarkably high divergence levels observed provide evidence that Collembola taxa are quite old; divergence levels among Collembola families equaled or exceeded divergences among pterygote insect orders. (Frati, Simon, Sullivan & Swofford, 1997:145,152).

Systematic overview

Pancrustacea
Crustacea Hexapoda (= Insecta sensu Leach, 1815)
Apterygota (Pterygota)
Entognatha Insecta sensu Handschin, 1958 (= Ectognatha sensu Hennig, 1953)
Monocondylia Dicondylia
Ellipura Diplura Thysanura sensu Lameere, 1895 Pterygota
Collembola Protura Archaeognatha Zygentoma
Tab.I. Conventional classification of related and higher taxa of Collembola,
in perspective of the Pancrustacea theory.
(Monophyletic taxa in bold. Paraphyletic assemblages not in bold)

Historically, single morphological character systems formed the basis for organising the hexapods into groups (Carpenter & Wheeler, 1999:333,344). Since the characters taken into account in such studies are independent of each other, each study results in a different phylogeny. Combining sets of independent characters into one study is the approach of the 'total evidence' of Kluge (1989) and 'simultaneous analysis' of Nixon and Carpenter (1996) to maximise parsimony of the tree (Carpenter & Wheeler, 1999:333,344). Given the high number of characters involved, a numerical cladistic analysis will simplify the work. Computer assisted analyses allow for combining a hugh amount of characters (morphological, molecular, ecological, physiological, etc.) to be taken into account simultaneously, allowing in this way simultaneous treatment of all available evidence. In the following discussion, the single character based groupings that lead to taxonomic units used in the systematic classifications are questioned by integrating manually the result of many single and multiple character studies in an attempt to confront the different opinions preliminary.

Are Collembola Ellipura?

Ellipura Börner, 1910 = Collembola + Protura (cited from Pass & Szucsich, 2011:318; cited from Dell'Ampio, Szucsich & Pass, 2011:347).
Parainsecta Kukalová-Peck, 1991 (cited from Bach de Roca, Gaju-Ricart & Compte-Sart, 1999:387) = Ellipura Börner, 1910.

Are Collembola Entognatha?

Entognathi(sic) von Stummer-Traunfels, 1891 (cited from Börner, 1901:3,11) = Collembola + Entotrophi(=Diplura)
Entognatha Snodgrass, 1938 (cited from Wheeler, Whiting, Wheeler & Carpenter, 2001:114) = Collembola + Protura + Diplura
Entognatha Imms, 1948:221 nec von Stummer-Traunfels, 1891 = Diplura
Entognatha Hennig, 1969 (cited from Sekiya & Machida 2011:399) = Collembola + Protura + Diplura
Entognatha Kukalová-Peck, 1991 (cited from Bach de Roca, Gaju-Ricart & Compte-Sart, 1999:387) nec von Stummer-Traunfels, 1891 = Diplura
Entognatha Kukalová-Peck, 1998 (cited from Bach de Roca, Gaju-Ricart & Compte-Sart, 1999:393) nec von Stummer-Traunfels, 1891 = Diplura
Entognatha Koch, 1997 (cited from Bach de Roca, Gaju-Ricart & Compte-Sart, 1999:393) nec von Stummer-Traunfels, 1891 = Diplura
Entognatha Koch, 1998 (cited from Bach de Roca, Gaju-Ricart & Compte-Sart, 1999:393) nec von Stummer-Traunfels, 1891 = Diplura

Are Collembola Apterygota?

Apterygota Lang, 1889 (cited from Imms, 1948:211) = Collembola + Thysanura(=Diplura+Archaeognatha+Zygentoma).
Apterygota Imms, 1948:213 = Apterygota Lang, 1889 + Protura.
Apterygota Kukalová-Peck, 1991 (cited from Bach de Roca, Gaju-Ricart & Compte-Sart, 1999:387) nec Lang, 1889 = Zygentoma.

Are Collembola Insecta?

Insecta Linnaeus, 1758 (cited from Kluge, 1999:348,369) = Arthropoda von Siebold & Stannius, 1848.
Amyocerata Remmington, 1955 (cited from Kluge, 1999:348,369) = Triplura(=Archaeognatha+Zygentoma) + Pterygota.
Insecta Handschin, 1958 (cited from Kluge, 1999:348,369) nec Linnaeus, 1758 = Amyocerata Remmington, 1955.
Insecta Kukalová-Peck, 1987 (cited from Giribet, Edgecombe & Wheeler, 1999:203) nec Linnaeus, 1758 = Insecta Handschin, 1958 + Diplura.
Insecta Kukalová-Peck, 1991 (cited from Bach de Roca, Gaju-Ricart & Compte-Sart, 1999:387) nec Linnaeus, 1758 = Insecta Kukalová-Peck, 1987 + Monura.
Insecta Kristensen, 1991 (cited from Bach de Roca, Gaju-Ricart & Compte-Sart, 1999:389) nec Linnaeus, 1758 = Kukalová-Peck, 1991 - Diplura.

Are Collembola Hexapoda?

Hexapoda Blainville, 1816 (cited from Kluge, 1999:348,369) = Insecta Leach, 1815 nec Linnaeus, 1758.
Hexapoda Koch, 1997 (cited from Bach de Roca, Gaju-Ricart & Compte-Sart, 1999:391) = Insecta Kukalová-Peck, 1987 + Collembola + Protura.
Insecta Larink, 1997 (cited from Bach de Roca, Gaju-Ricart & Compte-Sart, 1999:391) nec Linnaeus, 1758 = Insecta Kukalová-Peck, 1991 + Collembola + Protura.
Insecta Buckley & Cunningham, 2002:395,399

Are Collembola Crustacea?

Are Collembola Pancrustacea?

Exploring possible extra-pancrustacean ancestries of Collembola:

Do Collembola share characters with Arachnata?

Applying the Pancrustacea hypothesis to the definition of Arthropoda according to Cisne, 1974; Briggs et al., 1992; Budd, 1993 (cited from Giribet & Ribera, 2000:205): Myriapoda + Schizoramia (Arachnata + Pancrustacea), we will now summarise some arachnomorph characters in Collembola.

Collembola basic ground pattern

In the basic ground pattern of Collembola, the body is comprised of the frontal acron, followed by 15 true segments and terminated by the telson. All true body segments bear appendages. The segments are organised in 2 primary tagmata: the head and the trunk. The head is a composite of the acron fused with the 6 anterior body segments (1). Each of the head segments bears a pair of appendages, respectively the lateral composed eyes, the antennae, the post-antennal organs, the mandibulae, the maxillae and the cleft bipartite labium. The first 3 antennal segments bear intrinsic muscles (after Imms, 1939:292-296). The mouth opening is located ventrally between the antennal and mandibular segments. The trunk has 9 limb bearing segments. The limbs of the 5th, 8th and nineth trunk segment, although present in the early stages of the embryo, are completely reduced in the adult. Also the telson is only present in the early embryonic stages (fig.Xg). (3) The gonopore is located ventrally at the 8th trunk segment. The anus opens terminally at the nineth trunk segment.

The trunk is secondarily divided in two subtagmata: the thorax and abdomen. (2) The thorax comprises 3 thoracic segments. The abdomen comprises 6 segments. Embryonic studies show that the 6 abdominal segments are not the result of a reduction of segments. The appendages of the thoracic segments are adapted for locomotion. The appendages of the abdominal segments are specialised and fused at their basis. The first abdominal appendage is the collophore or ventral tube. The second abdominal appendage is only present in the embryo. The third abdominal appendage is the retinaculum. The fourth abdominal appendage is the furcula. Both retinaculum and furcula form a springing device that can be secondarily reduced in many species of Collembola. The fifth and sixth abdominal appendages are only present in the embryo (fig.Xg).
Fig.Ti. Tomocerus ishibashii, embryo stage 3, cephalic ganglia.
Modified after Uemiya (1991:127,fig.2).

(1) In Tomocerus ishibashii the protocerebrum consists of three pairs of ganglia (Lobes 1-3). Lobe 3 is regarded as the ganglion of the preantennal segment. The deutocerebrum is derived from the antennal, and the tritocerebrum from the intercalary ganglia. The tritocerebrum retains the original postoral position throughout the life cycle. The ventral nerve cord consists of 10 pairs of ganglia derived from the mandibular to the fourth abdominal segments. The metathoracic and four abdominal ganglia fuse to form a synganglion during embryogenesis. (Uemiya, 1991:127).
In stage 2, the ectoderm of the protocephalon situated anteriorly to the antennal segment is divided into two layers. The outer layer develops into the future epidermis and ommatidia, and the inner one develops into the anlagen of protocerebral ganglia. In stage 2, the inner layer is divided into three paired parts (lobes 1, 2 and 3). The lobe 3 is located just anteriorly to the antennal segments, and the lobes 1 and 2 are situated in each side lateral to the lobe 2. The protocerebrum originates from these three paired lobes. The lobe 1 develops into the future optic ganglion. According to Tyszkiewicz 1976, the lobe 1 is not formed in Tetrodontophora bielanensis. It may reflect the fact that the ommatidia are lacking in this species. (Uemiya, 1991:131).

Fig.Xg. Xenylla grisea embryo stained for Dll.
Modified after Palopoli & Patel (1998:588,fig.1c).

(2) The terminology used when comparing tagmata of hexapodans and crustaceans is quite confusing. In Crustacea, the thorax comprises all post-cephalic limb bearing body segments, while the abdomen consists of primary limbless body segments. In Collembola, the thorax comprises only the first three post-cephalic body segments, while the remaining body segments make part of the abdomen. In a pancrustacean context one could state that the (pan)crustacean thorax 'comprises' both the collembolan thorax and abdomen. Put otherwise: Collembola lack a (pan)crustacean abdomen.

(3) Palopoli & Patel (1998:588) used antibody staining in embryo's of Xenylla grisea for Distal-less (Dll) proteins (a well studied Hox regulatory target that is required for the development of distal limb structures) (see fig.Xg). In the ventral view of the posterior thorax and complete abdomen of an embryo, at approximately 40-50% of embryogenesis, each abdominal appendage primordium was stained black for Dll protein (arrows). The staining in the very posterior of the abdomen was not addressed in the study Palopoli & Patel. The black staining in the fifth (A5) and sixth (A6) abdominal segments is interpreted in this paper as primordia of embryonic appendages, revealing in this way the ancestral state of the Collembola body plan. Also the primordia of the ancestral crustacean rami of the telson (T) are still present in the embryo.

Pancrustacean perspective on Collembola

CollembolaHeadThoraxAbdomenTelson
Acron1a1b1c23456123123456
"Neotenic Malacostraca like"
ancestor of Collembola
HeadThoraxTelson
PereonPleon
Acron123456123456781
Basic body plan segmentation of Collembola compared with hypothetical crustacean ancestor
Segment numbers in red color indicate the location of the gonopore.

In several recent molecular studies, Collembola are clustered with Malacostraca (Spears & Abele, 1997 cited from Lange & Schram, 1999; Aleshin & Petrov, 1999; Gibiret & Ribera, 2000:213,215,216,217,218) or closely related to them (Carapelli, Liò, Nardi, van der Wath, & Frati, 2007). These results seem to be confirmed by morphological comparison of their respective body plans.
In the ground pattern of Malacostraca (Phyllocarida) (fig.h.A), the head bears 5 appendages (Walossek & Müller, 1997:151). Lateral compound eyes are present (segment 1) (Walossek & Müller 1998:221). The first antenna comprises a 3-segmented peduncle with intrinsic muscles, bearing a pair of annulated flagelliform rami. (after Imms, 1939:315). The trunk is divided in 3 tagmata: thorax 1 (pereon) with 8 limb bearing thoracomeres, thorax 2 (pleon) with 6 limb bearing thoracomeres and the abdomen with one primary limbless segment. The female gonopore is located at the sixth pereonic segment. The male gonopore is located at the 8th pereonic segment. The anus is located terminally at the telson bearing the furca. (Walossek & Müller 1998:220).

Given the basic Collembola ground plan, the basic ground pattern of a hypothetical crustacean ancestor of Collembola can be deduced as follows (fig.h.B):
A head with lateral compound eyes and 5 appendages. A trunk with 2 tagmata: thorax 1 (pereon) with 8 limb bearing thoracomeres, and thorax 2 (pleon) with one limb bearing thoracomere. Primary limbless abdominal segments are lacking. The gonopore opens at the 8th thoracomere. The anus opens terminally at the telson bearing the furca.

Comparing both ground patterns of Malacostraca and the hypothesised crustacean predecessor of Collembola suggest that Malacostraca are a more derived form and that the crustacean predecessor of Collembola can act as predecessor of the Malacostraca as well. This complies with studies that place Collembola more at the base of Crustacea, such as Aleshin & Petrov (1999:184,185), Gibiret & Ribera, (2000:214), Nardi et al. (2003) and Giribet & al (2004:327).

Fig.h. Hypothesis on crustacean predecessor of Collembola.
Modified after Walossek & Müller (1997:151).

Konopova & Akam (2014:9) showed in Orchesella cincta that the Hox genes Ultrabithorax (Ubx) and abdominal-A (abd-A) are expressed in abdominal segments, and that they specify the abdominal appendages. When both Ubx and abd-A are suppressed, the abdominal appendages are replaced by walking legs (the more ancestral appendages). This is support for the hypothesis that the abdomen of Collembola is derived from the thorax (the pereon) of its crustacean ancestor.

Discussion

Conventional hypothesis: Collembola are basal Hexapoda.
Pancrustacea
Crustacea
Hexapoda s.l.
Collembola Protura Diplura Insecta s.s. (= Ectognatha)
Archaeognatha
(= Monocondylia)
Dicondylia
Zygentoma Pterygota
Tab.II. Classification of related and higher taxa of Collembola.


		+---------- Insecta s.s. 
	     +--+
	     |  +---------- Diplura
	  +--+
	  |  |  +---------- Protura
	  |  +--+
	  |     +---------- Collembola
       +--+
       |  +---------------- Crustacea
    +--+
    |  +------------------- Myriapoda
 ---+
    +---------------------- Chelicherata

Fig.1. Simplified scheme of the systematic position of
Collembola in the Arthropoda
(conventional phylogeny)

Alternative hypothesis: Collembola are terrestrial Crustacea.
Pancrustacea
Crustacea s.l.
Hexapoda s.s.
Crustacea
s.s.
Collembola Protura Diplura Insecta s.s. (= Ectognatha)
Archaeognatha
(= Monocondylia)
Dicondylia
Zygentoma Pterygota
Tab.III. Classification of related and higher taxa of Collembola.
(modified after Shao, Zhang, Ke, Yue & Yin, 2000)


		    +------ Hexapoda s.s. 
		    |
	     +------------- Collembola
	     |      |
       +-----+------+------ Crustacea
    +--+
    |  +------------------- Myriapoda
 ---+
    +---------------------- Chelicherata

Fig.2. Simplified scheme of the systematic position of
Collembola in the Arthropoda
(modified after Shao, Zhang, Ke, Yue & Yin, 2000)

Alternative hypothesis 2: Collembola are terrestrial basal Crustacea.
Pancrustacea
Crustacea s.l.
Hexapoda s.s.
Crustacea
in pars
(Branchiopoda)
Collembola
Crustacea
in pars
(Malacostraca)
Protura Diplura Insecta s.s. (= Ectognatha)
Archaeognatha
(= Monocondylia)
Dicondylia
Zygentoma Pterygota
Tab.IV. Classification of related and higher taxa of Collembola.
(modified after Spears & Abele, 1997 cited from Lange & Schram, 1999; Aleshin & Petrov, 1999; Gibiret & Ribera, 2000:213,215,216,217,218)


		     +----- Hexapoda s.s. 
		     |
		 +---+----- Crustacea partim 
		 |
	     +------------- Collembola
	     |   |
       +-----+---+--------- Crustacea partim 
    +--+
    |  +------------------- Myriapoda
 ---+
    +---------------------- Chelicherata

Fig.3. Simplified scheme of the systematic position of
Collembola in the Arthropoda
(modified after Spears & Abele, 1997
cited from Lange & Schram, 1999; Aleshin & Petrov, 1999;
Gibiret & Ribera, 2000:213,215,216,217,218)

New hypothesis: Collembola are terrestrial basal Pancrustacea.
Pancrustacea
Collembola
Crustacea
Hexapoda s.s.
Protura Diplura Insecta s.s. (= Ectognatha)
Archaeognatha
(= Monocondylia)
Dicondylia
Zygentoma Pterygota
Tab.V. Classification of related and higher taxa of Collembola.
(modified after Aleshin & Petrov, 1999:184,185; Gibiret & Ribera, 2000:214; Nardi et al., 2003)


	     +------------- Hexapoda s.s. 
	  +--+
	  |  +------------- Crustacea
       +--+
       |  +---------------- Collembola
    +--+
    |  +------------------- Myriapoda
 ---+
    +---------------------- Chelicherata

Fig.4. Simplified scheme of the systematic position of
Collembola in the Arthropoda
(modified after Aleshin & Petrov, 1999:184,185;
Gibiret & Ribera, 2000:214; Nardi et al., 2003)

New hypothesis 2: Collembola are terrestrial basal Pancrustacea (Hexapoda rejected).
Protura Diplura Pancrustacea
Collembola
Crustacea
Insecta s.s. (= Ectognatha)
Archaeognatha
(= Monocondylia)
Dicondylia
Zygentoma Pterygota
Tab.VI. Classification of related and higher taxa of Collembola.
(modified after Giribet & al., 2004:327)


	     +------------- Ectognatha  
	  +--+
	  |  +------------- Crustacea
       +--+
       |  +---------------- Collembola
    +--+
    |  +- - - - - - - - - - Chelicherata 
 ---+
    |                +----- Diplura
    +----------------+
    |                +----- Protura
    |
    +---------------------- Myriapoda


	  +---------------- Ectognatha  
	  |
       +--+---------------- Collembola
       |  |
       |  +---------------- Crustacea
    +--+
    |  +- - - - - - - - - - Chelicherata 
 ---+
    |                +----- Diplura
    +----------------+
    |                +----- Protura
    |
    +---------------------- Myriapoda

Fig.5. Simplified schemes of the systematic position of
Collembola in the Arthropoda
(modified after Giribet & al., 2004:327)

New hypothesis 3: Collembola are terrestrial Maxillopoda (Hexapoda rejected, Crustacea rejected).
Pancrustacea
Pancrustacea type 1 Pancrustacea type 2
Crustacea
(Maxillopoda)
Collembola Protura Diplura
Crustacea
(Branchiopoda
Malacostraca)
Insecta s.s. (= Ectognatha)
Archaeognatha
(= Monocondylia)
Dicondylia
Zygentoma Pterygota
Tab.VII. Classification of related and higher taxa of Collembola.
(modified after Cook, Yue & Akam, 2005:1300; Luan & al., 2005:1584; Newman, 2005; Glenner & al, 2006:1883)


	  +---------------- Ectognatha  
       +--+
       |  +---------------- Crustacea (Branch. + Mal.)
       |
       |             +----- Diplura
    +--+     +-------+
    |  |  +--+       +----- Protura
    |  |  |  |
    |  +--+  +------------- Collembola
    |     |
    |     +---------------- Crustacea (Max.)
    |
    +---------------------- Myriapoda
 ---+
    +---------------------- Chelicherata

Fig.6. Simplified scheme of the systematic position of
Collembola in the Arthropoda
(modified after Cook, Yue & Akam, 2005:1300; Luan & al., 2005:1584; Newman, 2005; Glenner & al, 2006:1883)

New hypothesis 4: Collembola are basal terrestrial Panthoracopoda (Hexapoda rejected, Crustacea rejected).
Pancrustacea
?
Protura
?
Crustacea
(Maxillopoda + Remipedia)
{+ Diplura ?}
Panthoracopoda
Japyx ?
Collembola
Crustacea
(Thoracopoda partim 2 = Branchiopoda)
Crustacea
(Thoracopoda partim 1)
{+ Diplura ?}
Insecta s.s. (= Ectognatha)
Archaeognatha
(= Monocondylia)
Dicondylia
Zygentoma Pterygota
Tab.VIII. Classification of related and higher taxa of Collembola.
(modified after Kjer, 2004:511; Carapelli, Liò, Nardi, van der Wath, & Frati, 2007)


		   +------- Ectognatha  
		+--+
		|  +------- Crustacea (Thoracopoda partim 1)
	     +--+              + Diplura ?
	     |  +---------- Crustacea (Thoracopoda partim 2)
	  +--+
	  |  +------------- Collembola
       +--+
       |  +---------------- Crustacea (Maxillopoda + Remipedia)
    +--+                       + Diplura ?
    |  +- - - - - - - - - - Protura
    |
    +---------------------- Myriapoda
 ---+
    +---------------------- Chelicherata

Fig.7. Simplified scheme of the systematic position of
Collembola in the Arthropoda
(modified after Kjer, 2004:511; Carapelli, Liò, Nardi, van der Wath, & Frati, 2007)

Segment Arachnida Xiphosura Collembola Crustacea:
Malacostraca
Ectognatha Segment
Acron - - - - - Acron
1 (Lateral ocelli) Lateral ommatea (Lateral "ommatidia") (Lateral ommatea) (Lateral ommatea) 1
2 - - Antennae Antennulae Antennae 2
3a Rostrum part 1 Rostrum part 1 Embryonic intercalary appendages
(Post-antennal organ)
Labrum
Antennae
Labrum
Embryonic intercalary appendages
Labrum
3a
3b
Mouth opening
3b
3c Rostrum part 2 Rostrum part 2       3c
4 Chelicerae Chelicerae Mandibulae Mandibulae Mandibulae 4
5 Pedipalpae Pedipalpae Maxillae Maxillae Maxillae 5
6 Telopods tarsate Telopods chelate Cleft, bipartite labium Maxillae Labium 6
7 Telopods tarsate Telopods chelate Telopods unguiate Pereopods chelate Telopods tarsate 7
8 Telopods tarsate Telopods chelate Telopods unguiate Pereopods chelate Telopods tarsate 8
9 Telopods tarsate Telopods chelate Telopods unguiate Pereopods chelate Telopods tarsate 9
10-1 Embryonic segment 10-1 Chilaria 10-1 Collophore 10-1 Pereopods 10-1 Embryonic pleuropods 4
(Styli)
11-2 Embryonic appendages 11-2 Pereopods 11-2 (Styli)
12-3 (Styli)
13-4 (Styli)
14-5 (Styli)
15-6 (Styli)
16-7 (Styli)
11-2 Pectines g.o. 11-2 Opercula g.o. 12-3 (Retinaculum) 12-3 Pereopods g.o.f. 17-8 Gonophysae g.o.f.
13-4 (Furca) 13-4 Pereopods
14-5 Embryonic appendages2 g.o. 14-5 Pereopods g.o.m. 18-9 Gonophysae g.o.m.
12-3 Booklung 12-3 Opercula Bookgill 15-6 Pleopods 19-10 -
13-4 Booklung 13-4 Opercula Bookgill 16-7 Pleopods 20-11 Cerci
14-5 Booklung 14-5 Opercula Bookgill 17-8 Pleopods
15-6 Booklung 15-6 Opercula Bookgill 18-9 Pleopods
16-7 Booklung 16-7 Opercula Bookgill 19-10 Pleopods
17-8 - 20-11 Pleopods
18-9 - 17-1 Fossil segment 21-12 -
19-10 - 18-9 Fossil segment
20-11 - 19-10 Fossil segment
21-12 -
22-13 -
Telson a.o. Sting/whip/- - Embryonic appendages 2
Anal "valves" 3
Furca Anal lobes
Proctodaeum
Telson a.o.
Table IX. Schematic comparison of segmental bodyplan homologies in Arthropoda
(modified after Chamberlain, 1931:41; Störmer in Grassé, 1949:160-197; Weber, 1974:8,54,305; Leinaas, 1988:2833; Brusca & Bruca, 1990:608-609; Walossek & Müller, 1997:151; Palopoli & Patel, 1998:5882; Walossek & Müller 1998:220; Haas, Waloszek & Hartenberger, 2003:46; Oakley, 2003:524; Konopova & Akam, 2014:104)

Provisional conclusion

Collembola are difficult to position due to the discrepant results of morphological and molecular phylogenies; they are probably key taxa to explain arthropod relationships (Giberet & Ribera, 2000:225). The acceptance of nonmonophyly of Hexapoda s.l. implies that the tripartite and six-legged body plan typical of Hexapoda s.l. would be a convergent acquisition of Collembola, Protura, Diplura and Insecta s.s. Collembola diverged early from the ancestral pancrustacean line, and the development of a matching body plan with Protura, Diplura and Insecta s.s. is likely the result of homology rather than direct ancestry.

The recent discovery of the marine hexapod Devonohexapodus bocksbergensis Haas, Waloszek & Hartenberger, 2003:42-53 from the Lower Devonian challenges the traditional association between terrestralisation and hexapody, making room for alternative hypotheses concerning collembolan origins (Nardi et al., 2003:1482e). The recent phylogenetic analyses of molecular sequence data suggest a paradigm shift concerning the phylogenetic position of hexapods: that crustaceans successfully invaded land at least as insects. It is possible that when insects entered terrestrial habitats, their crustacean ancestors had already diversified in marine environments and occupied all potential niches, which could explain why insects were prevented from colonising the sea subsequently. (after Glenner, Thomsen, Hebsgaard & Sorensen, 2006:1884). The recent reinterpretation of a fragmentary insect fossil from the early Devonian Rhynie cherts of Scotland shows that the origin of insects is much earlier than conventionaly accepted (Engel & Grimaldi, 2004:627-630). This indicates that insects evolved independently in parallel with collembolans. This is confirmed by Newman (2005) who hypothesizes that the Ostracoda are close to the ancestor of the Hexapoda. Given the edaphic origin of Collembola (D'Haese, 2002), the collembolan ancestor must have completed the transition from marine aquatic habitats to littoral soil habitats already before the Lower Devonian.

The close relationship of Collembola and Malacostraca, is morphologically supported when comparing the body plans of malacostracan Phyllocarida and Collembola. This suggests the redefinition of the thorax concept, as known in Collembola, in their most recent common ancestor. The thorax of their predecessor apparently includes the abdominal segments of Collembola (including the anal segment) (see Table IX). In other words, the abdominal segments of Collembola are of ancestral malacostracan thoracic origin.

Acknowledgments

References