http://www.collembola.org/publicat/furca.htm - Last updated on 2009.01.05 by Frans Janssens
Checklist of the Collembola: Schematic Model of the Evolution of the Furcal Muscles

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

Abstract.
The evolution of the furcal muscles has impacted manifestly the general body shape in Collembola. The Poduromorpha are linear forms with reduced furcal muscles. The "Entomobryomorpha" are linear forms with well developed furcal muscles, realised in two schemes: 1. tomoceromorph linear forms with elongated third abdominal segment, and 2. euentomobryomorph comma-shaped forms with elongated fourth abdominal segment. Symphypleona are subglobular forms with well developed furcal muscles. Neelipleona are subglobular forms with reduced abdomen and are a remnant sistergroup of Euentomobryomorpha. Poduromorpha, such as Neanuridae, Onychiuridae and Tullbergiidae, with vestigial furcula, and Euentomobryomorpha, such as Microfalculidae and some Isotomidae, with a furcula are secondary regressive forms. The monospecific Mackenziellidae, Symphypleona with a furcula, is a remnant of a transitive form between Poduromorpha and Neocollembola.

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). In some Poduromorpha, it is larger then the other segments. In many entomobryomorph Collembola, the fourth abdominal segment is the largest segment of all. And in most Symphypleona, it is the fourth abdominal segment that contributes most to the enlargement of the trunk.

Basic morphological groups of Collembola

Poduromorpha. The Poduromorpha are characterised by: 1. the protergite being distinctly present, and 2. springing muscles situated in the fourth abdominal segment only (see fig. Pod.), and 3. secondarily an elongated and segmented habitus. The Poduromorpha are traditionally considered as being plesiomorphic (after Thibaud, Schulz & da Gama Assalino, 2004:3). In this work, they are considered apomorphic descendants of the protocollembolan ancestor having reduced springing muscles (see below).

Neocollembola. The "Entomobryomorpha", Neelipleona, and Symphypleona form a monophyletic grouping, the 'true' springtails with well developed furca, here called tentatively the Neocollembola (Nc in fig.1).
The Neocollembola, sister group of the Poduromorpha, are characterised by: 1. an absent protergite, and 2. springing muscles situated in the third and fourth abdominal segments (see fig. Neo.).

Tomoceromorpha. Xiong & al. (2008) confirm the findings of D'Haese (2002) that the superfamily Tomoceroidea is monophyletic.
Tomoceromorpha are characterised by: 1. an absent protergite, and 2. enforced springing muscles mainly situated in the third abdominal segment, due to the elongation of the third abdominal segment (see fig. Tom.).

Panentomobryomorpha. The sister group of Tomoceromorpha, tentatively called the Panentomobryomorpha (Fig. Tree:Pe), are characterised by: 1. an absent protergite, and 2. enforced springing muscles situated in the third and fourth abdominal segment, due to the elongation of the fourth abdominal segment (see fig. Pan.).

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. enforced springing muscles situated in the third and fourth abdominal segment, due to the enlarged fourth abdominal segment, 3. a ventral tube having two long eversible vesicles (see Fig. 2), and 4. secondarily a subglobular habitus.

Euentomobryomorpha. The Euentomobryomorpha are characterised by: 1. an absent protergite, 2. enforced springing muscles situated in the third and fourth abdominal segment, due to the enlarged fourth abdominal segment, 3. a ventral tube having two short eversible vesicles, which is considered plesiomorphic, since it is also found in Poduromorpha and Tomoceromorpha, and 4. a smooth midgut.

Neelipleona. The Neelipleona are characterised by: 1. an absent protergite, 2. enforced springing muscles situated in the third and fourth abdominal segment, due to the enlarged fourth abdominal segment, 3. a ventral tube having two short eversible vesicles, 4. a diverticulate midgut, and 5. secundarily a subglobular habitus.

Simplified model of the mesoabdominal furcal muscles

The development of the furca is closely related with the development of the furcal muscles and the mesoabdomen. The furcal muscles of the hypothetical collembolan ancestor 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. The levator muscles are not taking into account for the further discussion of the evolution of the body shape in function of the furcal muscles.
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.

At the moment of docking the furca in the retinaculum, the mesoabdominal antero-posterior 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.

Fig.Anc. Schematic diagram of muscles of ancestral legs
Janssens, F. 2008.
In the hypothetical ancestor of the Collembola, the mesoabdominal legs were still present and functional. In the simplified schematic model of the muscles involved in the formation of the overall body shape of Collembola, the muscles that operate the coxa of the leg, play a manifest important role. Both the promotor and remotor muscles are connected latero-tergally at the antecosta of their body segment. The promotor is connected at the anterior side of the leg and pulls the leg forwards. The remotor is connected at the posterior side of the leg and pulls the leg backwards.

Fig.Neo. Schematic diagram of furcal muscles in Neocollembola
Janssens, F. 2008.
In the Collembola, the ancestral mesoabdominal legs are mutated into the characteristic springing organ. The ancestral legs of the third abdominal segment are reduced and fused at the basis to form the retinaculum (not shown in the figures). The ancestral legs of the fourth abdominal segment are fused at the basis to form the furca. The remotor of the ancestral leg of the fourth abdominal segment now operates as the primary extensor of the furca. The promotor of the ancestral leg of the fourth abdominal segment now operates as the primary flexor of the furca.

Due to the reduction of the ancestral leg of the third abdominal segment the associated promotor and remotor muscles became obsolete. In the Neocollembola, the muscles are reconnected to the furcal base to function as secondary intersegmental furcal flexor and extensor. In this scheme, the furca has the capability to evolve larger.

Fig.Tom. Schematic diagram of furcal muscles in Tomoceromorpha
Janssens, F. 2008.
The secondary intersegmental furcal flexor and extensor can become stronger according to two different schemes. In the first scheme, the secondary intersegmental furcal flexor and extensor become stronger due to the relative elongation of the third abdominal segment. However, the elongation of the third abdominal segment is constrained by the geometrics of the body segments and the abdominal ventral groove.

Fig.Tommax. Maximal length of third abdominal segment in Tomoceromorpha
Janssens, F. 2008.
The elongation of the third abdominal segment in Tomoceromorpha is mainly constrained by the geometrics of the abdominal ventral groove. The depth of the ventral groove constrains the traject of the secondary intersegmental flexor muscles that have to pass ventrally through the lumen of the fourth abdominal segment to reach the anterior part of the furcal base. Fig. Tommax is a simplified schematic diagram representing the constrains. H = height of the third abdominal segment. L3 = length of the third abdominal segment. L4 = length of the fourth abdominal segment. f = position of the condyles of the furca. v = depth of the ventral groove at the joint of the abdominal segments.
v = n.H (n=0.2 to n=0.3)
f = m.L4 (m=0.5 to m=1)
L3 = ((1-n)/n).m.L4
The maximum length of the third abdominal segment is obtained with a furca that is translocated as posterior as possible, as can be observed clearly in Tomoceridae. A deeper ventral groove reduces the maximum length of the third abdominal segment. The theoretical maximum length of the third abdominal segment with most posterior position of the furca is about 2.3 times the length of the fourth abdominal segment (ventral groove depth about 0.3 of the height of the third abdominal segment), and about 4 times the length of the fourth abdominal segment (ventral groove depth about 0.2 of the height of the third abdominal segment).

Fig.Pan. Schematic diagram of furcal muscles in Panentomobryomorpha
Janssens, F. 2008.
In the second scheme, both the primary and the secondary furcal flexor and extensor become stronger due to the relative elongation of the fourth abdominal segment. The elongation is not constrained by the geometrics of the body segments and the abdominal ventral groove as in Tomoceromorpha. Therefore, the Panentomobryomorpha are more successfull in increasing the springing organ maximally.

Fig.Pod. Schematic diagram of furcal muscles in Poduromorpha
Janssens, F. 2008.
In the Poduromorpha, the muscles of the ancestral leg of the third abdominal segment reduced completely. In this scheme, the furca is implied to remain small.

Alternative tentative ordinal phylogenetic relationships

Fig.Tree. Tentative ordinal phylogenetic relationships
     +---------------- Poduromorpha
     |
<-pC-+    +----------- Tomoceromorpha
     +-Nc-+
	  |        +-- Euentomobryomorpha 
	  |    +---+
	  |    |   +-- Neelipleona
	  +-Pe-+
	       +------ Symphypleona

This ordinal tree (Fig. Tree) is compiled from 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), and Xiong & al. (2008). Traditionally, the Collembola have been divided into basic groups such as Poduromorpha, Neelipleona, Entomobryomorpha, and Symphypleona, which different authors have considered to represent orders, sections or every category in between these two. More recently, D'Haese (2002) and Xiong & al. (2008) have concluded that Entomobryomorpha is paraphyletic and D'Haese (2002:1148) proposed Tomoceromorpha as a new basic group of Collembola.

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. In the Poduromorpha this small furca 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 'true' springtails, 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 mainly accomodated by the third abdominal segment. In these Tomoceromorpha, the body curvature is minimal. In the second scheme, the Panentomobryomorpha, the larger furcal flexing muscles are accomodated by both the third and the fourth abdominal segment. 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 Neelipleona with a strongly curved body are here considered as a derived sidebranch of the Euentomobryomorpha. 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.

References