The fine structure of the eyes of some bristly millipedes (Penicillata, Diplopoda): Additional support for the homology of mandibulate ommatidia

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Abstract

The eyes of adult Phryssonotus platycephalus (Synxenidae) and Polyxenus lagurus (Polyxenidae) were investigated by light and electron microscopy. At each side of the head, various numbers of eye cups are situated on projections, the eye hills. The eye cups of P. platycephalus and P. lagurus are similarly structured and considered homologous sense organs. Each corneal lens is biconvex and formed by four to six pigmented corneagenous cells with their nuclei displaced towards the mid-periphery of the eye cup. The corneal surface displays a conspicuous nanostructure of fingerprint-like ridges in P. platycephalus. However, the corneal surface appears smooth in P. lagurus. In P. platycephalus. A rudimentary crystalline cone is observed in each eye cup, always produced by a constant number of three eucone cells. The crystalline cone is wedged between the corneal lens and the distal rhabdom and consists of three distinct compartments. Each cone compartment is connected to the voluminous proximal nuclear region by one elongated cytoplasmic process, which runs through the infraretinular space. A dual type retinula is always arranged in two distinct horizontal cell layers. The distal retinula contains an unfixed number of four to five cells in P. lagurus, whereas it contains five to eight cells in P. platycephalus. The distal retinula cells form a large and fused axial rhabdom. A constant number of three proximal retinula cells give rise to a small axial rhabdom, which looks more or less triangular in cross sections. The basal matrix is rather thin, inconspicuous and lines the bases of the eye cups. The ultrastructure of the eye cups of P. platycephalus resembles that observed in the ommatidia of the centipede Scutigera coleoptrata. The present study lends additional support to the homology of mandibulate ommatidia, because of the common possession of crystalline cone cells and a bilayered dual type retinula in the eye cups of P. platycephalus. Ommatidia or unicorneal eyes that include eucone cells with nuclei displaced outside the cone compartments, as found in Scutigeromorpha and Penicillata, might also be interpreted as an additional autapomorphy of the Myriapoda. The suggested homology of scutigeromorph and penicillate eyes implies that penicillate eye cups have to be considered modified, probably miniaturized ommatidia.

Introduction

Compound eyes are widespread among extinct and recent euarthropods. Paulus, 1979, Paulus, 2000 and Ax (1999) suggested that compound eyes with ommatidia devoid of crystalline cones and probably similar to those found in xiphosuran chelicerates belonged to the ground pattern of the Euarthropoda. However, considerable structural divergences between xiphosuran and mandibulate compound eyes brought some authors to the conclusion that euarthropod compound eyes and their photoreceptor units, the ommatidia, have been “acquired independently in different arthropod lineages” (Bitsch and Bitsch, 2005, p. 203). Likewise, the evolution of mandibulate and myriapod eyes has been the issue of controversial debates (Paulus, 1979, Paulus, 1986, Paulus, 2000, Paulus, 2003, Spies, 1981, Müller et al., 2003a, Bitsch and Bitsch, 2005, Harzsch et al., 2005, Harzsch and Hafner, 2006). The multitude of conflicting hypotheses is mainly caused by insufficient knowledge of the construction of median and lateral eyes in certain euarthropod subgroups thought to have a phylogenetic key role. While the ommatidial structure and development have been investigated in detail in many xiphosurans, crustaceans and insects, only little information is available about the morphology of myriapod eyes, especially when it comes to their fine structure. Among the Myriapoda, only the centipedes (Chilopoda) and millipedes (Diplopoda) bear eyes, whereas the minute subterrestrial Symphyla and Pauropoda always lack them. The fine structural architecture and some aspects of postembryogenic development of the ommatidia of house centipedes (Scutigeromorpha = Notostigmophora) and the structure of the dispersed or closely aggregated lateral ocelli of various Pleurostigmophora (Lithobiomorpha, Craterostigmomorpha, Scolopendromorpha) have been recently re-examined by Müller et al., 2003a, Müller et al., 2003b, Müller and Meyer-Rochow, 2006a, Müller and Meyer-Rochow, 2006b, Müller and Rosenberg, 2006, and Harzsch et al., 2006, Harzsch et al., 2007.

Among recent Diplopoda, some taxa, as for instance the Polydesmida, do not possess eyes. Other millipedes have eye cups, also called lateral ocelli or simply ocelli (Bedini, 1970, Spies, 1981), situated on either side of the head, the number of which may vary between a single pair present in some Stemmiulida and approximately 90 in the archispirostrepsid species Dendrostreptus macracanthus (Attems, 1914) (Enghoff, 1990). Bristly millipedes (Penicillata), assumed to be the sister group to all remaining millipedes, the Chilognatha, have minute eye cups of a unique structure when compared to the lateral ocelli of arachnids, pleurostigmophoran centipedes and chilognath millipedes. The Penicillata comprise about 160 species belonging to the four subgroups Lophoproctidae, Hypogexenidae, Synxenidae and Polyxenidae (see Nguyen Duy-Jacquemin and Geoffroy, 2003). To date, the anatomy of penicillate eyes was only investigated in the European species Polyxenus lagurus (Willem, 1892, Spies, 1981, Paulus, 2000). All five eye cups of P. lagurus are located on a posteriolateral projection at each side of the head, the so-called “vaulted eye field” (Spies, 1981) or “Ocellen- or Augenhügel” (Eisenbeis and Wichard, 1985). Higher numbers of eye cups, up to 11 units per eye hill, are known from the Synxenidae.

The only detailed account for the fine structural anatomy of the eyes of P. lagurus was given by Spies (1981). According to his description, the eye cups of P. lagurus are scattered and consist of a strongly domed corneal lens (up to 7 μm in diameter) produced by axially stretched corneagenous cells and a dual type retinula with four distal retinula cells and three proximal retinula cells (making up a bilayered, fused rhabdom). Additionally, Spies (1981) described two vitreous body cells, each of which produces one vitreous body that lies between the subcorneal corneagenous sheath and distal rhabdom. The vitreous body cells were assumed to represent modified hypodermal cells. However, Spies (1981) did not rule out the possibility that the vitreous bodies of P. lagurus may be also considered relics of a former crystalline cone. In a short note, Paulus (2000) made a further point on the latter idea. He presented an additional TEM micrograph showing two to four vitreous bodies/body cells beneath the corneal lenses of P. lagurus. Due to the finding of proximal cone cell roots, he proposed homology with Semper cells in crustacean and hexapod ommatidia. Therefore, Paulus, 2000, Paulus, 2003 assumed that the penicillate eye cup may be seen as a rudiment of an old mandibulate ommatidium. With the description of a multipartite crystalline cone (built by four eucone cells) in the house centipede Scutigera coleoptrata (Linnaeus, 1758) (Müller et al., 2003a), the homology of lateral eyes of the Mandibulata could be confirmed and eye structures became relevant again as characters of phylogenetic importance. The potential homology of scutigeromorph and penicillate ommatidia should therefore also contribute to the ongoing debate whether the Myriapoda should be considered either monophyletic or a paraphyletic grade of terrestrial, non-hexapod Mandibulata. However, this phylogenetic discussion certainly requires a critical evaluation of the contradicting interpretations of vitreous body structures in the eye cups of P. lagurus offered by Spies (1981) and Paulus, 2000, Paulus, 2003.

The current study aims at exploring the general structure of the crystalline cone cells supposedly present in the eye cups of the Penicillata. We re-investigated the eyes of P. lagurus and added a new description on the eyes of a further penicillate species, Phryssonotus platycephalus. Moreover, the newly found and existing eye characters are discussed in terms of their phylogenetic significance.

Section snippets

Materials and methods

Five adult specimens of the Penicillata P. lagurus (Linnaeus, 1758) (Fig. 1A) and Polyxenus sp. (possibly also belonging to the species P. lagurus) (Polyxenidae) as well as three adult individuals of the P. platycephalus (Lucas, 1846) (Synxenidae) (Fig. 1D), all measuring between 2 and 3 mm in length and counting 14–17 pairs of legs, were used in this study. Specimens of P. lagurus were collected in September 2005 under bark pieces of plane trees by Monique Nguyen Duy-Jacquemin in Paris, whereas

General morphology of penicillate eye cups

The eye cups of P. lagurus, P. sp. cf lagurus and P. platycephalus are located on a protrusion posteriolateral to the head capsule. A conspicuous suture delimits the eye hill from the posteriolateral part of the head capsule (Fig. 1B,E). P. lagurus has five loosely aggregated eye cups on each eye hill (Fig. 1B), whereas 10–13 eye cups are encountered on each eye hill of P. platycephalus (Fig. 1E). In the latter, the eye cups are more closely aggregated and arranged in one anterior and one

The penicillate eye cups: comparison to previous descriptions

The eye cups of adult individuals of the bristly millipedes P. lagurus (including the P. sp. cf lagurus from Ibiza) and P. platycephalus were investigated by light and electron microscopy. The constant number of five eye cups per eye hill in P. lagurus confirms previous observations of Spies (1981) and Paulus (2000). The different numbers of eye cups found in P. platycephalus (n = 10–13) may be explained either by individual variations or age-dependent differences. However, there are no

Acknowledgements

We are grateful to Dr. Monique Nguyen Duy-Jacquemin (Muséum National d'Histoire Naturelle, Paris) for sending us live specimens of Polyxenus lagurus. Furthermore, she confirmed our determination of Phryssonotus platycephalus from Ibiza. We wish to acknowledge Dipl. Biol. Stefan Fischer (University of Rostock) for his kind help in collecting various specimens of P. platycephalus. Furthermore, we cordially thank Dr. Martin Fanenbruck for letting us analyze his section series of the heads of two

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