Structure and development of onychophoran eyes: What is the ancestral visual organ in arthropods?

Abstract

Scarce and controversial information on visual organs and their innervation in Onychophora currently do not allow a thorough comparison with Euarthropoda. Therefore, this study sets out to provide additional data on the architecture and morphogenesis of the onychophoran visual system and to explore similarities and differences between the visual organs of onychophorans and other arthropods. Based on the new data for Epiperipatus biolleyi (Peripatidae) and Metaperipatus blainvillei (Peripatopsidae), it is suggested that the compound eyes represent an autapomorphy of Euarthropoda since similarities with the onychophoran eyes are weak or absent. Instead, the innervation from a central rather than lateral part of the brain, the presence of only one (paired or unpaired) visual center, and a similar ontogenetic origin from an ectodermal groove rather than a proliferation zone suggest homology between the onychophoran eyes and the median ocelli of euarthropods. In conclusion, I suggest that the last common ancestor of arthropods bore only one pair of ocellus-like visual organs that were modified in several arthropod lineages. This hypothesis is supported by recent paleontological data.

Introduction

With the exception of a few eyeless species (see Kemp, 1913, Kemp, 1914, Lawrence, 1931, Peck, 1975, Peck, 1990, Ruhberg et al., 1991), visual organs are externally seen in most representatives of the Onychophora (Fig. 1A, B). The onychophoran eyes have often been suggested to show affinities to both the Annelida and Euarthropoda (Kennel, 1888, Holmgren, 1916, Dakin, 1921, Fedorow, 1929, Hanström, 1935, Eakin and Westfall, 1964, Eakin and Westfall, 1965, Horridge, 1965, Eakin, 1966, Eakin, 1968, Hermans and Eakin, 1974, Paulus, 1979, Pflugfelder, 1980, Moritz, 1993, Storch and Ruhberg, 1993). Among the ‘annelid’ features, the rhabdomeric type of receptor organelles, the presence of two kinds of retinal cells and a ‘lens’ as well as cilia situated in the longitudinal axis of the receptor processes are listed whereas an even array of straight cylindrical microvilli are thought to be shared with euarthropods (see Eakin and Westfall, 1965, Hermans and Eakin, 1974).

While there is no evidence that lens-like structures belong to the ground pattern of Annelida (see Bartolomaeus, 1992a, Purschke, 2003, Purschke, 2005; see also contribution by Purschke et al., 2006), all the other similarities thought to be shared between onychophorans and annelids occur in other bilaterians as well, such as Platyhelminthes, Mollusca, and Sipuncula (see, e.g., Hermans and Eakin, 1969, Rosen et al., 1979, Sopott-Ehlers, 1984, Sopott-Ehlers, 1991, Sturrock and Baxter, 1995, Sopott-Ehlers et al., 2001). These similarities might thus be plesiomorphic for all these taxa. Moreover, any relationship of the onychophoran eyes to those of other arthropods is uncertain since no further similarities were found apart from an even array of microvilli. Yet, such an array also characterizes most rhabdomeric photoreceptors within the Bilateria (see, e.g., Eakin and Westfall, 1965, Eakin, 1968, Hermans and Eakin, 1974, Eakin and Hermans, 1988).

Our knowledge on the onychophoran visual system has not kept pace with recent advances in studies of structure, development, and innervation of visual organs in Euarthropoda (reviewed by Paulus, 2000, Bitsch and Bitsch, 2005, Harzsch et al., 2005a, Harzsch et al., 2005b, Strausfeld, 2005). Nevertheless, some information has been gathered during the last two centuries on the morphology (Balfour, 1883, Dakin, 1921, Eakin and Westfall, 1964, Eakin and Westfall, 1965), development (Sedgwick, 1887, Kennel, 1888, Eakin, 1966), and innervation (Holmgren, 1916, Schürmann, 1987, Schürmann, 1995) of onychophoran eyes. Yet there are persisting controversies regarding the presence of optic ganglia, significance of rudimentary cilia within the retina, and innervation of eyes in Onychophora (see Balfour, 1883, Kemp, 1914, Holmgren, 1916, Dakin, 1921, Hanström, 1935, Eakin and Westfall, 1965, Eakin, 1966, Schürmann, 1987, Schürmann, 1995).

Due to the scarcity of data and controversial observations on onychophorans, the visual organs of Onychophora and Euarthropoda are difficult to compare and their homology hard to establish. Nevertheless, the onychophoran eyes have intuitively been regarded as a starting point in the evolution of visual organs in arthropods (see Paulus, 1979). The main objective of this study is therefore to address the question whether there are further correspondences in structure, development, and basic innervation patterns of visual organs between Onychophora and Euarthropoda. In this study, I combine classical histological and electron-microscopic techniques in order to re-evaluate and supplement previous data.