Morphology of Cambrian lobopodian eyes from the Chengjiang Lagerstätte and their evolutionary significance

Abstract

Visual organs are widely distributed throughout the animal kingdom and exhibit a great diversity of morphologies. Compound eyes consisting of numerous visual units (ommatidia) are the oldest preserved visual systems of arthropods, but their origins are obscure and hypothetical models for their evolution have been difficult to test in the absence of unequivocal fossil evidence. Here we reveal the detailed eye structures of well-preserved Early Cambrian lobopodians Luolishania longicruris and Hallucigenia fortis from the Chengjiang Lagerstätte, China. These animals possess a pair of eyes composed of at least two visual units, interpreted as pigment cups. Contrary to previous suggestions that Cambrian lobopodians possessed ocellus-like eyes comparable to those of extant onychophorans, this multi-component structure is more similar to the lateral eyes of arthropods. Morphological comparison and phylogenetic analyses indicate that these lobopodian eyes may represent an early stage in the evolution of the ancestral visual system of euarthropods.

Introduction

The great diversity and disparity of visual systems makes the reconstruction of their evolutionary development extremely challenging. This is particularly so in the case of arthropods, for which the homology of optic organs plays an important role in the discussion of arthropod phylogeny (Paulus, 1979, 2000; Bitsch and Bitsch, 2005). Direct fossil evidence is vital in helping us to characterize the origin and early evolution of arthropod compound eyes. However, this evidence is lacking before the Cambrian Period (542–488.3 Ma). The oldest fossil record of eyes occurs in the earliest trilobites from Cambrian Stage 3 (Clarkson et al., 2006; Parker, 2003); these already possessed a pair of well-developed compound eyes, and by Cambrian Stage 4 some arthropods exhibited sophisticated vision (Lee et al., 2011). Recent research (Paterson et al., 2011) has also revealed large compound eyes from anomalocaridids, a group of stem arthropods from the Early Cambrian (approximately 515 million years old), pushing the origin of compound eyes further down the arthropod stem lineage. As the visual organs of Cambrian crown-group arthropods and of later branching stem arthropods were already highly developed and divergent, they cannot provide the ultimate clue to the origin of arthropod compound eyes. To address this question requires an investigation of the visual systems that developed prior to compound eyes within the arthropod stem lineage.

Lobopodian animals (including extant onychophorans and tardigrades, and extinct fossil lobopodians) are the obvious candidates for this purpose, as they are considered to have a close but antecedent phylogenetic association with arthropods (Budd and Telford, 2009; Edgecombe, 2010). Cambrian lobopodian animals are relatively rare and, mostly lacking mineralised bodyparts, they only occur in a few exceptionally well-preserved fossil assemblages, such as the Chengjiang Lagerstätte (Stage 3 of Cambrian Series 2, circa 520 Ma) and the Burgess Shale Lagerstätte (Stage 5 of Cambrian Series 3, 05-510 Ma). Lobopodian specimens with eyes preserved are even sparser, and their eye morphology is little understood. Dzik (2003) speculated that the paired sclerites in serial register along the trunk of Microdictyon sinicum were compound eyes, an interpretation accepted by Gehring (2011, 2012), who further suggested that structures previously reported as paired sclerites on the head of Cardiodictyon catenulum were likewise compound eyes with many ommatidia. A pair of black spots on the head of Luolishania longicruris (=Miraluolishania haikouensis Liu et al., 2004; see Ma et al., 2009) was interpreted as simple eyes (Schoenemann et al., 2008; also see below). These contradictory theories are based on limited evidence, and are open to testing through additional specimens, detailed observation, and consideration of the likely taphonomic effects on fossil eye morphology.

Here we describe detailed structures of the eyes of L. longicruris (Figs. 1and 2) with the application of new imaging and analytical techniques. Also, for the first time, visual organs are reported and described from Hallucigenia fortis (Fig. 3). The interpretation of these lobopodian eyes and their significance for the evolution of panarthropod visual systems is discussed.