The ‘division of labour’ model of eye evolution

European Molecular Biology Laboratory, Meyerhofstrasse 1, 69012 Heidelberg, Germany.
Philosophical Transactions of The Royal Society B Biological Sciences (Impact Factor: 7.06). 11/2009; 364(1531):2809-17. DOI: 10.1098/rstb.2009.0104
Source: PubMed


The 'division of labour' model of eye evolution is elaborated here. We propose that the evolution of complex, multicellular animal eyes started from a single, multi-functional cell type that existed in metazoan ancestors. This ancient cell type had at least three functions: light detection via a photoreceptive organelle, light shading by means of pigment granules and steering through locomotor cilia. Located around the circumference of swimming ciliated zooplankton larvae, these ancient cells were able to mediate phototaxis in the absence of a nervous system. This precursor then diversified, by cell-type functional segregation, into sister cell types that specialized in different subfunctions, evolving into separate photoreceptor cells, shading pigment cells (SPCs) or ciliated locomotor cells. Photoreceptor sensory cells and ciliated locomotor cells remained interconnected by newly evolving axons, giving rise to an early axonal circuit. In some evolutionary lines, residual functions prevailed in the specialized cell types that mirror the ancient multi-functionality, for instance, SPCs expressing an opsin as well as possessing rhabdomer-like microvilli, vestigial cilia and an axon. Functional segregation of cell types in eye evolution also explains the emergence of more elaborate photosensory-motor axonal circuits, with interneurons relaying the visual information.

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Available from: Günter Purschke, Oct 07, 2015
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    • "Consistent with this assumption is that, during evolution, bHLH and Sox proteins and their DNA binding sites have been mostly multiplied and diversified (Degnan et al. 2009; Guth and Wegner 2008; Pan et al. 2012) and, in particular, bHLH genes govern in extant metazoans the progression of individual cells toward their differentiation (Fig. 2). This ensures that multiple cell types can be differentiated through division of labor between cell types (Arendt et al. 2009), such as stimuli acquisition and information conductance and processing in sensory organs Fig. 1 The relationship of singlecelled and multicellular organisms and some critical events concerning the evolution of neurons and sensory systems. 1 Complicated life cycle with transient multicellularity; 2 most cellular communication signals are present, Sox-like and bHLH genes are present; 3 class A bHLH genes and SoxB genes that can induce neurons are present; 4 epithelial nerve nets and sensory organs evolve; 5 miR-124 specific for neurons and miR-183 specific for sensory cells appear; 6 ventral central nervous system (CNS) evolves; 7 'skin brains' with chordate-like patterning evolve; 8 neurons are concentrated in a dorsal neural tube and composite, organ-like sensory cell groups appear; 9 vertebrate sensory organs and the nervous system appear. # note that the position of Ctenophora is disputed. "
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    ABSTRACT: Understanding the evolution of the neurosensory system of man, able to reflect on its own origin, is one of the major goals of comparative neurobiology. Details of the origin of neurosensory cells, their aggregation into central nervous systems and associated sensory organs and their localized patterning leading to remarkably different cell types aggregated into variably sized parts of the central nervous system have begun to emerge. Insights at the cellular and molecular level have begun to shed some light on the evolution of neurosensory cells, partially covered in this review. Molecular evidence suggests that high mobility group (HMG) proteins of pre-metazoans evolved into the definitive Sox [SRY (sex determining region Y)-box] genes used for neurosensory precursor specification in metazoans. Likewise, pre-metazoan basic helix-loop-helix (bHLH) genes evolved in metazoans into the group A bHLH genes dedicated to neurosensory differentiation in bilaterians. Available evidence suggests that the Sox and bHLH genes evolved a cross-regulatory network able to synchronize expansion of precursor populations and their subsequent differentiation into novel parts of the brain or sensory organs. Molecular evidence suggests metazoans evolved patterning gene networks early, which were not dedicated to neuronal development. Only later in evolution were these patterning gene networks tied into the increasing complexity of diffusible factors, many of which were already present in pre-metazoans, to drive local patterning events. It appears that the evolving molecular basis of neurosensory cell development may have led, in interaction with differentially expressed patterning genes, to local network modifications guiding unique specializations of neurosensory cells into sensory organs and various areas of the central nervous system.
    Cell and Tissue Research 11/2014; 359(1). DOI:10.1007/s00441-014-2043-1 · 3.57 Impact Factor
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    • "A functional eye requires two fundamental building blocks: photoreceptors and shading pigment [1,2]. These functions may occur together in one cell type or they are separated and exhibited in two or more different cell types [2], commonly referred to as photoreceptor cells (PRCs) and pigmented supportive cells (PSCs) (see [3], for terminology). In Metazoa generally two types of PRCs can be recognized; rhabdomeric and ciliary PRCs [1,4-6]. "
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    ABSTRACT: In Annelida two types of photoreceptor cells (PRCs) are regarded as generally present, rhabdomeric and ciliary PRCs. In certain taxa, however, an additional type of PRC may occur, the so called phaosomal PRC. Whereas the former two types of PRCs are always organized as an epithelium with their sensory processes projecting into an extracellular cavity formed by the PRCs and (pigmented) supportive cells, phaosomes are seemingly intracellular vacuoles housing the sensory processes. Phaosomal PRCs are the only type of PRC found in one major annelid group, Clitellata. Several hypotheses have been put forward explaining the evolutionary origin of the clitellate phaosomes. To elucidate the evolution of clitellate PRC and eyes the leech Helobdella robusta, for which a sequenced genome is available, was chosen. TEM observations showed that extraocular and ocular PRCs are structurally identical. Bioinformatic analyses revealed predictions for four opsin genes, three of which could be amplified. All belong to the rhabdomeric opsin family and phylogenetic analyses showed them in a derived position within annelid opsins. Gene expression studies showed two of them expressed in the eye and in the extraocular PRCs. Polychaete eye-typic key enzymes for ommochromme and pterin shading pigments synthesis are not expressed in leech eyes. By comparative gene-expression studies we herein provide strong evidence that the phaosomal PRCs typical of Clitellata are derived from the rhabdomeric PRCs characteristic for polychaete adult eyes. Thus, they represent a highly derived type of PRC that evolved in the stem lineage of Clitellata rather than another, primitive type of PRC in Metazoa. Evolution of these PRCs in Clitellata is related to a loss of the primary eyes and most of their photoreceptive elements except for the rhabdomeric PRCs. Most likely this happened while changing to an endobenthic mode of life. This hypothesis of PRC evolution is in accordance with a recently published phylogeny of Annelida based on phylogenomic data. The data provide a nice example how morphologically highly divergent light sensitive structures emerged from a standard type of photoreceptor cell.
    Frontiers in Zoology 09/2013; 10(1):52. DOI:10.1186/1742-9994-10-52 · 3.05 Impact Factor
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    • "All animal phyla, with the exceptions of placozoans and sponges, employ the opsin-class of 7-transmembrane proteins for this purpose (Plachetzki et al., 2007 ; Porter et al., 2011 ; Feuda et al., 2012 ; Schnitzler et al., 2012 ). Other crucial and early steps in eye evolution must have been the development of specialized photoreceptor neurons capable of holding substantial quantities of opsin and the association with screening pigment to generate directionality (Arendt et al., 2009 ; Nilsson, 2009 ). Arrays of photoreceptors forming retinas and the development of optics to focus light must later on have been essential steps in the evolution of eyes and true vision. "
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    ABSTRACT: Eye evolution is driven by the evolution of visually guided behavior. Accumulation of gradually more demanding behaviors have continuously increased the performance requirements on the photoreceptor organs. Starting with nondirectional photoreception, I argue for an evolutionary sequence continuing with directional photoreception, low-resolution vision, and finally, high-resolution vision. Calculations of the physical requirements for these four sensory tasks show that they correlate with major innovations in eye evolution and thus work as a relevant classification for a functional analysis of eye evolution. Together with existing molecular and morphological data, the functional analysis suggests that urbilateria had a simple set of rhabdomeric and ciliary receptors used for directional photoreception, and that organ duplications, positional shifts and functional shifts account for the diverse patterns of eyes and photoreceptors seen in extant animals. The analysis also suggests that directional photoreception evolved independently at least twice before the last common ancestor of bilateria and proceeded several times independently to true vision in different bilaterian and cnidarian groups. This scenario is compatible with Pax-gene expression in eye development in the different animal groups. The whole process from the first opsin to high-resolution vision took about 170 million years and was largely completed by the onset of the Cambrian, about 530 million years ago. Evolution from shadow detectors to multiple directional photoreceptors has further led to secondary cases of eye evolution in bivalves, fan worms, and chitons.
    Visual Neuroscience 03/2013; 30(1-2):5-20. DOI:10.1017/S0952523813000035 · 2.21 Impact Factor
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