Article

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

ABSTRACT

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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    • "In this scenario, a biological structure like a gene, cell, or organ could first gain a function, making it multifunctional [a process sometimes termed gene sharing (Piatigorsky 2007)]. Later, the structure could duplicate and subdivide the ancestral functions between the duplicates, in a subfunctionalization or division of labor mode of evolution (Arendt et al. 2009, Darwin 1859, Force et al. 1999). Subfunctionalization could yield a different pattern than neofunctionalization yields, whereby subfunctionalization leads to two closely related modules with different functions and a multifunctional outgroup module (Figure 2b). "
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    • "Nilsson ( 2009 Nilsson ( , 2013 ) agrees with Arendt et al. ( 2009 ) , who proposed that early photoreceptors incorporated the pigment into the same cell as the membranes, as seen today in some cnidarian photoreceptors (Westfall and Kinnamon 1978 ; Nordström et al. 2003 ). Arendt's team proposed a " division of labor " sequence for further elaboration, whereby the screening functions were moved to specialized cells (Arendt et al. 2009 ; see also Arendt and Wittbrodt 2001 ; Arendt 2003 ). The pairing of a single pigmentary cell with a rhabdomeric photoreceptor cell is already suffi cient to orient phototaxis in marine zooplanktonic larvae (Jékely et al. 2008 ). "
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