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• W2010069196 abstract "From skeletons to sense organs, vertebrates possess a variety of complex structures for which there are no obvious invertebrate antecedents. The evolutionary origin of such structures is hence poorly understood if not wholly obscure. The vertebrate eye is an example, as it has a characteristic architecture, image-forming capability, and retinal circuitry in even the most basal vertebrates, yet nothing similar is known from invertebrates. Where the latter have complex eyes, as in arthropods, octopus, and squid, these are independently evolved anatomical structures. The best candidate to date for a precursor to the vertebrate eye has been the frontal eye of the lancelet (amphioxus), a translucent, fish-like protochordate a few centimeters long that buries itself in shallow sands, and subsists by filter feeding. Tunicates, a separate protochordate lineage of vertebrate cousins, have a variety of simple photoreceptors, but these consist of so few cells that morphological comparisons with vertebrate eyes are problematic. The frontal eye in amphioxus is a more complex structure, located at the very front of the nerve cord (Figure 1, top). EM-level reconstruction (Lacalli, 1996) shows it to consist of a single pigment cup and two adjacent rows of cells whose cilia project from the anterior opening of the nerve cord (Figure 1, bottom). Because of their proximity to the pigment cup, one or both rows of cells have been reputed to be photoreceptors that, in combination with neurons lying just behind, form something like a simple retina. As the sensory array is one-dimensional, the frontal eye is not capable of forming a proper image. The behavioral evidence shows that it acts instead to orient the larvae to light as they feed at the water surface. Its function in the adult is not known. To date, the supposed homology between the amphioxus frontal eye and the paired eyes of vertebrates has been largely a matter of conjecture, but this has now been beautifully confirmed by the detailed molecular analysis of Vopalensky et al. They show that the row of cells positioned just behind the pigment cup (the magenta-colored cells in the figure) express a combination of transcription factors (transient Rx, Pax4/6, Otx, Six3/6) and opsins (c-opsins 1 and 3) matching that of vertebrate rods and cones. Hence, they are vertebrate-type photoreceptors despite their simple morphology. The cells immediately behind them (light blue in the figure) are serotonergic neurons with caudal projections to the amphioxus equivalent of the basal midbrain, a region where locomotory activities are initiated in lower vertebrates. Finally, the pigment in the shielding pigment cup (red in the figure) is melanin and shows a vertebrate-type regulatory signature. There is still a big evolutionary gap to bridge between this tiny eye, lacking image-forming capabilities, and vertebrate eyes, but at least that bridge is now firmly anchored at both ends. The difference between amphioxus and vertebrate eyes that is most readily explained is that between one eye and two. The embryonic eye rudiment in vertebrates is medial, and without normal developmental control will remain so, to produce the condition known as cyclopea, that is, a single medial eye. Changing from one eye to two, or back again, is thus easily accomplished by altering the relevant developmental signals. Although unlikely, it is at least possible that amphioxus once had a larger eye, or even paired eyes, that were later reduced to the simple medial structure we see today. If so, however, there is no way to prove this or any other such scenario when the animals representing intermediate steps in the sequence are all long extinct. Amphioxus is like any other animal in being specialized in various ways, notably in the ability to burrow head first through sand. Its narrow, pointed head is probably an adaptation to facilitate burrowing, and an accompanying reduction in size or loss of its anterior sense organs would not be unexpected. In addition, when amphioxus larvae first hatch, they are unusually tiny for a fully functional chordate compared with comparable hatching stages in aquatic vertebrates. This is probably another specialization and may have resulted in a further reduction of once larger structures, including the nerve cord itself. This could explain why amphioxus lacks some of the signaling pathways thought to be responsible for patterning the CNS in both hemichordates and vertebrates (Pani et al., 2012), as signaling over distance in a secondarily miniaturized embryonic rudiment may be either unnecessary, or could even interfere with alternative and more localized (e.g., cell-to-cell) forms of developmental communication. A general point deserves emphasis, however, which is that an animal can be specialized and evolutionarily divergent in some ways, while still being quite conservative in others. The trick for the evolutionary biologist is to distinguish the former from the latter and to explain why. Amphioxus has, in fact, been in and out of fashion as a model for ancestral chordates, spending much of the 20th century on the sidelines of phylogenetic debate. This new study of the frontal eye is part of a relatively recent trend, since about 1990, to re-examine amphioxus with modern analytical techniques and bring it back to center stage, as the best available model for the proximate ancestor of vertebrates. It is well known that the amphioxus genome is surprisingly little modified, which probably limits how much secondary modification its anatomy has undergone. In addition to similarities in the frontal eye and optic circuitry, the anterior nerve cord of amphioxus almost certainly shares other key organizational features with the vertebrate brain, at least for those anatomically basal brain centers responsible for ancient and essential survival functions like feeding, circadian rhythms, habitat selection, and escape from predators. Amphioxus larvae have practical advantages for such investigations, of small size, limited cell numbers, and transparency. Important new information on conserved neural pathways and brain organization should emerge as the authors of the featured study, and others in the field [see Candiani et al. (2012) for a recent and related study], continue their work. Large gaps remain in the story of how ancestral chordates originated and how, from among these, the first vertebrates arose. Where there are no surviving species to fill these gaps, the alternative is to look to fossils. In the absence of hard skeletons, the fossil record predating vertebrates is extremely sparse, but there are new discoveries that bear on these issues, as well as reinterpretations of previously known but poorly understood fossil material. Pikaia, from the Middle Cambrian Burgess Shale, was first reported in 1911, but has only recently been fully described. It resembles amphioxus in many respects, but is probably more primitive (e.g., it lacks eyes) and may be showing us an early stage in the evolution of segmental muscles in chordates (Lacalli, 2012). The enigmatic vetulicolians (Smith, 2012), mainly from China, are now thought to show what the ancestors of the earliest chordates were like at a stage when they had a pharynx perforated by gill pores, but lacked the notochord and somite-based musculature that we normally associate with chordates. Understanding the true nature of these sometimes bizarre creatures is a challenge, but there has been progress nevertheless. Prospects for obtaining new insights into the key events of early chordate evolution, based on a combination of molecular, genomic and paleontological data, are now better then ever." @default.
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• W2010069196 date "2012-12-20" @default.
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• W2010069196 title "Looking into eye evolution: amphioxus points the way" @default.
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• W2010069196 doi "https://doi.org/10.1111/pcmr.12057" @default.
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