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Vertebrate with Protrusible Eyes with Cattle: Oryx5 and Domestic Cat (W SCIENTIFIC CORRESPONDENCE taminated food4 and which do not share the codon 146(C) and 158(C) amino acids Vertebrate with protrusible eyes with cattle: oryx5 and domestic cat (W. G., unpublished data). Many amino-acid SrR - Caecilians are among the most African family Scolecomorphidae, the eye changes in PrP change the phenotype of divergent and least-known major verte­ is not under bone or in a socket. Instead, it prion diseases; it is intriguing to speculate brate groups. Found throughout the is attached laterally to the base of the ten­ about evolutionary adaptation against humid tropics (with the exception of tacle7-9. In most caecilians, this would pre­ these diseases operating via sequence Madagascar), these limbless, fossorial vent the eye from being exposed to light, changes in PrP protein. It may therefore as it would be under heavily be the case that codons 143, 155 and, as pigmented skin. But in scole­ suggested above, 168 of the human PrP comorphids, the tentacular gene are key amino-acid positions in the groove is covered by pig­ interaction with components of the infec­ mentless skin. Thus, as the tive agent. However, a correlation tentacle is protracted and between a particular feature of a PrP pro­ retracted, the eye moves tein sequence and predisposition to a cer­ with it along a translucent tain strain of agent can only be track and remains exposed demonstrated experimentally. to ambient light regardless In addition, Krakauer et al. based their of position (a in the figure). analysis on only 56 variant codon posi­ The anatomy of preserved tions. In fact, there are at least 80 posi­ museum specimens of scole­ tions in the full open reading frame which comorphids suggested that show a minimum of one amino-acid their eyes might be protrusi­ replacement, leading to 3,160 possible dif­ ble9. That is, these animals ferent pairs of amino-acid replacements. might be able to protract the There are, for example, eight sheep PrP tentacle far enough to move protein variants and not the single sheep the eye beyond the roofing sequence shown in the phylogeny6. We bones of the skull, out suggest that a calculation on the basis of through the tentacular aper­ all prion protein sequences (including all ture and into the external known polymorphisms) would not only environment. Several living change the phylogenetic tree but would specimens of S. kirkii result in a higher probability for the became available recently, occurrence by chance of the convergence giving us the opportunity to observed. Serine and asparagine are high­ test this hypothesis. Using a ly variable in many codon positions of PrP. 35-mm camera and a syn­ In addition to hominoids and cattle, the chronized strobe, we cap­ codon 143 asparagine-to-serine replace­ a, Living specimen of S. kirkii with the tentacle retracted. tured images (b in the ment occurs twice as a single replacement: Note that the eye is still visible in the tentacular groove under figure) which demonstrate a layer of unpigmented skin. b, Another specimen with the in pig7, omitted by Krakauer et al. 1, PrP that Scolecomorphus can analysis also shows that codon 155 is one tentacle completely protracted, clearly showing the eye indeed protrude its eyes beyond the roofing bones of the skull. of the few positions which have two possi­ beyond the skull. Some ver­ ble amino-acid replacements ( asparagine amphibians possess many unique and tebrates (for example, mudskippers and in hamster), perhaps indicating a toler­ often strange characteristics, not the least frogs) have eyes that are retractable within ance for differences in this region. being their tentacles. These protrusible their sockets, but this is the only known A priori prediction of the incidence or organs, one on each side of the snout, are vertebrate with highly mobile, protrusible cross-species transmissibility of a spongi­ derived from the tear duct, certain extrin­ eyes. form encephalopathy requires a more sic eye muscles and other parts of the James C. O'Reilly adequate three-dimensional structural eye 1•2• The tentacle can be protracted a Department of Biological Sciences, model for PrP protein and its molecular considerable distance out of the head in Northern Arizona University, interactions than is available, and a much many species. Anatomically, it is directly Flagstaff, Arizona 86011-5640, USA better understanding of the molecular connected to the vomeronasal organ3, and Ronald A. Nussbaum basis of the strains of these unconvention­ behavioural experiments suggest that it is Museum of Zoology, al disease agents. involved in chemoreception4. We now University of Michigan, Wilfred Goldmann show for the first time that the east Ann Arbor, Michigan 48109-1079, USA Nora Hunter African caecilian Scolecomorphus kirkii Daniel Boone Robert Somerville can protrude its eyes beyond the skull by Bilby Research Center, James Hope means of the tentacle. Northern Arizona University, BBSRC & MRC Neuropathogenesis Unit, In all caecilians, the eyes are lidless and Flagstaff, Arizona 86011-6013, USA Institute for Animal Health, reduced, and at best function to detect 1. Wiedersheim, R. Die Anatomie der Gymnophiona, West Mains Road, Edinburgh EH9 3JF, UK changes in light intensity'·6• In many 44- 5 7 (Fisher, Jena, 1879). 2. Billo, R. & Wake, M. H.J. Morph. 192, 101- 111 1. Krakauer. D. C., Pagel, M .• Southwood, T. R. E. & species the eyes are fixed in bony sockets, (198 7). Zanotto. P. M. de A. Nature 380, 675 (1996). in others they are completely covered by 3. Badenhorst, A. Ann. Univ. Stellenbosch (A2) 1, 1- 26 2. Bruce, M. et al. Phil. Trans. R. Soc. 8343, 405-411 the roofing bones of the skull, while yet (1978). (1994). 4. Himstedt , W. & Simon, D. Herpet. J. 5, 266- 270 3 . Goldmann, W., Hunter, N., Smith, G., Foster, J. & Hope. others apparently lack eyes entirely. In (1995). J. J. gen. Virol. 75, 989-995 (1994). most caecilians that have eyes, the eye and 5. Wake, M . H. Zoomorphology105, 277- 295 (1985). 4 . Wilesmith, J. W., N. Z. Vet. J. 42, 1--8 (1994). 6. Frilzsch, B., Himstedt, W. & Crapon de Caprona, M.-0. 5 . Poidinger, M., Kirkwood. J. & Almond, W. Archs Virol. tentacle are morphologically distinct, the Devi Brain Res. 23, 201- 210 (1985). 131, 193-199 (1993). tentacle residing in a separate opening in 7. Boulenger. G. A. A Mag. nat. Hist. 11, 48 (1883). 6. Hunter, N. et al. Archs Virol. (in the press). 8. Nussbaum. R. A. Copeia 1981, 265- 269 (1981). 7. Mart in, T., Hughes, S., Hughes, K. & Dawson, M. the skull called the tentacular groove. 9. Nussbaum, R. A. Occl Pap. Mus . Zoo/. Univ. Michigan Biochem. biophys. Acta 1270, 211- 214 (1995). However, among the species of the 713, 1-49 (1985). NATURE · VOL 382 · 4 JULY 1996 33 .
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