REVIEWS Solitarychemosensorycells: why do primaryaquaticvertebrates need anothertaste system? Kurt Kotrschal A generally more evenly distributed The taste-like system of solitary t the body surface of fish, over the body surface20Jl. Howchemosensory cells (SCCs) has almost a few chemosensory sysever, higher densities of SCCsmay eluded scientific attention. This is tems extract information particularly remarkable, since recent be found along the head than &from a plethora of disalong body and tail, and SCCs may surveys have revealed that this system solved chemical#. Most fish have of epidermal cells is widespread and cluster around free neuromastsl4. a keen sense of smell and, in addiabundant among the anamniotic aquatic tion, they may carry abundant Where are SCCs found and vertebrates. In the rocklings (Gadidae, taste buds on barbels or at other Teleostei), high densities of SCCs occur how abundant are they? body surface#. Consequently, SCCsor oligovillous cells have at a specialized dorsal fin. Recent catfish have even been compared evidence from this model indicates that been found in the epidermis of with tetrapod tonguess. However, SCCs are narrowly tuned to dilutions most primary aquatic vertebrates fish also possess other skin theme of fish body mucus and bile. Thus, investigated2J. They are present in receptors, resulting in an ill-charSCCs may sample the ambient water most species of fish, including lamacterized ‘general chemosense’6J. for the upstream presence of potential preys, paleonisciform and teleost The solitary chemosensory actinopterygians, sarcopterygians cells (SCCs) are the least known of competitors or predators. However, in sea robins (Triglldae, Teleostei), SCCs seem and even elasmobranchs (a ray, these chemoreceptor&*. Staining to be involved in finding food. Information Raju clauat&‘). SCCshave not been with methylene blue demonstrated the presence of spindle-shaped from many more species is needed to found in a few species of fish, such cells within the epidermis of some explain why SCCs and taste buds have as the benthic and sluggish northbeen maintained in parallel for such a ern Atlantic Agonus cataphractus23. teleost fishg. Because of their ap parent basal contacts with nerve long evolutionary period of time - from The lack of a recurrent facial nerve fibers and their ultrastructural the age of the agnathans to that of the (which innervates the trunk skin resemblance to taste-bud cell+12, most advanced teleost fishes. in most fish) does not necessarily these secondary sensory cells were mean that SCCs are absent. For assumed to be chemosensory; this example, SCC-likecells innervated Kurt Kotrschal is at the Konrad Lorenz hypothesis was supported by elecby spinal nerves are present in the Forschungsstelle and Dept of Zoology, University of trophysiological recordings13J4. finger-like free pectoral-fin rays of Vienna, A-4645 Grtinau 11, Austria. Throughout this review, ‘smell’ sea robins (Triglidae, Teleostei)llJ4. refers to inputs provided by the Among the amphibians, SCClike cells have been found only in nasal olfactory mucosa, whereas ‘taste’ means inputs via taste buds. No proper term as yet ranid tadpoleGJ5. However, it is uncertain how much this limited phylogenetic distribution reflects the difficulties in exists to name the SCC input and, to avoid confusion, none is suggested. searching for these cells in animals where the epidermis is covered by a keratineous slough. A systematic re-investigation that includes cecilian and urodelan larvae may clarify Structure of SCCs versus taste buds the situation. In most species, SCCs show a single microvillous apex, Quantitative estimates of SCC densities over the body which is sometimes furcated or even brush-like, and contacts the ambient waters. In lampreys, similar cells carry a few surface are only available for 13 mainly ostariophysan teleapical microvilli, and are thus known as ‘oligovillouscells’l5-17. osts20Jl. These range from 200 SCCsmm-2 in the neon tetra The obvious difference between taste-bud cells and SCCs (Hypessobrycon innesi) to 3000mm-2 in the roach (Rutilus rutilus;Fig. la), with peak values of 21000 mm-2 in halos of is that the former are part of a distinct organ, whereas the 100 km radius around free neuromasts. Thus, an averagelatter are embedded between unspecialized epidermal cells. sized roach of 200mm body length may carry approxiEven when SCCsoccur at high densities (e.g. in the epidermis mately 5 million SCCs. In eight species of cyprinids, 5748% of the rockling anterior dorsal finIs) thin glial-likesheets from epidermal cells prevent direct contact of adjacent SCCs. of all epidermal chemoreceptors identified were SCCs, and the remaining chemoreceptors were organized in taste Taste-bud cells are innervated by intragemmal fibers, and, similarly, SCCs form synaptic contacts at their bases bud.9. A considerably higher density of approximately with one to three (facial) nerve fiberG. SCCs are not inner1OOOOOSCCs mm-2was found in the epidermis of the specialvated by perigemmal fibers, which may transmit tactile infor- ized anterior dorsal fin of rocklings (Fig. lb; see below)zJ6. mation in taste buds, but the free spinal nerve endings that are never far from any SCCmay be their functional analoglg. Cell-line orlgln of epidermal chemoreceptors The fine structural similarity of oligovillous cells and In many ostariophysan fishes (e.g. cyprinids and catfishy, SCCSsuggests that they are part of a homologous (phyloexternal taste buds may cover the entire body surface and genetically continuous) vertebrate cell line*.Their apex seems aggregate at areas that frequently contact and locate food, to reflect some phylogenetic change from oligovillous in the such as lips, barbels4 or elongated fins. By contrast, SCCsare 110 o 1996, Elsevier Science Ltd TREE vol. II, no. 3 March 1996 REVIEWS agnathans to univillous in the gnathostomes, with a further shift from a furcated tip of the villus to an unbranched tip towards the perciformsQ. The fine structural resemblance of SCCs to taste-bud cells adds to the speculation that taste buds developed during the early phylogeny of (agnathan) vertebrates by accumulation of SCCs(Refs 2,8,11).This direction of evolutionary change is plausible, because it would be from the simple (SCC)to the more complex structure (taste bud). However, the opposite direction of evolutionary change (which would imply that SCCs are disaggregated taste buds) cannot be rejected, because there are no extant taxa with either SCCs or taste buds. Lampreys have taste-bud-like structures, the so-called terminal budsl6, in addition to their oligovillous cells. As a third possibility, SCCs and taste buds may have developed independently. The question of cell-line relationships of SCCsand tastebud cells may be of minor importance, since increasing evidence indicates that these secondary epidermal chemosensory cells do not originate from neural crest material, but are induced from undifferentiated epidermal stem cells27J8 by the innervating nerves. Thus, the ability to differentiate into epidermal chemoreceptors would mainly be due to a stimulating potential of the innervating (facial or even spinal) nerves. This, of course, does not explain why some of these nerves induce and innervate SCCs and others induce and innervate taste buds. It is not even known whether SCCs and taste buds are always innervated by different nerve fibers, or whether a single (facial) fiber may sample both structures. SCC function: the rockling anterior dorsal fin Because of the difficulties of studying SCCsin generalized distributed systems2J1, most of our present knowledge on SCCs is from studies of the anterior dorsal fin of a few species of rocklings (Gadidae, Teleostei). This fin is a complex chemosensory organ, with approximately 100000SCCsmm-2 (approximately 5 million SCCs in tota1)[email protected] structure of cells, their innervation and synapses, representation in the central nervous system (CNS), sampling movements of the fin and, to some extent, the function and biological roles of SCCshave been investigated in this model. From these studies, inferences have been made about the function of distributed SCCsystems21. It has been demonstrated that several hundred SCCsconverge onto a single facial nerve fiber along the anterior dorsal fin of rocklingsl2,17,19,26.29. These fibers are somatotopically represented in a distinct dorsal part of the brain-stem facial lobe26.However, the higher-order brain connections are not particularly distinct from the taste-bud system, and the primary somatotopy is not preserved in ascending or descending connections21 (K. Kotrschal and T. Finger, unpublished data). For these reasons, it seems adequate to consider SCCs as a taste (facilis) sub-system. Chemoresponses could only be recorded electrophysie logically from the moving fin. Furthermore, responses were only elicited by a narrow spectrum of stimulil4JOJ1,including dilutions of heterospecific fish body mucus, fish bile or human sputum, but not by typical taste stimuli, such as food extracts and amino acids. The fin samples by an undulation of lo-20 Hz, depending on the temperature. Specific stimulation caused a decrease in opercular breathing movements, which is associated with alertness, and an increase in sampling frequency of the fin32J3.Therefore, it was concluded that the rockling anterior dorsal fin is a low-threshold bulkwater sampler, which probes for the upstream presence of other fish, including potential predator&*l. TREE vol. II, no. 3 March 1996 (4 Taste (b) Fig. 1. (a) Solitary chemosensoty cell (SCC) system of a roach (Rutilus rutilus) as an example of a generalized distributed system. Length of the fish is approximately 200 mm. The cross-section through the head skin (top) shows a taste bud and an SCC. The epidermis is approximately 50 km thick, and 1 mm* epidermis may contain a few thousand SCCs. (b) A specialized aggregated SCC system in the rockling (Gaidropsarus sp.) anterior dorsal fin. Length of the fish is approximately 200 mm. Fin rays on top of the fish are approximately 3 mm in length and 0.1-0.2 mm in diameter. The ray epidermis is approximately 30 pm thick, and 1 mm2 ray epidermis contains approximately 100000 SCCs. These results render it unlikely that SCCs are the morphological substrate for the ‘common chemical sense’ (sensu Parke@2JJl, which mediates high-threshold avoidance reactions to harmful chemical stimuli. This unspecialized them@ sense7JJ is likely to reside in free trigeminal (head) and spinal (body) nerve endings34. Sampling in SCCs and taste buds Fluid flow decreases towards surfaces, resulting in relatively stagnant ‘boundary layers’. Stimulus molecules can only access sensory surfaces by slow molecular diffusion through these layers. Enhanced flow decreases the thickness of boundary layers and, therefore, accelerates the access of chemicals to receptor sites. This principle applies to both taste buds and SCCs. In the SCCsof the rockling anterior dorsal fin, responses could only be recorded from the moving fin, where undulation frequency determines the access of the stimulus to receptor surfaces. Therefore, the response intensity of the system at constant ambient concentrations of stimulus depends upon both the physiological properties of the receptors and fluid flow14.This also means that individuals can only extract information on stimulus strength by integration of flow velocities. In rocklings, this may be achieved by an integration of the motor activity of the fin with sensory gain in the brain stem21.In other fish, aggregations of SCCsaround free neuromasts can be observed20v21; thus, an integration bc tween neuromast and SCCinput may be achieved within the brain. This is supported by l,l’-dioctadecyl-3,3,3’,3’-tetramethylindo-carbocyanine (di1) tracings of secondary facial lobe connections within rockling brains (K. Kotrschal and T. Finger, unpublished data). By contrast to SCCs, flow may be generally of minor importance for taste-bud function, because taste buds seem to be most useful for the co-localization of tactile and chemical stimuli2 (i.e. allowing discrimination of palatable items upon touch). However, flow may be important in cases such as catfish barbels, where taste buds can provide orientation in chemical gradients 35.Also, in the taste-bud pore, 111 REVIEWS V’ Pike Fig. 2. Fish downstream of a potential predator (a pike, Esox lucius) exploring the odor plume. Epibenthic fish samples the plume with the SCCs at its body surface by swimming a zig-zag path. Benthic rockling samples the plume with its anterior dorsal fin while at rest. the supporting cells provide a peculiar thin-layered mucus environment for the apical villous chemoreceptorsir. This is not the case for SCC apices, which reside within the relatively thick body mucus. By contrast to the rockling anterior dorsal fin, the distributed SCCsin other fish are not mounted on a specialized support that can be moved independently of the body. However, it is reasonable to assume that currents are also indispensable for SCC sampling in generalized distributed systems. Such currents may be generated by the environment, but are predominately produced by active swimming movement.+. Thus, swimming in fish is not only a means of locomotion; it also serves to actively sample the environment for chemical (as well as visual and electrical) stimuli, analogous to sniffing. Dashing and zig-zagging are part of the behavioral responses of some fish to the presence of alarm substance36J7,and such behavior was interpreted previously as predator avoidance or distraction behavior. However, increased swimming activity with no clear spatial vector may also serve to sample the environment for (chemical) stimuli and to use chemosensory organs, including SCCs, to their full potential. High-resolution swim-path analysis has indeed shown an increase in swimming velocity and unsteady swimming in European minnows stimulated with potential predator odor (dilutions of trout body mucus)38J9. The evolutionary significance of SCCs The rockling anterior dorsal fin provides the basis for speculations on the evolutionary benefit of SCCsystems. The dorsal fin confers a unique advantage on substrate-orientated night-active rocklings as compared with the distributed SCC systems of all other fish: rocklings may scan the upstream water for the presence of fish, including potential predators, without having to leave their sheltersss. Comparisons between successive measurements would allow a rockling to judge the situation ahead of the fish and to adjust its own behavior accordingly. Water currents generated by the active sampling movements of the fin are necessary to trigger responses from their SCCs(Fig. 2)iJ. To generate flow at their body surfaces, all other fish would have to sample odor plumes by swimming through them (Fig. 2). Although these fish can collect quick and precise information on spatial structures and dynamics of odor plumes, active swimming potentially increases their exposure to predators. 112 Such SCCsystems may have evolved as bulk-water samplers, providing the fish with useful information on the presence of other fish upstream. Evidence in rocklings indicated that heterospecific fish mucus triggered responsesl4, and that proper stimulation of rocklings caused a cessation of opercular breathing movements, which can be interpreted as an arousal response (see above)3zJs. Therefore, it was assumed that a major ecological role of SCCs may be predator avoidance. However, suction-electrode recordings in isolated fin rays showed that conspecific bile may also be a potent stimulus o<. Kotrschal and K. Doving, unpublished data). In general, information on the upstream presence of other fish may affect intra- and interspecific spacing, competition, or even home range and habitat recognition. If predator avoidance is a major function of SCCsystems, it can be predicted that the system should be particularly well developed in fish that are most susceptible to predation: juveniles or species that remain relatively small. However, no relationship between body size and SCC densities was found in 12 species of teleosts*O.The ontogenetic develop ment of SCC densities in zebrafish (Danio rerio) shows a steep positively allometric increase of SCCdensities relative to body surface during early postlarval growth, when small juvenile fish are probably most susceptible to predation (K. Kotrschal and A. Hansen, unpublished data). Clearly, these data are still insufficient to judge a possible role of SCCs in predator avoidance. Rather than body size, predation pressures (for example, in the original habitats of the species) are probably relevant. SCC densities have been shown to increase in carp as a response to acidification40, but no other data exist about possible adaptive changes of SCCdensities in individuals. A number of recent publications indicate a remarkable complexity in chemical predator-prey communication and, hence, stress the importance for potential prey fish to keenly distinguish between different chemical stimuli from conspecifics (alarm substance) and predators (Refs 41-43). Experimentally anosmic fish do not behaviorally respond to relevant stimuli, such as chemicals from predators44, but this does not necessarily disprove an SCC involvement in this kind of chemo-communication, because of the following points: (1) Rendering fish anosmic dramatically decreases their overall activity, which makes behavioral effects of chemo-stimulation hard to detecPJ9. (2) Appropriate methods allow subtle behavioral changes in anosmic fish in response to food stimuli to be detected, but responses to body-mucus dilutions of potential predators were ambiguou.+‘J3,38,39. (3) Both SCC and olfactory inputs may need to be integrated within the brain to evoke motor outputs*l. This may occur within the telencephalon, which is reached by viscerosensory input via lemniscal pathways4s, and if this is the case, only electrophysiological recording from the telencephalon, not behavioral experiments with anosmic fish, will be conclusive. What we ought to know: why one should be extremely cautious in generalizing As indicated in this article, the majority of functional results on SCCsare from rocklings, which are only a few spe ties out of more than 20000 teleost species. However, support for the present rockling-based generalization is provided by the observation that oligovillous cells in lampreys responded vigorously to water in which frozen trout, a major lamprey predator, had been allowed to thaw13. Of all the aquatic vertebrates with SCCs (excluding rocklings), the source of innervation has only been established in the sea robins, where SCC-likecellsll seem to be supplied TREE vol. II, no. 3 March 1996 REVIEWS by spinal nerves46and respond to food-related stimuW. This is almost in complete contrast to the results in rocklings, and underlines the need to be extremely cautious when generalizing about SCCs with our present knowledge. The majority of other unexplored SCCsystems may either be facially or spinally innervated and may even functionally differ from those in both rocklings and sea robins. Where we ought to go from here Studies on the innervation and function of distributed SCCsystems outside the rocklings are urgently needed. However, rocklings will remain one of the most important models in SCCresearch, mainly because of the abundance of SCCsin their anterior dorsal fin and because of the accessibility of this system for research. Recordings from single facial nerve fibers and patch-clamp recordings from isolated SCCs are required. Furthermore, rockling SCCs should be used as as a bioassay during further isolation and characterization of the active stimulus components. Finally, CNSrecordings in rocklings and other fish are needed to elucidate the potential crosstalk between olfactory and SCCinputs. Against such a background of morphological and functional data, further behavioral experiments will help to clarify the ecological roles of SCC systems and to explain why the primary aquatic vertebrates have kept their SCCs, in parallel with taste buds, over such long evolutionary periods. Acknowledgements I thank the ‘Verein der Fijrderer’ and the H.v.Cumberland-Stiftung for permanent support. I am particularly grateful to Mary Whitear, Jelle Atema, Kjell Doving, Tom Finger and Rob Peters, my colleagues and friends who have contributed significantly to our present knowledge about SCCs. References Atema, J. (1988) Distribution of chemical stimuli, in Sensov Biology Vertebrates (Atema, J. et al., eds), pp. 29-56, Springer Kotrschal, K. (1991) Solitary chemosensory cells -taste, common chemical sense or what? Rev. Fish Biol. Fish. 1,3-22 Bardach, J.E. and Atema, J. (1971) The sense of taste in fishes, in Handbook ofSensory Physiology Iv, 2 (Beidler, L.M., ed.), pp. 293-336, Springer 4 Gomahr, A., Palzenberger, M. and Kotrschal, K. (1992) Density and distribution of external taste buds in cyprinids, Enuiron. Biol. Fish. ofAquatic 33,125-134 5 Caprio, J. et al. (1993) The taste system of channel catfish: from biophysics to behavior, Trends Neurosci. 16, 192-197 6 Parker, G.H. (1912) The relation of smell, taste and the common chemical sense in vertebrates, .I.Nat1 Acad. Sci. 15,219-234 7 Silver, W.L. (1987) The common chemical sense, in Neurobiology of Taste and Smell (Finger, T.E. and Silver, W.L., eds), pp. 65-87, Wiley 8 Whitear, M. (1992) Solitary chemosensory cells, in Chemoreception in Fishes (Hara, T.J., ed), pp. 103-125, Chapman &Hall 9 Whitear, M. (1952) The innervation of the skin of teleost fishes, Q. J. Microsc. Sci. 93,298-305 10 Whitear, M. (1965) Presumed sensory cells in fish epidermis, Nature 208, 703-704 11 Whitear, M. (1971) Cell specialization and sensory function in fish epidermis, J. Zool. 163,237-264 12 Whitear, M. and Kotrschal, K. (1988) The chemosensory anterior dorsal fin in rocklings (Gaidropsaras and Ciliata, Teleostei, Gadidae): activity, fine structure and innervation, J. Zool. 2 16, 339-366 13 Baatrup, E. and Doving, K. (1985) Physiological studies on solitary receptor, of the oral die papillae in the adult brook lamprey, Lump&a planeri (Bloch), Chem. Senses 10,559-566 14 Peters, RI., Kotrschal, K. and Krautgartner, W-D. (1991) Solitary chemoreceptor cells of Ciriata mastelu (Gadidae, Teleosteo are tuned to mucoid stimuli, Chem. Senses 16,31-42 TREE vol. I I, RO. 3 March 1996 15 Whitear, M. and Lane, E.B. (1983) Oligovillous cells of the epidermis: sensory elements of lamprey skin, J Zool. 199, 359-384 16 Baatrup, E. (1983) Terminal buds in the brancbial tube of brook lamprey [Lumpetra planet-i (Bloch)] - putative respiratory monitors, Acta Zool. 64, 139-147 17 Jakubowski, M. and Whitear, M. (1990) Comparative morphology and cytology of taste buds in teleosts, Z. Mikrosk.-Anal. Forsch. 104, 529-560 18 Kotrschal, K., Kinnamon, J.C. and Royer, SM. (1990) High voltage electron microscopy and 3-D reconstruction of solitary chemosensory cells and Dil labelling of primary afferent newe fibers, in Proc. Xllth Int. Congr. Electron Microsc., San Francisco, pp. 412-413 19 Kotrschal, K., Whitear, M. and Finger, T. (1993) Spinal and facial innervation of the skin in the gadid fish Cihta mastela (Teleostei), J. Comp. Neural. 331,407-417 20 Kotrschal, K. (1992) Quantitative scanning electron microscopy of solitary chemoreceptor cells in cyprinids and other teleosts, Environ. Biol. Fish. 35,273-282 21 Kotrschal, K. Ecomorphology of solitary chemosensory cell systems in fish, Environ. Biol. Fish. (in press) 22 Whitear, M. and Moate, R.M. (1994) Chemosensory cells in the oral epithelium of Ruju clauata, J. Zool. 232,295-312 23 Whitear, M. and Mittal, A.K. (1986) Structure of the skin of Agonus cataphractas fleleostei), J Zool. 210,551-574 24 Scharrer, E. (1935) Die Empfindlichkeit der freien Flossenstrahlen des Knurrhahns CTrigla) fiir chemische Reize, Z. Vergl. Physiol. 22, 145-154 25 Whitear, M. (1976) Identification of the epidermal ‘StifIchenzellen’ of frog tadpoles by electron microscopy, Cell Tissue Res. 175, 391-402 26 Kotrschal, K., Whitear, M. and Adam, H. (1984) Morphology and histology of the anterior dorsal fin of Caidropsuras mediterraneas (F&es, Teleostei), a specialized sensory organ, Zoomorphology 104,365-372 27 Stone, L.M. and Finger, T.E. (1994) Mosaic analysis of the embryonic origin of taste buds, Chem. Senses 19,725-735 28 Lee, J.E. et al. (1995) Conversion of Xenopus ectoderm into neurons by neural), a basic helix-loop protein, Science 268, 836-844 29 Kotrschal, K. and Whitear, M. (1988) Chemosensory anterior dorsal An in rocklings (Gaidropsaras and Ciliata, Teleostei, Gadidae): somatotopic representation of the Ramus recurrens facialis as revealed by transganglionic transport of HRP,J. Comp. Neurol. 268,109-120 30 Peters, R.C., Van Steenderen, G.W. and Kotrschal, K. (1987) A chemoreceptive function for the anterior dorsal fin in rocklings (Gaidropsaras and Ciliata: Teleostei: Gadidae): electrophysiological evidence, J Mar. Biol. Assoc. 67,819-823 31 Peters, R.C. et al. (1989) A novel chemosensory system in fish: electrophysiological evidence for mucus detection by solitary chemoreceptor cells in rocklings (Ciliata mastela, Gadidae), Biol. Bull. Mar. Biol. Lab. Woods Hole 177,329 32 Kotrschal, K., Peters, R. and Atema, J. (1989) A novel chemosensory system in fish: do rocklings (Ciliata mastela, Gadidae) use their solitary cbemoreceptor cells as fish detectors? Biol. Bull. Mar. Biol. Lab. Woods Hole 177,328 33 Kotrschal, K., Peters, R.C. and Atema, J. (1993) Sampling and behavioral evidence for mucus detection in a unique chemosensory organ: the anterior dorsal fin in rocklings (Ciliata mastela: Gadidae: Teleosteg, Zool. Jahrb. Physiol. 97, 47-67 34 Whitear, M. (1983) The question of free nerve endings in the epidermis of lower vertebrates, Actu Biol. Hungurica 34, 303-319 35 Atema, J. (1971) Structures and functions of the sent of taste in catfish (Ictalarus natalis), Brain Behav. Evol. 4,273-294 36 von Frisch, K. (1941) fiber den Schreckstoff der Fiihhaut und seine biologische Bedeutung, Z. Vergl. Physiol. 29,46-145 37 Heczko, E. and Seghers, B.H. (1981) Effects of alarm substance on schooling in the common shiner (Notropis cornutas, Cyprinidae), Environ. Biol. 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(1995) Acquired recognition of chemical sthnuii from pike, E&x fucius, by brook sticklebacks, Culaea inconstans (Osteichthyes, Gasterosteidae), Ethology 99,234-242 44 Chivers, D.P. and Smith, R.J.F. (1993) The role of olfaction in chemosensory-based predator recognition in the fathead minnow, Pimephales promefas, .I. Chem. Ecol. 19,623-633 45 Finger, T.E. (1988) Organization of the chemosensory systems within the brains of bony fishes, in Sensory Biology ofAquatic Animals (Atema, J. et al., eds), pp. 339-363, Springer 46 Finger, T.E. (1982) Somatotopy of the representation of the pectoral fht and tree fin rays in the spinal cord of the sea robin, Prionotus carolinus, Biol. Bull. Mar. Biol. Lab. Woods Hole 163, 154-161 47 Silver, W.L. and Finger, T.E. (1984) Electrophysiologtcal examination of a non-olfactory, non-gustatory chemosense in the sea robin, Prionotus carolinus, J. Comp. Physiol. A 154, 167-174 A molecularapproachto the evolutionof vertebrate pairedappendages Paolo Sordino and Denis Duboule he origin and the strucOver the past few years, genes involved a comparative analysis of molecutural transformation of in the ontogenesis of tetrapod limbs lar mechanisms. paired appendages is a have been isolated and characterized. The elusive origin of paired fundamental trait of verteSome of the developmental mechanisms appendicular systems has pre brate evolution. Since the recogniresponsible for the morphogenesis eluded the identification of the tion of structural homology among of these complex structures can now progenitor organisms from which tetrapod limbs, the existence of a be investigated through a new such endoskeletons originated. unique developmental programme approach. In addition, these genes can Thus, the history of fins remains for limb patterning has been proserve as tools to re-evaluate some speculative. It is generally be posed. Basic instructions would aspects of the long-standing question lieved that early chordates had a constitute an informational groundof the Rn-to-limb transition. Comparative continuous median fin fold along plan on which species-specific molecular developmental biology is the dorsal-ventral axis. This fold, neontological customizations are similar to that found in cephaloproviding new insight into the generated. Paleontological and similarities and differences in the chordates and some urochordate embryological (experimental and morphologies of these homologous larvae, may have allowed unducomparative) observations have latory movement in the aquatic structures. led to various conceptual frameenvironment. A further improveworks for understanding the origin ment of hydrodynamism and moPaolo Sordino and Denis Duboule are at the Dept of and evolution of tetrapod limbs tility was achieved by the ap Zoology and Animal Biology, University of Geneva, (reviewed in Refs 1,2). Yet our pearance of fin-like paired lateral Sciences Ill, Quai Ernest Ansermet 30, knowledge of the transformational structures during the evolution 1211 Geneva 4, Switzerland. sequence between lower and of early vertebrates. The jawless higher vertebrates is still too ostracoderms (Ordovician and scarce for the evolutionary history Devonian; 480-350 million years of lateral appendages to be described unequivocally. In ago) exhibited different types of appendages. Spines, cornuae and plates1 were probably derived from the dermal this context, the study of the evolution of basic morphobody armour, and conferred stability rather than propulsion, genetic and molecular programmes in vertebrates may be in the absence of air-filled swim bladders. However, some informative. That the underlying biomolecular systems have retained some important features during millions of fossil ostracoderms show anterior paired appendages, years suggests that minimal variations within such sys- which may be representative of the oldest genuine pectoral tems may have been a source of morphological evolution fins. Nevertheless, the earliest occurrence of both flexible (macroevolution)sv4. To learn how conserved molecules pectoral and pelvic fins (phylogenetically related to modern may generate morphological diversity requires detailed fish fins) has been found in a heterogeneous array of early functional comparisons, with emphasis on an evolutionjawed fish fossils from the late Silurian (410 million years ago)iJ. It is clear that this innovation was a successful soluary perspective. Here, we use recent molecular data (obtained while studying teleost fin morphogenesis) to tion to the need for locomotion, since these systems have assess how evolutionary scenarios built upon palaeonundergone wide functional radiation and morphological tological and ontogenetic evidence can be reconciled with evolution during vertebrate phylogeny. T 114 0 1996, Elsevier Science Ltd TREE vol. II, no. 3 March 1996
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