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Elasmobranch Central Nervous System Organization and Its Possible Evolutionary Significance

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Elasmobranch Central Nervous System Organization and Its Possible Evolutionary Significance AMER. ZOOL., 17:411-429 (1977). Elasmobranch Central Nervous System Organization and Its Possible Evolutionary Significance R. GLENN NORTHCUTT Division of Biological Sciences, University of Michigan, Ann Arbor, Michigan 48109 SYNOPSIS. Examination of shark brain:body ratios reveals that these taxa possess relative brain volumes in a range overlapping those of bony fish as well as birds and mammals. Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 Much of the variation is due to relative development of the telencephalon and cerebellum. Telencephalic weights vary from 24% in Squalus to 52% in Sphyrna. Analysis of the cytoarchitectonics of the shark brains reveals at least two patterns of development. Squalomorph sharks possess low brain:body ratios, and the telencephalon of these taxa possess well developed lateral ventricles and poorly developed pallial areas. The dienceph- alon is characterized by prominent periventricular laminae, and the cerebellum lacks foliation. The lamniform and carcharhiniform sharks are characterized by high brain: body ratios, and there is marked hypertrophy of the telencephalon. The roof (pallial) regions, as well as the diencephalon, are characterized by extensive cellular migrations. The cerebella of these forms possess extensive complex foliation. These brain patterns are compared with the brain organization of Holocephali, and I conclude that the holocephalans are a sister radiation of the elasmobranchs. Comparisons with bony fish and land vertebrates suggest that elasmobranchs have independently developed complex pallial fields and cerebellar foliation as a result of parallel evolutionary trends. INTRODUCTION neural features unique to any given ver- tebrate radiation and thus fail to consider One of these simple vertebrates is rep- resented by a selachian of the modern seas, the specific neural changes that are adap- somewhat specialized in certain directions, of tive. course, but retaining, withal, much of the ar- Thus I believe a major task of compara- chaic nervous organization from which higher tive neurobiology is to sample brain varia- brains have gradually evolved. Houser, 1901 tion among living taxa and to recognize In the past, most comparative I am extremely grateful to Dr. Louise Luckenbill- neuroanatomical studies were framed Edds, Mr. Leonard Compagno, and the Steinhart within typological considerations. The Aquarium for furnishing some of the specimens used brains of non-mammalian vertebrates in this study. Mr. Daniel Moreno and the staff of the Cleveland Aquarium devoted considerable time and were assumed to represent earlier, thus effort to the initial phase of my shark work. I have simpler, stages in the evolution of mamma- been fortunate to utilize facilities at the Duke Univer- lian brains. Attention was focused on rec- sity Marine Laboratory, and at the Marine Field ognizing neural features common to all Station (University of Delaware College of Marine vertebrates, and on describing the Studies) where Dr. Robert Boord and I have spent many pleasant, hopefully productive hours studying "phylogenetic level" of different brain di- shark brains. I have benefited greatly from the assis- visions. Neural features common to all tance of Mr. Gerrit Klay of Marathon, Florida, whose vertebrates clearly tell us little about spe- enthusiasm for sharks is exceeded only by his talent cific adaptations and thus evolution. At for collecting and maintaining these animals. His- best, features common to widely divergent tological preparations were done by Mrs. Alice Hartman, Mr. Ronald Nicholes and Mrs. Elizabeth species offer clues to the initial adaptation Reed; and art work by Mr. Donald Luce. Dr. Mark and the origin of vertebrates. Braford read the manuscript and provided many helpful suggestions. Dr. Timothy Neary also read the Similarly, it is fallacious to characterize manuscript and applied his considerable expertise in the brains of various vertebrate species as helping me with the statistical calculations. This work points on a linear, simple-to-complex scale was supported by grants from the National Institutes with mammalian brains at the acme. Such of Health (NS11006) and the National Science Foun- unilinear hierarchies fail to recognize the dation (GB-40134). 411 412 R. GLENN NORTHCUTT common morphological patterns and their MATERIALS AND METHODS adaptive significance, rather than to recon- struct the probable phylogenetic history of Gross anatomy brains "from fish to man." Only by sampl- The genera utilized in this analysis are ing the existing variation can common listed in Table 1. Those examined by the adaptive patterns be recognized. Once author are indicated by an asterisk, while such patterns are identified, hypotheses published accounts exist for all other gen- regarding their biological value can be era listed. formulated and tested. Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 In this paper, the gross variation in Brain:body data elasmobranch brains is described with par- ticular emphasis on sharks. Two patterns Brains of a number of elasmobranch or levels of neural organization are recog- species (Table 2) were perfused or fixed by nized, and our present knowledge regard- emersion in AFA. All specimens were ing shark CNS organization is reviewed. adults based on gonadal tissues and re- Neural similarities possibly due to parallel ported adult body lengths. AFA fixation evolution among sharks, birds and mam- results in an 8-9% reduction in brain mals are noted. weight, and all brain weights reported are TABLE 1. Elasmobranch CNS in literature or examined by author. (Those examined by author are indicated by an asterisk.) Class Chondrichthyes *Etmoptenis hihanus Subclass Holocephali Callorhynchus antarcticus *Squalus acanlhms (Kuhlenbeck and Niimi, 1969) (Johnston, 1911; Holmgren, 1922; Backstrom, 1924; Leghissa, 1962; Chimaera monstrosa Smeets and Nieuwenhuys, 1967) (Holmgren, 1922; Faucette, 1969) Deania rostrata *Hydrolagus colliei (Okada rf a/., 1969) (Kuhlenbeck and Niimi, 1969) Centroscylhum ritteri Subclass Elasmobranchii (Okada et al., 1969) Superorder Squalomorphii Order Pristiophoriformes Order Hexanchiformes Pristiophorus japonicus (Okada et al., 1969) Chlamydoselachus anguineus (Masai, 1961) Superorder Batoidea Hexanchus (KlapperseJa/., 1936) Order Rajiformes *Notorynchus maculatus *Rhinobatos produclus Heptraruhias *Platyrhinoidis triseriata (Johnston, 1911; Backstrom, 1924) Raja clavata Order Squaliformes (Johnston, 1911; Backstrom, 1924; Leghissa, 1962; Veselkin, 1965) Eimopterus lucifer (Okada «* a/., 1969; Masai et *Raja eglanteria al., 1973) ELASMOBRANCH CNS ORGANIZATION 413 TABLE 1. Elasmobranch CNS in literature or examined by author, (con't.) Order Pristiformes Lamna (Klapperse(a/., 1936) No known literature Order Carcharhiniformes Order Torpediniformes Scyliorhinus caniculus Torpedo ocellata (Haller, 1898; Edinger, 1901; (Backstrom, 1924; Hugosson, 1955; Johnston, 1911; Dart, 1920; Leghissa, 1962; Bruckmoser, 1973; Backstrom, 1924; Beccari, Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 Bruckmoser and Dieringer, 1973; 1930; Bruckmoser and Platte(a/., 1974) Dieringer, 1973; Platted al., 1974; Smeets and Nieuwenhuys, 1976) Order Myliobatiformes *Scyhorhinus retifer *Potamotrygon motoro Scyliorhinus stellans Myliobatis aquila (Johnston, 1911; Backstrom, 1924; (Johnston, 1911; Kappers el al., Leghissa, 1962) 1936) *Mustelus canis Superorder Squatinomorphii (Shaper, 1898; Houser, 1901; Backstrom, 1924; Gerlach, 1947; McCready and Boord, 1976) No known literature Mustelus laems Superorder Galeomorphii (Backstrom, 1924; Leghissa, 1962; P\att etal., 1974) Order Heterodontiformes *Heterodontus francisci *Triakis scyllia Heterodontus japonicus *Galeocerdo cuivieri (Masai, 1962; Kusunoki el al., (Ebbesson and Ramsey, 1968) 1973) Scohodon Order Orectolobiformes (Johnston, 1911; Masai, 1962) *Ginglymostoma cirratum (Ebbesson and Ramsey, 1968; *Carcharhinus floridanus Ebbesson and Heimer, 1970; Ebbesson and Schroeder, 1971; *Carcharhinus leucas Ebbesson, 1972; Cohen, et al., 1973; Ebbesson and Campbell, 1973 *Carcharhinus milberti Schroeder and Ebbesson, 1974; Schroeder and Ebbesson, 1975) *Apnonodon isodon Order Lamniformes *Negaprion brevirostris (Tester, 1963; Graeber and Ebbesson, 1972a) Odontaspis *Pnonace glauca (Okada e< a/., 1969) (Aronson, 1963; Okada etal, 1969) Mitsukurina owstoni (Masai et al., 1973) *Sphyrna lexvini Alopias *Sphyrna tiburo (Okada et al., 1969) Sphyrna zygaena (Okada etal., 1969) Carcharodon carcharias (Gilbert, 1963) Isurus oxyrinchus (Gilbert, 1963; Okada et al, 1969) 414 R. GLENN NORTHCUTT not corrected for this reduction. Reported they nor the meninges, blood vessels or body weights are from fresh, unfixed choroid plexus of the fourth ventricle were material. Additional data were utilized included in the brain division weights. from values cited by Crile and Quiring Each brain division was blotted im- (1940) and Ridet et al. (1973) and are mediately prior to weighing. A Mettler noted in Table 2. analytical balance (Model H10) was used Data for relative development of major for all measurements. The accuracy of ten brain divisions (Fig. 4) were obtained by repeated measurements on small brain di- immersing AFA fixed brains in fixative visions (0.003 g) was ± 1.6%. Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 and dissecting
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