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Molecular phylogenetic perspective on the evolution of the deep-sea fish genusCyclothone (Stomiiformes: Gonostomatidae)

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Abstract

A portion of mitochondrially encoded 12S and 16S ribosomal RNA genes were sequenced from 13 currently recognized species of the midwater deep-sea fish genusCyclothone (Stomiiformes: Gonostomatidae) and three gonostomatid outgroup taxa. Phylogenetic analyses using maximum parsimony and maximum likelihood methods were performed on unambiguously aligned, combined sequences (803 bp) of the two genes. The resultant tree topologies from the two methods were congruent, being robust and supported by various tree statistics, enabling the evolutionary history ofCyclothone to be described in detail. The molecular phylogeny demonstrated striking inconsistencies with previously proposed “natural groups”, although the latter could be confidently refuted by the molecular data. The most significant characteristic of the evolutionary history ofCyclothone was the independent acquisition of an apomorphic depth habitat from the relatively ancestral, lower mesopelagic habitat, by each of three major distinct lineages that had diverged earlier in their evolution. Moreover, such macroevolutionary habitat shifts had been necessarily accompanied by morphological and ecological novelties, presumably originating from paedomorphosis. Repeated evolution of such changes strongly suggests ontogenetic plasticity inCyclothone which could enable these fishes to acquire larval-like, simple organization of body structure. Such a body plan could help them subsist in food-poor surroundings and regulate reproductive variables that take advantage of increasing larval survival toward shallower depths. Recent speciation events, on the contrary, have produced contemporary sister species of allopatric (or microallopatric) distributions, but few morphological and ecological differences. Even if remarkable miniaturization has occurred, such as in the Mediterranean endemicC. pygmaea, it had to have been a simple truncation of ancestral species' ontogeny without attendance of any discernible paedomorphic features. On the basis of the fossil record, geological history of the Mediterranean region, and ectotherm molecular divergence rate, it was estimated thatCyclothone radiation had already started in the early-middle Miocene (17–20 million years ago).

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Literature Cited

  • Aharon, P., S. L. Goldstein, C. W. Wheeler and G. Jacobson. 1993. Sea-level events in the South Pacific linked with the Messinian salinity crisis. Geology, 21: 771–775.

    Article  CAS  Google Scholar 

  • Ahlstrom, E. H., W. J. Richards and S. H. Weitzman. 1984. Families Gonostomatidae, Sternoptychidae and associated stomiiform groups: development and relationships. Pages 184–198in H. G. Moser, W. J. Richards, D. M. Cohen, M. P. Fahay, A. W. Kendall, Jr. and S. L. Richardson, eds. Ontogeny and systematics of fishes. Am. Soc. Ichthy. Herpet. Spec. Publ. No. 1. Lawrence, Kansas.

  • Alberch, P. and E. A. Gale. 1983. Size dependence during the development of the amphibian foot. Colchicine-induced digital loss and reduction. J. Embryol. Exp. Morphol., 76: 177–197.

    CAS  PubMed  Google Scholar 

  • Alberch, P. and E. A. Gale. 1985. A developmental analysis of an evolutionary trend: digital reduction in amphibian. Evolution, 39: 8–23.

    Google Scholar 

  • Allard, M. W. and M. M. Miyamoto. 1992. Testing phylogenetic approaches with empirical data, as illustrated with the parsimony method. Mol. Biol. Evol., 9: 778–786.

    CAS  PubMed  Google Scholar 

  • Alves-Gomes, J., G. Ortí, M. Haygood, W. Heiligenberg and A. Meyer. 1995. Phylogenetic analysis of the South American electric fishes (order Gymnotiformes) and the evolution of their electrogenic system: a synthesis based on morphology, electrophysiology and mitochondrial sequence data. Mol. Biol. Evol., 12: 298–318.

    CAS  PubMed  Google Scholar 

  • Anderson, S., A. T. Bankier, B. G. Barrell, M. H. L. de Bruijn, A. R. Coulson, J. Drouin, I. C. Eperon, D. P. Nierlich, B. A. Roe, F. Sanger, P. H. Schreier, A. J. H. Smith, R. Staden and I. G. Young. 1981. Sequence and organization of the human mitochondrial genome. Nature, 290: 457–465.

    CAS  PubMed  Google Scholar 

  • Aughtry, R. H. 1953. The biology and ecology ofCyclothone signata Garman in the Monterey Bay area. Unpubl. M. A. thesis, Stanford Univ. California. iii+72 pp.

    Google Scholar 

  • Badcock, J. 1982. A new species of the deep-sea fish genusCyclothone Goode & Bean (Stomiatoidei, Gonostomatidae) from the tropical Atlantic. J. Fish Biol., 20: 197–211.

    Article  Google Scholar 

  • Badcock, J. 1984. Gonostomatidae. Pages 284–301in P. J. P. Whitehead, M.-L. Bauchot, J.-C. Hureau, J. Nielsen and E. Tortonese, eds. Fishes of the North-eastern Atlantic and the Mediterranean. Vol. I. UNESCO, Paris.

    Google Scholar 

  • Badcock, J. 1986. Aspects of the reproductive biology ofGonostoma bathyphilum (Gonostomatidae). J. Fish Biol., 29: 589–603.

    Article  Google Scholar 

  • Badcock, J. and N. R. Merrett. 1976. Midwater fishes in the eastern North Atlantic—I. Vertical distribution and associated biology in 30°N, 23°W, with developmental notes on certain myctophids. Prog. Oceanogr., 7: 3–58.

    Article  Google Scholar 

  • Badcock, J. and N. R. Merrett. 1977. On the distribution of midwater fishes in the eastern North Atlantic. Pages 249–282in N. R. Andersen and B. J. Zahuranec, eds. Oceanic sound scattering prediction. Plenum Press, New York.

    Google Scholar 

  • Bailey, T. G. and B. H. Robison. 1986. Food availability as a selective factor on the chemical compositions of midwater fishes in the eastern North Pacific. Mar. Biol., 91: 131–141.

    Article  CAS  Google Scholar 

  • Bargelloni, L., P. A. Ritchie, T. Patarnello, B. Battaglia, D. M. Lambert and A. Meyer. 1994. Molecular evolution at subzero temperatures: mitochondrial and nuclear phylogenies of fishes from Antarctica (Suborder Notothenioidei), and the evolution of antifreeze glycopeptides. Mol. Biol. Evol., 11: 854–863.

    CAS  PubMed  Google Scholar 

  • Barham, E. G. 1971. Deep-sea fishes. Lethargy and vertical orientation. Pages 100–118in G. B. Farquhar, ed. Proceedings of an international symposium on biological sound scattering in the ocean. U. S. Gov. Print Office. Washington D.C.

    Google Scholar 

  • Berry, F. H. and H. C. Perkins. 1966. Survey of pelagic fishes of the California Current area. Fish. Bull., 65: 625–682.

    Google Scholar 

  • Boughton, D. A., B. B. Collette and A. R. McCune. 1991. Heterochrony in jaw morphology of needlefishes (Teleostei: Belonidae). Syst. Zool., 40: 329–354.

    Google Scholar 

  • Brooks, D. R. and D. A. McLennan. 1991. Phylogeny, ecology, and behavior: a research program in comparative biology. Univ. Chicago Press, Chicago. xii+434 pp.

    Google Scholar 

  • Chappill, J. A. 1989. Quantitative characters in phylogenetic analysis. Cladistics, 5: 217–234.

    Google Scholar 

  • Cita, M. B. 1982. The Messinian salinity crisis in the Mediterranean. A review. Geodynamics, 7: 113–140.

    Google Scholar 

  • David, L. R. 1943. Miocene fishes of southern California. Geol. Soc. Am. Spec. Pap., 43: 1–193.

    Google Scholar 

  • DeBry, R. W. 1992. Biogeography of new world taiga-dwellingMicrotus (Mammalia: Arvicolidae): a hypothesis test that accounts for phylogenetic uncertainty. Evolution, 46: 1347–1357.

    Google Scholar 

  • DeSalle, R., T. Freedman, E. M. Prager and A. C. Wilson. 1987. Tempo and mode of sequence evolution in mitochondrial DNA of HawaiianDrosophila. J. Mol. Evol.,26: 157–164.

    Article  CAS  PubMed  Google Scholar 

  • DeWitt, F. A., Jr. 1972. Bathymetric distributions of two common deep-sea fishes,Cyclothone acclinidens andC. signata, off southern California. Copeia, 1972: 88–96.

    Google Scholar 

  • Donoghue, M. J., R. G. Olmstead, J. F. Smith and J. D. Palmer. 1992. Phylogenetic relationships of the Dipsacales based onrbcL sequences. Ann. Missouri Bot. Gard., 79: 333–345.

    Google Scholar 

  • Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39: 783–791.

    Google Scholar 

  • Felsenstein, J. 1995. PHYLIP (phylogeny inference package), ver. 3.57c. Univ. of Washington, Seattle, Washington.

    Google Scholar 

  • Fisher, R. A. 1983. Protandric sex reversal inGonostoma elongatum (Pisces: Gonostomatidae) from the eastern Gulf of Mexico. Copeia, 1983: 554–557.

    Google Scholar 

  • Goodyear, R. H., B. J. Zahuranec, W. L. Pugh and R. H. Gibbs, Jr. 1972. Ecology and vertical distribution of Mediterranean midwater fishes. Pages 91–229. Mediterranean biological studies. Final report, Vol. I, Part 3. Smiths. Instit., Washington D.C.

    Google Scholar 

  • Gould, S. J. 1977. Ontogeny and phylogeny. Harvard Univ. Press, Cambridge, Massachusetts. xvi+501 pp.

    Google Scholar 

  • Grady, J. M. and W. H. LeGrande. 1993. Phylogenetic relationships, modes of speciation, and historical biogeography of the madtom catfishes genusNoturus Rafinesque (Siluriformes: Ictaluridae). Pages 747–777in R. L. Mayden, ed. Systematics, historical ecology, and North American freshwater fishes. Stanford Univ. Press, Stanford, California.

    Google Scholar 

  • Grey, M. 1964. Family Gonostomatidae. Pages 78–240in H. B. Bigelow, ed. Fishes of the western North Atlantic, No. 1 (Part 4). Mem. Sears Found. Mar. Res. Yale Univ, New Haven.

    Google Scholar 

  • Hanken, J. and D. B. Wake. 1993. Miniaturization of body size: organismal consequences and evolutionary significance. Annu. Rev. Ecol. Syst., 24: 501–519.

    Article  Google Scholar 

  • Harold, A. S. In press. Phylogenetic relationships of the Gonostomatidae. Bull. Mar. Sci.

  • Harold, A. S. and S. H. Weitzman. In press. Interrelationships of stomiiform fishes.In M. J. L. Stiassny, L. R. Parenti and G. D. Johnson, eds. The interrelationships of fishes revisited. Academic Press, New York.

  • Higgins, D. G. and P. M. Sharp. 1988. CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene, 73: 237–244.

    Article  CAS  PubMed  Google Scholar 

  • Hillis, D. M. and J. P. Huelsenbeck. 1992. Signal, noise, and reliability in molecular phylogenetic analyses. J. Heredity, 83: 189–195.

    CAS  Google Scholar 

  • Hsü, K. J., R. E. Garrison, L. Montadert, R. B. Kidd, D. Bernoulli, F. Mèlierés, M. B. Cita, C. Müller, A. Erickson and R. Wright. 1977. History of the Mediterranean salinity crisis. Nature, 267: 399–403.

    Article  Google Scholar 

  • Jespersen, P. and A. V. Tåning. 1926. Mediterranean Sternoptychidae. Report of the Danish oceanographical expeditions 1908–10 to the Mediterranean and adjacent seas, 2, A12: 1–59.

    Google Scholar 

  • Kawaguchi, K. 1973. Biology ofGonostoma gracile Günther (Gonostomatidae). II. Geographical and vertical distribution. J. Oceanogr. Soc. Japan, 29: 113–120.

    Article  Google Scholar 

  • Kawaguchi, K. and R. Marumo. 1967. Biology ofGonostoma gracile (Gonostomatidae). I. Morphology, life-history and sex-reversal. Inf. Bull. Planktol. Japan, Comem. No. Dr. Y. Matsue: 53–69.

  • Kobayashi, B. N. 1973. Systematics, zoogeography and aspects of the biology of the bathypelagic fish genusCyclothone in the Pacific Ocean. Unpubl. Ph. D. dissertation, Univ. of California, San Diego, xxvii+487 pp.

    Google Scholar 

  • Kumar, S., K. Tamura and M. Nei. 1993. MEGA: molecular evolutionary genetics analysis, ver. 1.0. The Pennsylvania State Univ. University Park, Pennsylvania.

    Google Scholar 

  • Lindsey, C. C. and A. N. Arnason. 1981. A model for responses of vertebral numbers in fish to environmental influences during development. Can. J. Fish. Aquat. Sci., 38: 334–347.

    Google Scholar 

  • Lynch, J. D. 1989. The gauge of speciation: on the frequency of modes of speciation. Pages 527–553in D. H. Otte and J. A. Endler, eds. Speciation and its consequences. Sinauer Assoc, Sunderland, Massachusetts.

    Google Scholar 

  • McKelvie, D. S. 1989. Latitudinal variation in aspects of the biology ofCyclothone braueri andC. microdon (Pisces: Gonostomatidae) in the eastern North Atlantic Ocean. Mar. Biol., 102: 413–424.

    Article  Google Scholar 

  • Maddison, W. P. and D. R. Maddison. 1992. Mac-Clade, ver. 3. Sinauer, Sunderland, Massachusetts. xii+398 pp.

    Google Scholar 

  • Marshall, N. B. 1984. Progenetic tendencies in deepsea fishes. Pages 91–101in G. W. Potts and R. J. Wooton, eds. Fish reproduction: strategies and tactics. Academic Press, London.

    Google Scholar 

  • Martin, A. P., G. J. P. Naylor and S. R. Palumbi. 1992. Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature, 357: 153–155.

    Article  CAS  PubMed  Google Scholar 

  • Martin, A. P. and S. R. Palumbi. 1993. Body size, metabolic rate, generation time, and the molecular clock. Proc. Natl. Acad. Sci. USA, 90: 4087–4091.

    CAS  PubMed  Google Scholar 

  • Maynard, S. D. 1982. Aspects of the biology of mesopelagic fishes of the genusCyclothone (Pisces: Gonostomatidae) in Hawaiian waters. Unpubl. Ph. D. dissertation, Univ. of Hawaii, Honolulu. xv+257 pp.

    Google Scholar 

  • Maynard, S. D., V. F. V. Riggs and J. F. Walters. 1975. Mesopelagic micronekton in Hawaiian waters: faunal composition, standing stock, and diel vertical migration. Fish. Bull., 73: 726–736.

    Google Scholar 

  • Mindell, D. P. 1991. Aligning DNA sequences: homology and phylogenetic weighting. Pages 73–89in M. M. Miyamoto and J. Cracraft, eds. Phylogenetic analysis of DNA sequences. Oxford Univ. Press, New York.

    Google Scholar 

  • Mindell, D. P. and R. L. Honeycutt. 1990. Ribosomal RNA in vertebrates: evolution and phylogenetic applications. Annu. Rev. Ecol. Syst., 21: 541–566.

    Article  Google Scholar 

  • Miya, M. 1994a.Cyclothone kobayashii, a new species of gonostomatid fish (Teleostei: Stomiiformes) from the Southern Ocean, with notes on its ecology. Copeia, 1994: 191–204.

    Google Scholar 

  • Miya, M. 1994b. First record ofCyclothone parapallida (Gonostomatidae) from the Pacific Ocean, with notes on its geographic distribution. Japan. J. Ichthyol., 41: 326–329.

    Google Scholar 

  • Miya, M. and T. Nemoto. 1985. Protandrous sex reversal inCyclothone atraria (family Gonostomatidae). Japan. J. Ichthyol., 31: 438–440.

    Google Scholar 

  • Miya, M. and T. Nemoto. 1986a. Reproduction, growth and vertical distribution of the mesopelagic fishCyclothone pseudopallida (family Gonostomatidae). Pages 830–837in T. Uyeno, R. Arai, T. Taniuchi and K. Matsuura, eds. Indo-Pacific fish biology: proceedings of the second international conference on Indo-Pacific fishes. Ichthyol. Soc. Japan, Tokyo.

    Google Scholar 

  • Miya, M. and T. Nemoto. 1986b. Life history and vertical distribution of the mesopelagic fishCyclothone alba (family Gonostomatidae) in Sagami Bay, central Japan. Deep-Sea Res., 33: 1053–1068.

    Article  Google Scholar 

  • Miya, M. and T. Nemoto. 1987. Some aspects of the biology of the micronektonic fishCyclothone pallida andC. acclinidens (family Gonostomatidae) in Sagami Bay, central Japan. J. Oceanogr. Soc. Japan, 42: 473–480.

    Google Scholar 

  • Miya, M. and T. Nemoto. 1991. Comparative life histories of the meso- and bathypelagic fishes of the genusCyclothone (Pisces: Gonostomatidae) in Sagami Bay, central Japan. Deep-Sea Res., 38: 67–89.

    Article  Google Scholar 

  • Miya, M., M. Yamaguchi and M. Okiyama. 1995. Midwater fishes off the Pacific coast of Boso Peninsula, central Japan: species composition, abundance, biomass, and zoogeographic affinities. Japan. J. Ichthyol., 42: 392–400.

    Google Scholar 

  • Moritz, C., T. E. Dowling and W. M. Brown, 1987. Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Annu. Rev. Ecol. Syst., 18: 269–292.

    Article  Google Scholar 

  • Mukhacheva, V. A. 1964. The composition of species of the genusCyclothone (Pisces, Gonostomatidae) in the Pacific Ocean. Trudy Inst. Okeanol., 73: 93–138. (in Russian with English summary.)

    Google Scholar 

  • Mukhacheva, V. A. 1967. Fishes of the genusCyclothone (Gonostomatidae). Pages 150–164in T. S. Rass, ed. Biology of the Pacific Ocean, Vol. 7, Book III. Ratisu, Tokyo. (In Japanese translated from Russian.)

    Google Scholar 

  • Mukhacheva, V. A. 1974. Cyclothones (gen.Cyclothone, fam. Gonostomatidae) of the world and their distributions. Trudy Inst. Okeanol., 96: 205–249. (In Russian with English summary.)

    Google Scholar 

  • Nelson, J. S. 1994. Fishes of the world, 3rd ed. John Wiley & Sons, New York. xx+600 pp.

    Google Scholar 

  • Ohe, F. 1993. Deep fish assemblage from the Middle Miocene Morozaki Group, southern part of Chita Peninsula, Aichi Prefecture, central Japan. Pages 169–262in The Tokai Fossil Society, ed. Fossils from the Miocene Morozaki Group. The Tokai Fossil Society, Nagoya. (In Japanese with English summary.)

    Google Scholar 

  • Palumbi, S., A. P. Martin, W. O. Romano, L. Stice and G. Grabowski. 1991. The simple fool's guide to PCR, ver. 2.0. Univ. of Hawaii, Honolulu.

    Google Scholar 

  • Pimentel, R. A. and R. Riggins. 1987. The nature of cladistic data. Cladistics, 3: 201–209.

    Google Scholar 

  • Smith, K. L., Jr. and M. B. Laver. 1981. Respiration of the bathypelagic fishCyclothone acclinidens. Mar. Biol., 61: 261–266.

    Google Scholar 

  • Swofford, D. L. 1993. PAUP: phylogenetic analysis using parsimony, ver. 3.1.1. Smiths. Inst., Washington.

    Google Scholar 

  • Templeton, A. R. 1983. Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of human and the apes. Evolution, 37: 221–244.

    CAS  Google Scholar 

  • Titus, T. A. and A. Larson. 1995. A molecular phylogenetic perspective on the evolutionary radiation of the salamander family Salamandridae. Syst. Biol., 44: 125–151.

    Google Scholar 

  • Weitzman, S. H. 1974. Osteology and evolutionary relationships of the Sternoptychidae, with a new classification of stomiatoid families. Bull. Am. Mus. Nat. Hist., (153): 327–478.

    Google Scholar 

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  1. Department of Zoology, Natural History Museum & Institute, Chiba, 955-2 Aoba-cho, Chuo-ku, 260, Chiba, Japan

    Masaki Miya

  2. Department of Marine Bioscience, Fukui Prefectural University, 1-1 Gakuen-cho, Obama, 917, Fukui, Japan

    Mutsumi Nishida

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  1. Masaki Miya
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Miya, M., Nishida, M. Molecular phylogenetic perspective on the evolution of the deep-sea fish genusCyclothone (Stomiiformes: Gonostomatidae). Ichthyological Research 43, 375–398 (1996). https://doi.org/10.1007/BF02347637

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