Your Inner Fish: A Journey Into the 3.5-Billion-Year History of the Human Body

by Neil Shubin

  CHAPTER SIX THE BEST-LAID (BODY) PLANS

  The origin of body plans has been the subject of a number of book-length treatments. For one with an exceptional scope and bibliography, go to J. Valentine, On the Origin of Phyla (Chicago: University of Chicago Press, 2004).

  There have been several biographies of von Baer. A short one is Jane Oppenheimer, “Baer, Karl Ernst von,” in C. Gillespie, ed., Dictionary of Scientific Biography, vol. 1 (New York: Scribners, 1970). For more detailed treatments, see Autobiography of Dr. Karl Ernst von Baer, ed. Jane Oppenheimer (1986; originally published in German, 2nd ed., 1886). See also B. E. Raikov, Karl Ernst von Baer, 1792–1876, trans. from Russian (1968), and Ludwig Stieda, Karl Ernst von Baer, 2nd ed. (1886). All these resources have large bibliographies. See also S. Gould, Ontogeny and Phylogeny (Cambridge, Mass.: Harvard University Press, 1977), for a discussion of von Baer’s laws.

  Spemann and Mangold’s experiments are discussed in embryology textbooks: S. Gilbert, Developmental Biology, 8th ed. (Sunderland, Mass.: Sinauer Associates, 2006). A modern genetic perspective on the Organizer is contained in De Robertis, E. M. (2006) Spemann’s organizer and self regulation in amphibian embryos, Nature Reviews 7:296–302, and De Robertis, E. M., and Arecheaga, J. The Spemann Organizer: 75 years on, International Journal of Developmental Biology 45 (special issue).

  For access to the huge literature on Hox genes and evolution, the best starting reference is Sean Carroll’s recent book Endless Forms Most Beautiful (New York: Norton, 2004). A recent review and interpretation of the ways that genes allow us to understand the common ancestor of bilaterally symmetrical animals is in Erwin, D., and Davidson, E. H. (2002) The last common bilaterian ancestor, Development 129:3021–3032.

  A number of investigators argue that a genetic “flip” between the body plan of an anthropod and the body plan of a human happened sometime in the distant past. This idea is discussed in De Robertis, E., and Sasai, Y. (1996) A common plan for dorsoventral patterning in Bilateria, Nature 380:37–40. Historical perspective on St. Hilaire’s views, as well as other controversies in the early years of comparative anatomy, are found in T. Appel, The Cuvier-Geoffroy Debate: French Biology in the Decades Before Darwin (New York: Oxford University Press, 1987). Data from acorn worms does not easily fit this model, and suggests that in some taxa the map between gene activity and axis specification may have evolved. For this work, see Lowe, C. J., et al. (2006) Dorsoventral patterning in hemichordates: insights into early chordate evolution, PLoS Biology online access: http://dx.doi.org/journal.0040291.

  The evolution of the genes that determine the body axes is reviewed in Martindale, M. Q. (2005) The evolution of metazoan axial properties, Nature Reviews Genetics 6:917–927. Body plan genes in cnidarians (jellyfish, sea anemones, and their relatives) are discussed in a series of primary papers: Martindale, M. Q., Finnerty, J. R., Henry, J. (2002) The Radiata and the evolutionary origins of the bilaterian body plan, Molecular Phylogenetics and Evolution 24:358–365; Matus, D. Q., Pang, K., Marlow, H., Dunn, C., Thomsen, G., Martindale, M. (2006) Molecular evidence for deep evolutionary roots of bilaterality in animal development, Proceedings of the National Academy of Sciences 103:11195–11200; Chourrout, D., et al. (2006) Minimal protohox cluster inferred from bilaterian and cnidarian Hox complements, Nature 442:684–687; Martindale, M., Pang, K., Finnerty, J. (2004) Investigating the origins of triploblasty: “mesodermal” gene expression in a diploblastic animal, the sea anemone Nemostella vectensis (phylum, Cnidaria; class, Anthozoa), Development 131:2463–2474; Finnerty, J., Pang, K., Burton, P., Paulson, D., Martindale, M. Q. (2004) Deep origins for bilateral symmetry: Hox and Dpp expression in a sea anemone, Science 304:1335–1337.

  CHAPTER SEVEN ADVENTURES IN BODYBUILDING

  Three key articles review the origins and evolution of bodies and offer an integrative perspective on genetics, geology, and ecology: King, N. (2004) The unicellular ancestry of animal development, Developmental Cell 7:313–325; Knoll, A. H., and Carroll, S. B. (1999) Early animal evolution: Emerging views from comparative biology and geology, Science 284:2129–2137; Brooke, N. M., and Holland, P. (2003) The evolution of multicellularity and early animal genomes, Current Opinion in Genetics and Development 13:599–603. All three papers are well referenced and offer a good introduction to the topics of the chapter.

  For stimulating treatments of the consequences of the origin of bodies and of other new forms of biological organization, see L. W. Buss, The Evolution of Individuality (Princeton: Princeton University Press, 2006), and J. Maynard Smith, and E. Szathmary, The Major Transitions in Evolution (New York: Oxford University Press, 1998).

  The story behind the Ediacarian animals is covered, with references, in Richard Fortey’s Life: A Natural History of the First Four Billion Years of Life on Earth (New York: Knopf, 1998), and Andrew Knoll’s Life on a Young Planet (Princeton: Princeton University Press, 2002).

  The experiment that yielded “proto-bodies” from “no-bodies” is described in Boraas, M. E., Seale, D. B., Boxhorn, J. (1998) Phagotrophy by a flagellate selects for colonial prey: A possible origin of multicellularity, Evolutionary Ecology 12:153–164.

  CHAPTER EIGHT MAKING SCENTS

  The University of Utah has an effective website, Learn. Genetics, that provides a wonderfully simple kitchen protocol for extracting DNA. The URL is http://learn.genetics.utah.edu/units/activities/extraction/.

  The evolution of the so-called odor genes or, more precisely, olfactory receptor genes has a large literature. Buck and Axel’s seminal paper is Buck, L., and Axel, R. (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition, Cell 65:175–181.

  Comparative aspects of olfactory gene evolution are treated in Young, B., and Trask, B. J. (2002) The sense of smell: genomics of vertebrate odorant receptors, Human Molecular Genetics 11:1153–1160; Mombaerts, P. (1999) Molecular biology of odorant receptors in vertebrates, Annual Reviews of Neuroscience 22:487–509.

  Olfactory receptor genes in jawless fish are discussed in Freitag, J., Beck, A., Ludwig, G., von Buchholtz, L., Breer, H. (1999) On the origin of the olfactory receptor family: receptor genes of the jawless fish (Lampetra fluviatilis), Gene 226:165–174. The distinction between aquatic and terrestrial olfactory receptor genes is described in Freitag, J., Ludwig, G., Andreini, I., Rossler, P., Breer, H. (1998) Olfactory receptors in aquatic and terrestrial vertebrates, Journal of Comparative Physiology A 183:635–650.

  Human olfactory receptor evolution is discussed in a number of papers. This selection reflects the issues discussed in the text: Gilad, Y., Man, O., Lancet, D. (2003) Human specific loss of olfactory receptor genes, Proceedings of the National Academy of Sciences 100:3324–3327; Gilad, Y., Man, O., and Glusman, G. (2005) A comparison of the human and chimpanzee olfactory receptor gene repertoires, Genome Research 15:224–230; Menashe, I., Man, O., Lancet, D., Gilad, Y. (2003) Different noses for different people, Nature Genetics 34:143–144; Gilad, Y., Wiebe, V., Przeworski, M., Lancet, D., Paabo, S. (2003) Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates, PLoS Biology online access: http://dx.doi.org/journal.pbio.0020005.

  The notion of gene duplication as an important source of new genetic variation traces to the seminal work of Ohno almost forty years ago: S. Ohno, Evolution by Gene Duplication (New York: Springer-Verlag, 1970). A recent review of the issue that contains a discussion of both opsins and olfactory receptor genes is found in Taylor, J., and Raes, J. (2004) Duplication and divergence: the evolution of new genes and old ideas, Annual Reviews of Genetics 38:615–643.

  CHAPTER NINE VISION

  Opsin genes in the evolution of eyes have been described in a number of papers in recent years. Reviews of the basic biology and the consequences of opsin gene evolution include Nathans, J. (1999) The evolution and physiology of human color vision: insights from molecular genetic studies of visual pigments, Neuron 24:299–312; Dominy, N., Svenning, J. C., Li, W. H. (2
003) Historical contingency in the evolution of primate color vision, Journal of Human Evolution 44:25–45; Tan, Y., Yoder, A., Yamashita, N., Li, W. H. (2005) Evidence from opsin genes rejects nocturnality in ancestral primates, Proceedings of the National Academy of Sciences 102:14712–14716; Yokoyama, S. (1996) Molecular evolution of retinal and nonretinal opsins, Genes to Cells 1:787–794; Dulai, K., von Dornum, M., Mollon, J., Hunt, D. M. (1999) The evolution of trichromatic color vision by opsin gene duplication in New World and Old World primates, Genome 9:629–638.

  Detlev Arendt and Joachim Wittbrodt’s work on photoreceptor tissues was originally described in a paper from the primary literature: Arendt, D., Tessmar-Raible, K., Synman, H., Dorresteijn, A., Wittbrodt, J. (2004) Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain, Science 306:869–871. An associated commentary appeared with the piece: Pennisi, E. (2004) Worm’s light-sensing proteins suggest eye’s single origin, Science 306:796–797. An earlier review by Arendt provides the larger framework that he uses to interpret the discovery: Arendt, D. (2003) The evolution of eyes and photoreceptor cell types, International Journal of Developmental Biology 47:563–571. Further commentary can be found in Plachetzki, D. C., Serb, J. M., Oakley, T. H. (2005) New insights into photoreceptor evolution, Trends in Ecology and Evolution 20:465–467. Still more commentary on Arendt and Wittbrodt’s work by Bernd Fritzsch and Joram Piatigorsky appeared in a later issue of Science, with a comment-reply that discussed the notion that the origin of eyes may be extremely ancient, and traced to a very deep branch of our evolutionary tree. This text can be found in Science (2005) 308:1113–1114.

  A review of Walter Gehring’s work on Pax 6 and its consequences for eye evolution is contained in a personal account: Gehring, W. (2005) New perspectives on eye development and the evolution of eyes and photoreceptors, Journal of Heredity 96:171–184.

  Papers that look at the different possible relationships between conserved eye formation genes and the evolution of eye organs include Oakley, T. (2003) The eye as a replicating and diverging modular developmental unit, Trends in Ecology and Evolution 18:623–627, and Nilsson D.-E. (2004) Eye evolution: a question of genetic promiscuity, Current Opinion in Neurobiology 14:407–414.

  The relationship between the lens proteins in our eyes and those of larval sea squirts is discussed in Shimeld, S., Purkiss, A. G., Dirks, R.P.H., Bateman, O., Slingsby, C., Lubsen, N. (2005) Urochordate by-crystallin and the evolutionary origin of the vertebrate eye lens, Current Biology 15:1684–1689.

  CHAPTER TEN EARS

  The genetics of inner ear evolution is discussed in Beisel, K. W., and Fritzsch, B. (2004) Keeping sensory cells and evolving neurons to connect them to the brain: molecular conservation and novelties in vertebrate ear development, Brain Behavior and Evolution 64:182–197. Ear development and the genes behind it are discussed in Represa, J., Frenz, D. A., Van de Water, T. (2000) Genetic patterning of embryonic ear development, Acta Otolaryngolica 120:5–10.

  The transformation of the hyomandibula into the stapes is reviewed in comprehensive book-length treatments of the evolution of primitive fish or the origin of land-living animals: J. Clack, Gaining Ground (Bloomington: Indiana University Press, 2002); P. Janvier, Early Vertebrates (Oxford, Eng.: Oxford University Press, 1996). It is also discussed in recent research papers, including Clack, J. A. (1989) Discovery of the earliest known tetrapod stapes, Nature 342:425–427; Brazeau, M., and Ahlberg, P. (2005) Tetrapod-like middle ear architecture in a Devonian fish, Nature 439:318–321.

  The origin of the mammalian middle ear is discussed from the perspective of a scientific historian in P. Bowler, Life’s Spendid Journey (Chicago: University of Chicago Press, 1996). Key primary sources include: Reichert, C. (1837) Uber die Visceralbogen der Wirbeltiere im allgemeinen und deren Metamorphosen bei den Vogeln und Saugetieren, Arch. Anat. Physiol. Wiss. Med. 1837:120–222; Gaupp, E. (1911) Beiträge zur Kenntnis des Unterkiefers der Wirbeltiere I. Der Processus anterior (Folii) des Hammers der Sauger und das Goniale der Nichtsäuger, Anatomischer Anzeiger 39:97–135; Gaupp, E. (1911) Beiträge zur Kenntnis des Unterkiefers der Wirbeltiere II. Die Zusammensetzung des Unterkiefers der Quadrupeden, Anatomischer Anzeiger, 39:433–473; Gaupp, E. (1911) Beiträge zur Kenntnis des Unterkiefers der Wirbeltiere III. Das Probleme der Entstehung eines “sekundären” Kiefergelenkes bei den Säugern, Anatomischer Anzeiger, 39:609–666; Gregory, W. K. (1913) Critique of recent work on the morphology of the vertebrate skull, especially in relation to the origin of mammals, Journal of Morphology 24:1–42.

  Major literature on the origin of the mammalian jaw, chewing, and the three-boned middle ear includes Crompton, A. W. (1963) The evolution of the mammalian jaw, Evolution 17:431–439; Crompton, A. W., and Parker, P. (1978) Evolution of the mammalian masticatory apparatus, American Scientist 66:192–201; Hopson, J. (1966) The origin of the mammalian middle ear, American Zoologist 6:437–450; Allin, E. (1975) Evolution of the mammalian ear, Journal of Morphology 147:403–438.

  The evolutionary origin of Pax 2 and Pax 6 and the evolutionary link of ears and eyes to box jellyfish is discussed in Piatigorsky, J., and Kozmik, Z. (2004) Cubozoan jellyfish: an evo/devo model for eyes and other sensory systems, International Journal for Developmental Biology 48:719–729.

  Links of sensory receptor molecules to different molecules in bacteria are discussed in Kung, C. (2005) A possible unifying principle for mechanosensation, Nature 436:647–654.

  CHAPTER ELEVEN THE MEANING OF IT ALL

  The methods of phylogenetic systematics are discussed in a number of sources. Key primary literature includes the classic work of Willi Hennig, published originally in German (Grundzüge einer Theorie der phylogenetischen Systematik [Berlin: Deutscher Zentralverlag, 1950]) and translated into English more than a decade later (Phylogenetic Systematics, trans. D. D. Davis and R. Zangerl [Urbana: University of Illinois Press, 1966]).

  Methods of phylogenetic reconstruction, which form the basis for the chapter, are discussed in detail in P. Forey, ed., Cladistics: A Practical Course in Systematics (Oxford, Eng.: Clarendon Press, 1992); D. Hillis, C. Moritz, and B. Mable, eds., Molecular Systematics (Sunderland, Mass.: Sinauer Associates, 1996); R. DeSalle, G. Girbet, and W. Wheeler, Molecular Systematics and Evolution: Theory and Practice (Basel: BirkhauserVerlag, 2002).

  A comprehensive treatment of the phenomenon of independent evolution of similar features is in M. Sanderson and L. Hufford, Homoplasy: The Recurrence of Similarity in Evolution (San Diego: Academic Press, 1996).

  To see the tree of life and the different hypotheses for the relationships between living creatures, visit http://tolweb.org/tree/.

  The notion that our evolutionary history has medical implications has been the subject of several good recent books. For comprehensive and well-referenced treatments, see N. Boaz, Evolving Health: The Origins of Illness and How the Modern World Is Making Us Sick (New York: Wiley, 2002); D. Mindell, The Evolving World: Evolution in Everyday Life (Cambridge, Mass.: Harvard University Press, 2006); R. M. Nesse and G. C. Williams, Why We Get Sick: The New Science of Darwinian Medicine (New York: Vintage, 1996); W. R. Trevathan, E. O. Smith, and J. J. McKenna, Evolutionary Medicine (New York: Oxford University Press, 1999).

  The apnea example I derived from discussions with Nino Ramirez, chairman of the Department of Anatomy at the University of Chicago. The hiccup example is derived from Straus, C., et al. (2003) A phylogenetic hypothesis for the origin of hiccoughs, Bioessays 25:182–188. The human-bacterial gene switch used in the study of mitochondrial cardioencephalomyopathy was originally discussed in Lucioli, S., et al. (2006) Introducing a novel human mtDNA mutation into the Paracoccus denitriticans COX 1 gene explains functional deficits in a patient, Neurogenetics 7:51–57.

  ONLINE RESOURCES

  A number of websites and blogs carry accurate information and are updated frequently.

  http://www.ucmp.berkeley.edu/ Produced by the Museum of Paleontology at the University of California–Berkeley, this is
one of the best online resources on paleontology and evolution. It is continuously updated and revised.

  http://www.scienceblogs.com/loom/ This is Carl Zimmer’s blog, a well-written, timely, and thoughtful source of information and discussion on evolution.

  http://www.scienceblogs.com/pharyngula/ P. Z. Myers, a professor of developmental biology, writes this accessible, informative, and cutting-edge blog. This is a rich source of information, well worth following.

  Both Zimmer’s and Myers’s blogs are at http://www.scienceblogs.com, a site that contains a number of excellent blogs also worth following for information and commentary on recent discoveries. Blogs relevant to the theme of this book at that site include Afarensis, Tetrapod Zoology, Evolving Thoughts, and Gene Expression.

  http://www.tolweb.org/tree/ The Tree of Life Project provides a regularly updated and authoritative treatment of the relationships among all groups of life. Like the UCMP page at Berkeley, it also includes resources for learning about how evolutionary trees are made and interpreted.

  ACKNOWLEDGMENTS

  All the illustrations, except where noted, are by Ms. Kalliopi Monoyios (www.kalliopimonoyios.com). Kapi read drafts of the manuscript and not only improved the text but designed art that matched it. I have been truly fortunate to work with someone with so many talents. Scott Rawlins (Arcadia University) generously gave permission to use his elegant rendering of Sauripterus in Chapter 2. Ted Daeschler (Academy of Natural Sciences of Philadelphia) graciously provided his superb photos of the great Tiktaalik “C” specimen. Thanks are due to Phillip Donoghue (University of Bristol) and Mark Purnell (University of Leicester) for permission to use their rendering of the conodont tooth array, McGraw-Hill for permission to use the textbook figure that started the hunt for Tiktaalik, and Steven Campana of the Canadian Shark Research Laboratory for the photos of shark organs.