Read Your Inner Fish: A Journey Into the 3.5-Billion-Year History of the Human Body Online
Authors: Neil Shubin
A recent overview of the genetic basis of gill arch formation is found in Kuratani, S. (2004) Evolution of the vertebrate jaw: comparative embryology and molecular developmental biology reveal the factors behind evolutionary novelty,
Journal of Anatomy
205:335–347. Examples of the experimental manipulation of one gill arch into another, using genetic technologies, include Baltzinger, M., Ori, M., Pasqualetti, M., Nardi, I., Riji, F. (2005)
Hoxa 2
knockdown in
Xenopus
results in hyoid to mandibular homeosis,
Developmental Dynamics
234:858–867; Depew, M., Lufkin, T., Rubenstein, J. (2002) Specification of jaw subdivisions by
Dlx
genes,
Science
298:381–385.
A comprehensive, well-illustrated, and informative resource for early fossil records of skulls, heads, and primitive fish is reviewed in P. Janvier,
Early Vertebrates
(Oxford, Eng.: Oxford University Press, 1996). The paper describing
Haikouella,
the 530-million-year-old worm with gills, is Chen, J.-Y., Huang, D. Y., and Li, C. W. (1999) An early Cambrian craniate-like chordate,
Nature
402:518–522.
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. (2003) 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.