Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Deep homology and the origins of evolutionary novelty

Abstract

Do new anatomical structures arise de novo, or do they evolve from pre-existing structures? Advances in developmental genetics, palaeontology and evolutionary developmental biology have recently shed light on the origins of some of the structures that most intrigued Charles Darwin, including animal eyes, tetrapod limbs and giant beetle horns. In each case, structures arose by the modification of pre-existing genetic regulatory circuits established in early metazoans. The deep homology of generative processes and cell-type specification mechanisms in animal development has provided the foundation for the independent evolution of a great variety of structures.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Deep homology of eye development and the parallel evolution of animal eyes.
Figure 2: Deep homology of late-phase Hox expression.
Figure 3: The evolution of beetle horns by co-option of a limb-outgrowth program.

References

  1. 1

    Shubin, N., Tabin, C. & Carroll, S. Fossils, genes, and the evolution of animal limbs. Nature 388, 639–648 (1997). This paper provides an original description of deep homology and an analysis of the extensive developmental similarities between arthropod and vertebrate appendages.

    ADS  CAS  PubMed  Google Scholar 

  2. 2

    Gould, S. J. The Structure of Evolutionary Theory (Harvard Univ. Press, 2002). Gould's magnum opus has an extensive analysis of deep homology and the fundamental ways that parallel evolution is a major pattern of evolution.

    Google Scholar 

  3. 3

    Panganiban, G. et al. The origin and evolution of animal appendages. Proc. Natl Acad. Sci. USA 94, 5162–5166 (1997).

    ADS  CAS  PubMed  Google Scholar 

  4. 4

    Mercader, N. et al. Conserved regulation of proximodistal limb axis development by Meis1/Hth. Nature 402, 425–429 (1999).

    ADS  CAS  PubMed  Google Scholar 

  5. 5

    Capdevila, J. et al. Control of vertebrate limb outgrowth by the proximal factor Meis2 and distal antagonism of BMPs by Gremlin. Mol. Cell 4, 839–849 (1999).

    CAS  PubMed  Google Scholar 

  6. 6

    Darwin, C. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life (John Murray, 1859).

    Google Scholar 

  7. 7

    Salvini-Plawen, L. V. & Mayr, E. On the evolution of photoreceptors and eyes. Evol. Biol. 10, 207–263 (1977).

    Google Scholar 

  8. 8

    Halder, G., Callaerts, P. & Gehring, W. J. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila . Science 267, 1788–1792 (1995).

    ADS  CAS  PubMed  Google Scholar 

  9. 9

    Gehring, W. J. New perspectives on eye development and the evolution of eyes and photoreceptors. J. Hered. 96, 171–184 (2005).

    CAS  PubMed  Google Scholar 

  10. 10

    Kozmik, Z. Pax genes in eye development and evolution. Curr. Opin. Genet. Dev. 15, 430–438 (2005).

    CAS  PubMed  Google Scholar 

  11. 11

    Oakley, T. H. The eye as a replicating and diverging, modular developmental unit. Trends Ecol. Evol. 18, 623–627 (2003).

    Google Scholar 

  12. 12

    Arendt, D., Tessmar-Raible, K., Snyman, H., Dorresteijn, A. W. & Wittbrodt, J. Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science 306, 869–871 (2004). By showing that polychaetes have a 'vertebrate-type' opsin in their brains, this paper reveals how divergent eyes of bilaterians could have evolved from a common ancestor.

    ADS  CAS  PubMed  Google Scholar 

  13. 13

    Erclik, T., Hartenstein, V., Lipshitz, H. D. & McInnes, R. R. Conserved role of the Vsx genes supports a monophyletic origin for bilaterian visual systems. Curr. Biol. 18, 1278–1287 (2008).

    CAS  PubMed  Google Scholar 

  14. 14

    Pearse, J. S. & Pearse, V. B. Vision of cubomedusan jellyfishes. Science 199, 458 (1978).

    ADS  CAS  PubMed  Google Scholar 

  15. 15

    Yamasu, T. & Yoshida, M. Fine structure of complex ocelli of a cubomedusan, Tamoya bursaria . Cell Tissue Res. 170, 325–339 (1976).

    CAS  PubMed  Google Scholar 

  16. 16

    Kozmik, Z. et al. Assembly of the cnidarian camera-type eye from vertebrate-like components. Proc. Natl Acad. Sci. USA 105, 8989–8993 (2008).

    ADS  CAS  PubMed  Google Scholar 

  17. 17

    Suga, H., Schmid, V. & Gehring, W. J. Evolution and functional diversity of jellyfish opsins. Curr. Biol. 18, 51–55 (2008).

    CAS  PubMed  Google Scholar 

  18. 18

    Plachetzki, D. C., Degnan, B. M. & Oakley, T. H. The origins of novel protein interactions during animal opsin evolution. PLoS ONE 10, e1054 (2007).

    ADS  Google Scholar 

  19. 19

    Coates, M. I., Jeffery, J. E. & Ruta, M. Fins to limbs: what the fossils say. Evol. Dev. 4, 390–401 (2002).

    PubMed  Google Scholar 

  20. 20

    Shubin, N. The evolution of paired fins and the origin of the tetrapod limb: phylogenetic and transformational approaches. Evol. Biol. 28, 39–86 (1995).

    Google Scholar 

  21. 21

    Shubin, H. Daeschler, E. B. & Jenkins, F. A. The pectoral fin of Tiktaalik roseae and the origin of the tetrapod limb. Nature 440, 764–771 (2006). The description of the pectoral fin and shoulder of T. roseae shows how the closest relatives to tetrapods evolved supporting appendages using components of the tetrapod autopod.

    ADS  CAS  PubMed  Google Scholar 

  22. 22

    Sordino, P. & Duboule, D. A molecular approach to the evolution of vertebrate paired appendages. Trends Ecol. Evol. 11, 114–119 (1996).

    CAS  PubMed  Google Scholar 

  23. 23

    Sordino, P., Hoeven, F. V. D. & Duboule, D. Hox gene expression in teleost fins and the origin of vertebrate digits. Nature 375, 678–681 (1995).

    ADS  CAS  PubMed  Google Scholar 

  24. 24

    Zakany, J., Fromental-Ramain, C., Warot, X. & Duboule, D. Regulation of number and size of digit by posterior Hox genes: a dose dependent mechanism with potential evolutionary implications. Proc. Natl Acad. Sci. USA 94, 13695–13700 (1997).

    ADS  CAS  PubMed  Google Scholar 

  25. 25

    Wagner, G. P. & Chiu, C.-H. The tetrapod limb: a hypothesis on its origin. J. Exp. Zool. 291, 226–240 (2001).

    CAS  PubMed  Google Scholar 

  26. 26

    Spitz, F., Gonzalez, F. & Duboule, D. A global control region defines a chromosomal regulatory landscape containing the HoxD cluster. Cell 113, 405–417 (2003).

    CAS  PubMed  Google Scholar 

  27. 27

    Davis, M. C., Dahn, R. D. & Shubin, N. H. An autopodial-like pattern of Hox expression in the fins of a basal actinopterygian fish. Nature 447, 473–476 (2007).

    ADS  CAS  PubMed  Google Scholar 

  28. 28

    Johanson, Z. et al. Fish fingers: digit homologues in sarcopterygian fish fins. J. Exp. Zool. 308, 757–768 (2007).

    Google Scholar 

  29. 29

    Ahn, D.-G. & Ho, R. K. Hox genes and development of paired fins in teleost: an alternative view. Dev. Biol. 295, 419–435 (2008).

    Google Scholar 

  30. 30

    Freitas, R., Zhang, G. & Cohn, M. Biphasic Hoxd gene expression in shark paired fins reveals an ancient origin of the distal limb domain. PLoS ONE 2, e754 (2007).

    ADS  PubMed  PubMed Central  Google Scholar 

  31. 31

    Boisvert, C. A., Mark-Kurik, E. & Ahlberg, P. The pectoral fin of Panderichthys and the origin of digits. Nature 456, 636–638 (2008).

    ADS  CAS  PubMed  Google Scholar 

  32. 32

    Darwin, C. The Descent of Man, and Selection in Relation to Sex (John Murray, 1871).

    Google Scholar 

  33. 33

    Hunt, J. & Simmons, L. W. Status-dependent selection in the horn-dimorphic beetle Onthophagus taurus . Proc. R. Soc. Lond. B 268, 2409–2414 (2001).

    CAS  Google Scholar 

  34. 34

    Moczek, A. P. & Nagy, L. M. Diverse development mechanisms contribute to different levels of diversity in horned beetles. Evol. Dev. 7, 175–185 (2005).

    PubMed  Google Scholar 

  35. 35

    Moczek, A. P. Integrating micro- and macroevolution of development through the study of horned beetles. Heredity 97, 168–178 (2006).

    CAS  PubMed  Google Scholar 

  36. 36

    Moczek, A. P., Rose, D., Sewell, W. & Kesselring, H. R. Conservation, innovation, and the evolution of horned beetle diversity. Dev. Genes Evol. 216, 655–665 (2006).

    PubMed  Google Scholar 

  37. 37

    Arrow, G. H. Horned Beetles (Junk, 1951).

    Google Scholar 

  38. 38

    Moczek, A. P., Cruickshank, T. E. & Shelby, A. When ontogeny reveals what phylogeny hides: gain and loss of horns during development and evolution of horned beetles. Evolution 60, 2329–2341 (2006).

    PubMed  Google Scholar 

  39. 39

    Emlen, D. J., Lavine, L. C. & Ewen-Campen, B. On the origin and evolutionary diversification of beetle horns. Proc. Natl Acad. Sci. USA 104, 8661–8668 (2007).

    ADS  CAS  PubMed  Google Scholar 

  40. 40

    Denes, A. S. et al. Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell 129, 277–288 (2007).

    CAS  PubMed  Google Scholar 

  41. 41

    Pueyo, J. I., Lanfear, R. & Couso, J. P. Ancestral Notch-mediated segmentation revealed in the cockroach Periplaneta americana . Proc. Natl Acad. Sci. USA 105, 16614–16619 (2008).

    ADS  CAS  PubMed  Google Scholar 

  42. 42

    Tessmar-Raible, K. et al. Conserved sensory-neurosecretory cell types in annelid and fish forebrain: insights into hypothalamus evolution. Cell 129, 1389–1400 (2007).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

N.S. is supported by grants from the National Science Foundation and the National Geographic Society. C.T. is supported by grants from the National Institutes of Health. S.C. is an investigator of the Howard Hughes Medical Institute.

Author information

Affiliations

Authors

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Reprints and permissions information is available at http://www.nature.com/reprints.

Correspondence should be addressed to N.S. (nshubin@uchicago.edu).

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Shubin, N., Tabin, C. & Carroll, S. Deep homology and the origins of evolutionary novelty. Nature 457, 818–823 (2009). https://doi.org/10.1038/nature07891

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing