Skip to main content
SpringerLink
Log in

Ecological Developmental Biology: Interpreting Developmental Signs

  • Perspective
  • Published:
Biosemiotics Aims and scope Submit manuscript

Abstract

Developmental biology is a theory of interpretation. Developmental signals are interpreted differently depending on the previous history of the responding cell. Thus, there is a context for the reception of a signal. While this conclusion is obvious during metamorphosis, when a single hormone instructs some cells to proliferate, some cells to differentiate, and other cells to die, it is commonplace during normal development. Paracrine factors such as BMP4 can induce apoptosis, proliferation, or differentiation depending upon the history of the responding cells. In addition, organisms have evolved to alter their development in response to differences in temperature, diet, the presence of predators, or the presence of competitors. This allows them to develop the phenotype, within the limits imposed by the genotype, best suited for the immediate habitat of the organism. Most developing organisms have also evolved to expect developmental signals from symbionts, and these organisms develop abnormally if the symbiont signals are not present. Thus Hoffmeyer’s “vertical semiotic system” of genetic communication and “horizontal semiotic system” of ecological communication are integrated during development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Notes

  1. Here we see the sign/signal as being interpreted into a meaning that is not determined by the physical sign, itself, but by the context in which the sign is given. This will not be news to anyone who has studied immunology. It will also not be news to any traveler who has discovered that a “C” on a shower faucet has opposite meanings in Spain and England.

References

  • Agrawal, A. A., Laforsch, C., & Tollrian, R. (1999). Transgenerational induction of defenses in animals and plants. Nature, 401, 60–63.

    Article  CAS  Google Scholar 

  • Andersen, F. G., Jensen, J., Heller, R. S., Petersen, H. V., Larsson, L.-I., Madsen, O. D., & Serup, P. (1999). Pax6 and Pdx1 form a functional complex on the rat somatostatin gene upstream enhancer. FEBS Letters, 445, 315–320.

    Article  CAS  PubMed  Google Scholar 

  • Angier, N. (1992). A first step in putting genes into action: Bend the DNA. New YorkTimes, August 4, pp. C1, C7.

  • Bonner, J. T. (1958). The evolution of development. Cambridge: Cambridge University Press.

    Google Scholar 

  • Brucker, R. M., & Bordenstein, S. R. (2013). The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia. Science, 341(6146), 667–669.

    Article  CAS  PubMed  Google Scholar 

  • Cai, L., & Brown, D. D. (2004). Expression of type II iodothyronine deiodinase marks the time that a tissue responds to thyroid hormone-induced metamorphosis in Xenopus laevis. Developmental Biology, 266, 87–95.

    Article  CAS  PubMed  Google Scholar 

  • Chan, Y. F., Marks, M. E., Jones, F. C., Villarreal, G., Jr., Shapiro, M. D., Brady, S. D., Southwick, A. M., Absher, D. M., Grimwood, J., Schmutz, J., et al. (2010). Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science, 327, 302–305.

    Article  CAS  PubMed  Google Scholar 

  • Cvekl, A., & Piatigorsky, J. (1996). Lens development and crystallin gene expression: many roles for Pax-6. BioEssays, 18, 621–630.

    Article  CAS  PubMed  Google Scholar 

  • Dedeine, F., Vavre, F., Fleury, F., Loppin, B., Hochberg, M. E., & Bouletreau, M. (2001). Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proceedings of the National Academy of Sciences of the United States of America, 98, 6247–6252.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dimmitt, M. A., & Ruibal, R. (1980). Environmental correlates of emergence in spadefoot toads (Scaphiopus). Journal of Herpetology, 14, 21–29.

    Article  Google Scholar 

  • Dunbar, H. E., Wilson, A. C. C., Ferguson, N. R., & Moran, N. A. (2007). Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS Biology, 5, 1006–1015.

    Article  CAS  Google Scholar 

  • Gilbert, S. F. (2003). The genome in its ecological context: philosophical perspectives on interspecies epigenesis. Annals of the New York Academy of Science, 981, 202–218.

    Article  Google Scholar 

  • Gilbert, S. F. (2012). Ecological developmental biology: environmental signals for normal animal development. Evolution and Development, 14, 20–28.

    Article  PubMed  Google Scholar 

  • Gilbert, S. F. (2013). Developmental biology (10th ed.). Sunderland: Sinauer Associates.

    Google Scholar 

  • Gilbert, S. F., & Bard, J. (2014). Formalizing theories of development: A fugue on the orderliness of nature. In A. Minelli & Pradeu (Eds.), Towards a theory of development (pp. 129–143). Oxford: Oxford University Press.

    Chapter  Google Scholar 

  • Gilbert, S. F., & Epel, D. (2015). Ecological developmental biology. Sunderland: Sinauer Associates.

    Google Scholar 

  • Gilbert, S. F., McDonald, E., Boyle, N., Buttino, N., Gyi, L., Mai, M., Prakash, N., & Robinson, J. (2010). Symbiosis as a source of selectable epigenetic variation: taking the heat for the big guy. Philippine Trans.action on Royal Society B, 365, 671–678.

    Article  Google Scholar 

  • Gilbert, S. F., Sapp, J., & Tauber, A. I. (2012). A symbiotic view of life: We have never been individuals. Quarterly Review of Biology, 87, 325–341.

    Article  PubMed  Google Scholar 

  • Gluckman, P. D., & Hanson, M. A. (2007). Mismatch: Why our world no longer fits our bodies. Oxford: Oxford University Press.

    Google Scholar 

  • Griffiths, P. E., & Stotz, K. (2007). Gene. In D. Hull & M. Ruse (Eds.), Cambridge companion to the philosophy of biology (pp. 85–102). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Guenther, C., Pantalena-Filho, L., & Kingsley, D. M. (2008). Shaping skeletal growth by modular regulatory elements in the Bmp5 gene. PLoS Genetics, 4(12), e1000308.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoffmeyer, J., & Emmeche, C. (1991). Code-duality and the semiotics of nature. In M. Anderson & F. Merrell (Eds.), On semiotic modeling (pp. 117–166). New York: Mouton de Gruyter.

    Google Scholar 

  • Hooper, L. V., Wong, M. H., Thelin, A., Hansson, L., Falk, P. G., & Gordon, J. I. (2001). Molecular analysis of commensal host-microbial relationships in the intestine. Science, 291, 881–884.

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi, K., Sawada, K., Yamamoto, H., Wada, S., Saiga, H., & Nishida, H. (2003). Maternal Macho-1 is an intrinsic factor that makes cell response to the same FGF signal differ between mesenchyme and notochord induction in ascidian embryos. Development, 130, 5179–5190.

    Article  CAS  PubMed  Google Scholar 

  • Koropatnick, T. A., Engle, J. T., Apicella, M. A., Stabb, E. V., Goldman, W. E., & McFall-Ngai, M. J. (2004). Microbial factor-mediated development in a host bacterial mutualism. Science, 306, 1186–8.

    Article  CAS  PubMed  Google Scholar 

  • Laforsch, C., & Tollrian, R. (2004). Embryological aspects of inducible morphological defenses in Daphnia. Journal of Morphology, 262, 701–707.

    Article  PubMed  Google Scholar 

  • Laubichler, M. D., & Maienschein, J. (2005). Development. In M. C. Horowitz (Ed.), New dictionary of the history of ideas (pp. 570–574). Detroit: Thomson Gale.

    Google Scholar 

  • McFall-Ngai, M. J. (2002). Unseen forces: the influence of bacteria on animal development. Developmental Biology, 242, 1–14.

    Article  CAS  PubMed  Google Scholar 

  • McFall-Ngai, M., Hadfield, M. G., Bosch, T. C., Carey, H. V., Domazet-Lošo, T., Douglas, A. E., Dubilier, N., Eberl, G., Fukami, T., Gilbert, S. F., et al. (2013). Animals in a bacterial world: a new imperative for the life sciences. Proceedings of the National Academy of Sciences of the United States of America, 110, 3229–3236.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishida, H., & Sawada, K. (2001). macho-1 encodes a localized mRNA in ascidian eggs that specifies muscle fate during embryogenesis. Nature, 409, 724–729.

    Article  CAS  PubMed  Google Scholar 

  • Oyama, S. (1985). The ontogeny of information: Developmental systems and evolution. Durham: Duke University Press.

    Google Scholar 

  • Pradeu, T., Laplane, L., Prévot, K., Hoquet, T., Reynaud, V., Fusco, G., Minelli, A., Orgogozo, V., & Vervoort, M. (2016). Defining :development. Current Topics on Developmental Biology. doi:10.1016/bs.ctdb.2015.10.012.

    Google Scholar 

  • Relyea, R. (2004). Fine-tuned phenotypes: Tadpole plasticity under 16 combinations of predators and competitors. Ecology, 85, 172–179.

    Article  Google Scholar 

  • Rhee, K. J., Sethupathi, P., Driks, A., Lanning, D. K., & Knight, K. L. (2004). Role of commensal bacteria in development of gut-associated lymphoid tissue and preimmune antibody repertoire. Journal of Immunology, 172, 1118–1124.

    Article  CAS  Google Scholar 

  • Rosenberg, E., Sharon, G., & Zilber-Rosenberg, I. (2009). The hologenome theory of evolution: a fusion of neo-Darwinism and Lamarckism. Environmental Microbiology, 11, 2959–2962.

    Article  PubMed  Google Scholar 

  • Sabeter, B., van Ham, R. C. H. J., Martínez-Torres, D., Silva, F., Latorre, A., & Moya, A. (2001). Molecular-evolution of aphids and their primary (Buchnera sp.) and secondary endosymbionts: implications for the role of symbiosis in insect evolution. Interciencia, 26, 508–512.

    Google Scholar 

  • Saffo, M. B. (2006). Symbiosis: The way of all life. In J. Seckbach (Ed.), Life as we know it (pp. 325–339). New York: Springer.

    Google Scholar 

  • Shapiro, M. D., Marks, M. E., Peichel, C. L., Blackman, B. K., Nereng, K. S., Jónsson, B., Schluter, D., & Kingsley, D. M. (2004). Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature, 428, 717–723.

    Article  CAS  PubMed  Google Scholar 

  • Sharon, G., Segal, D., Ringo, J. M., Hefetz, A., Zilber-Rosenberg, I., & Rosenberg, E. (2010). Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 107, 20051–20056.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spemann, H. (1943). Forschung und Leben. Quoted. In T. J. Horder, J. A. Witkowski, & C. C. Wylie (Eds.), A history of embryology (p. 219). New York: Cambridge University Press.

    Google Scholar 

  • Stappenbeck, T. S., Hooper, L. V., & Gordon, J. I. (2002). Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proceedings of the National Academy of Sciences of the United States of America, 99, 15451–15455.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tournamille, C., Colin, Y., Cartron, J.-P., & Le Van Kim, C. (1995). Disruption of a GATA motif in the Duffy gene promoter abolishes erythroid gene expression in Duffy-negative individuals. Nature Genetics, 10, 224–228.

    Article  CAS  PubMed  Google Scholar 

  • Van Buskirk, J., & Relyea, R. A. (1998). Natural selection for phenotypic plasticity: predator-induced morphological responses in tadpoles. Biological Journal of the Linnean Society, 65, 301–328.

    Article  Google Scholar 

  • Vaughn, D., & Strathmann, R. R. (2008). Predators induce cloning in echinoderm larvae. Science, 319, 1503.

    Article  CAS  PubMed  Google Scholar 

  • Visick, K. L., & Ruby, G. E. (2006). Vibrio fischeri and its host: it takes two to tango. Current Opinions in Microbiology, 9, 1–7.

    Article  Google Scholar 

  • Waddington, C. H. (1940). Organizers and genes. Cambridge: Cambridge University Press.

    Google Scholar 

  • Waddington, C. H. (1957). The strategy of the genes. London: Allen & Unwin.

    Google Scholar 

  • Warkentin, K. M. (2005). How do embryos assess risk? vibrational cues in predator-induced hatching of red-eyed treefrogs. Animal Behavior, 70, 59–71.

    Article  Google Scholar 

  • Warkentin, K. M., Caldwell, M. S., & McDaniel, J. G. (2006). Temporal pattern cues in vibrational risk assessment by embryos of the red-eyed treefrog, Agalychnis callidryas. Journal of Experimental Biology, 209, 1376–1384.

    Article  PubMed  Google Scholar 

  • Zaffran, S., & Frasch, M. (2002). Early signals in cardiac development. Cardiovascular Research, 91, 457–469.

    CAS  Google Scholar 

Download references

Acknowledgments

This paper was funded by a faculty research grant from Swarthmore College and by National Science Foundation Grant IOS 145177.

Author information

Authors and Affiliations

  1. Department of Biology, Swarthmore College, Swarthmore, PA, USA

    Scott F. Gilbert

  2. Institute of Biotechnology, University of Helsinki, Helsinki, Finland

    Scott F. Gilbert

Authors
  1. Scott F. Gilbert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Scott F. Gilbert.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gilbert, S.F. Ecological Developmental Biology: Interpreting Developmental Signs. Biosemiotics 9, 51–60 (2016). https://doi.org/10.1007/s12304-016-9257-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12304-016-9257-4

Keywords

Search

Navigation