CSIRO Publishing blank image blank image blank image blank imageBooksblank image blank image blank image blank imageJournalsblank image blank image blank image blank imageAbout Usblank image blank image blank image blank imageShopping Cartblank image blank image blank image You are here: Journals > Australian Journal of Zoology   
Australian Journal of Zoology
Journal Banner
  Evolutionary, Molecular and Comparative Zoology
blank image Search
blank image blank image
blank image
  Advanced Search

Journal Home
About the Journal
Editorial Structure
Online Early
Current Issue
Just Accepted
All Issues
Special Issues
Sample Issue
For Authors
General Information
Submit Article
Author Instructions
Open Access
Awards and Prizes
For Referees
Referee Guidelines
Review an Article
Annual Referee Index
For Subscribers
Subscription Prices
Customer Service
Print Publication Dates
Library Recommendation

blue arrow e-Alerts
blank image
Subscribe to our Email Alert or RSS feeds for the latest journal papers.

red arrow Connect with us
blank image
facebook twitter logo LinkedIn


Open Access Article << Previous     |     Next >>   Contents Vol 62(1)

The evolution of morphogenetic fitness landscapes: conceptualising the interplay between the developmental and ecological drivers of morphological innovation

Charles R. Marshall

Department of Integrative Biology and University of California Museum of Paleontology, University of California, Berkeley, CA 94720, USA. Email: crmarshall@berkeley.edu

Australian Journal of Zoology 62(1) 3-17 http://dx.doi.org/10.1071/ZO13052
Submitted: 11 July 2013  Accepted: 8 January 2014   Published: 13 February 2014

 Full Text
 PDF (1.6 MB)
 Export Citation

Here I show how fitness landscapes can be used to understand the relative importance of developmental and ecological change in initiating morphological innovation. Key is the use of morphogenetic ‘rules’ as the axes of the landscape, which enables explicit incorporation of the contribution that specific morphologies make to fitness. Four modes of fitness landscape evolution are identified: (1) change in the density of peaks on the landscape, driven by an increase in the number of selective pressures encountered; (2) change in the dimensionality of the landscape through the addition of morphogenetic rules; (3) change in the size of one or more dimensions of the landscape through elaboration of already existing morphogenetic rules; and, (4) shifting the position of peaks in the landscape. Morphological innovation is initiated by ecological change in Mode (1), for example the Cambrian explosion of animals, and Mode (4), for example, when taxa such as sticklebacks make a shift in environment, or during coevolutionary escalation. Morphological change is initiated by developmental innovation for Mode (2), typified by some macroevolutionary innovations, such as the emergence of jaws, and in Mode (3), for example, in the differentiation of flower morphology facilitated by gene duplication of the B-class developmental genes.


Alroy, J. (1998). Cope’s Rule and the dynamics of body mass evolution in North American fossil mammals. Science 280, 731–734.
CrossRef | CAS | PubMed |

Arnold, S. J., Pfrender, M. E., and Jones, A. G. (2001). The adaptive landscape as a conceptual bridge between micro- and macroevolution. Genetica 112/113, 9–32.
CrossRef |

Bell, M. A., and Foster, S. A. (1994). ‘The Evolutionary Biology of the Threespine Stickleback.’ (Oxford University Press: Oxford.)

Bell, M. A., Travis, M. P., and Blouw, D. M. (2006). Inferring natural selection in a fossil threespine stickleback. Paleobiology 32, 562–577.
CrossRef |

Brodie, E. D., and Ridenhour, B. J. (2003). Reciprocal selection at the phenotypic interface of coevolution. Integrative and Comparative Biology 43, 408–418.
CrossRef | PubMed |

Brodie, E. D., Moore, A. J., and Janzen, F. J. (1995). Visualizing and quantifying natural selection. Trends in Ecology & Evolution 10, 313–318.
CrossRef |

Brodie, E. D., Feldman, C. R., Hanifin, C. T., Motychak, J. E., Mulcahy, D. G., Williams, B. L., and Brodie, E. D. (2005). Parallel arms races between garter snakes and newts involving tetrodotoxin as the phenotypic interface of coevolution. Journal of Chemical Ecology 31, 343–356.
CrossRef | CAS | PubMed |

Calcott, B. (2008). Assessing the fitness landscape revolution. Biology and Philosophy 23, 639–657.
CrossRef |

Calsbeek, R., Gosden, T. P., Kuchta, S. R., and Svensson, E. I. (2012). Fluctuating selection and dynamic adaptive landscapes. In ‘The Adaptive Landscape in Evolutionary Biology’. (Eds E. I. Svensson and R. Calsbeek.) pp. 89–109. (Oxford University Press: Oxford.)

Carroll, S. B., Grenier, J. K., and Weatherbee, S. D. (2001). ‘From DNA to Diversity.’ (Blackwell Science: Oxford.)

Chan, Y. F., Marks, M. E., Jones, F. C., Villarreal, G., Shapiro, M. D., Brady, S. D., Southwick, A. M., Absher, D. M., Grimwood, J, Schmutz, J, Myers, R. M., Petrov, D, Jónsson, B, Schluter, D, Bell, M. A., and Kingsley, D. M. (2010). Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327, 302–305.
CrossRef | CAS | PubMed |

Csete, M. E., and Doyle, J. C. (2002). Reverse engineering of biological complexity. Science 295, 1664–1669.
CrossRef | CAS | PubMed |

Davidson, E. H. (2006). ‘The Regulatory Genome: Gene Regulatory Networks in Development and Evolution.’ (Academic Press: Oxford.)

Davidson, E. H. (2010). Emerging properties of animal gene regulatory networks. Nature 468, 911–920.
CrossRef | CAS | PubMed |

Davidson, E. H., and Erwin, D. H. (2006). Gene regulatory networks and the evolution of animal body plans. Science 311, 796–800.
CrossRef | CAS | PubMed |

Erwin, D. H., and Davidson, E. H. (2009). The evolution of hierarchical gene regulatory networks. Nature Reviews. Genetics 10, 141–148.
CrossRef | CAS | PubMed |

Erwin, D. H., and Valentine, J. W. (2013). ‘The Cambrian Explosion: The Construction of Animal Biodiversity.’ (Roberts and Company: Greenwood Village, CO.)

Estes, S., and Arnold, S. J. (2007). Resolving the paradox of stasis: models with stabilizing selection explain evolutionary divergence on all timescales. American Naturalist 169, 227–244.
CrossRef | PubMed |

Gavrilets, S. (2004). ‘Fitness Landscapes and the Origin of Species.’ (Princeton University Press: Princeton.)

Gerhart, J., and Kirschner, M. (1997). ‘Cells, Embryos, and Evolution.’ (Blackwell Science: Oxford.)

Gilbert, S. F., and Epel, D. (2009). ‘Ecological Developmental Biology.’ (Sinauer Associates: Sunderland, MA.)

Gingerich, P. D. (1983). Rates of evolution: effects of time and temporal scaling. Science 222, 159–161.
CrossRef | CAS | PubMed |

Gould, S. J. (1980). The promise of paleobiology as a nomothetic, evolutionary discipline. Paleobiology 6, 96–118.

Gould, S. J. (1989). ‘Wonderful Life: The Burgess Shale and the Nature of History.’ (W.W. Norton and Co.: New York.)

Gould, S. J., and Eldredge, N. (1993). Punctuated equilibrium comes of age. Nature 366, 223–227.
CrossRef | CAS | PubMed |

Green, D. A., and Extavour, C. G. (2012). Convergent evolution of a reproductive trait through distinct developmental mechanisms in Drosophila. Developmental Biology 372, 120–130.
CrossRef | CAS | PubMed |

Harper, M. (2009). The replicator equation as an inference dynamic. arXiv:0911.1763v3 [math.DS].

Hendry, P. H., Millien, V., Gonzalez, A., and Larsson, C. E. (2012). How humans influence evolution on adaptive lansdscapes. In ‘The Adaptive Landscape in Evolutionary Biology’. (Eds E. I. Svensson and R. Calsbeek.) pp. 180–202. (Oxford University Press: Oxford.)

Hertel, F. (1994). Diversity in body size and feeding morphology within past and present vulture assemblages. Ecology 75, 1074–1084.
CrossRef |

Hua, H., Pratt, B. R., and Zhang, L. (2003). Borings in Cloudina shells: complex predator–prey dynamics in the terminal Neoproterozoic. Palaios 18, 454–459.
CrossRef |

Hunt, G. (2007). The relative importance of directional change, random walks, and stasis in the evolution of fossil lineages. Proceedings of the National Academy of Sciences of the United States of America 104, 18404–18408.
CrossRef | CAS | PubMed |

Hunt, G., Bell, M. A., and Travis, M. P. (2008). Evolution towards a new adaptive optimum: phenotypic evolution in a fossil stickleback lineage. Evolution 62, 700–710.
CrossRef | PubMed |

Jones, F. C., Grabherr, M. G., Chan, Y. F., Russell, P., Mauceli, E., Johnson, J., Swofford, R., Pirun, M, Zody, M. C., White, S, Birney, E, Searle, S, Schmutz, J, Grimwood, J, Dickson, M. C., Myers, R. M., Miller, C. T., Summers, B. R., Knecht, A. K., Brady, S. D., Zhang, H, Pollen, A. A., Howes, T, Amemiya, C, Broad Institute Genome Sequencing Platform & Whole Genome Assembly Team Lander, E. S., Di Palma, F, Lindblad-Toh, K, and Kingsley, D. M. (2012). The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484, 55–61.
CrossRef | CAS | PubMed |

Kauffman, S. A. (1993). ‘Origins of Order: Self-organization and Selection in Evolution.’ (Oxford University Press: Oxford.)

Lande, R. (1976). Natural selection and random genetic drift in phenotypic evolution. Evolution 30, 314–334.
CrossRef |

Lande, R. (1979). Quantitative genetic analysis of multivariate evolution, applied to brain : body size allometry. Evolution 33, 402–416.
CrossRef |

Lewontin, R. C. (1974). ‘The Genetic Basis of Evolutionary Change.’ (Columbia University Press: New York.)

Litt, A., and Kramer, E. M. (2010). The ABC model and the diversification of floral organ identity. Seminars in Cell & Developmental Biology 21, 129–137.
CrossRef | CAS |

Lynch, M., and Force, A. (2000). The probability of gene preservation by subfunctionalization. Genetics 154, 459–473.
| CAS | PubMed |

Marshall, C. R. (1995). Darwinism in an Age of Molecular Revolution. In ‘Evolution and the Molecular Revolution’. (Eds C. R. Marshall and J. W. Schopf.) pp. 1–30. (Jones and Bartlett: Sudbury, MA.)

Marshall, C. R. (2003). Nomothetism and understanding the Cambrian “explosion”. Palaios 18, 195–196.
CrossRef |

Marshall, C. R. (2006). Explaining the Cambrian “explosion” of animals. Annual Review of Earth and Planetary Sciences 34, 355–384.
CrossRef | CAS |

Marshall, C. R. (2010). The next 150 years: towards a richer theoretical biology. In ‘Evolution Since Darwin: The First 150 Years’. (Eds M. A. Bell, D. J. Futuyma, W. F Eanes, and J. S. Levinton.) pp. 657–661. (Sinauer Associates: Sunderland, MA.)

Marshall, C. R., and Valentine, J. W. (2010). The importance of preadapted genomes in the origin of the animal bodyplans and the Cambrian explosion. Evolution 64, 1189–1201.
| PubMed |

McCune, A. R. (1990). Evolutionary novelty and atavism in the Semionotus complex: relaxed selection during colonization of an expanding lake. Evolution 44, 71–85.
CrossRef |

McGhee, G. R. (1999). ‘Theoretical Morphology: the Concept and its Application.’ (Columbia University Press: New York.)

McGhee, G. R. (2007). ‘The Geometry of Evolution. Adaptive Landscapes and Theoretical Morphospaces.’ (Cambridge University Press: Cambridge.)

McKinnon, J. S., and Rundle, H. D. (2002). Speciation in nature: the threespine stickleback model systems. Trends in Ecology & Evolution 17, 480–488.
CrossRef |

McMenamin, M. A. S. (2000). ‘The Garden of Ediacara.’ (Columbia University Press: New York.)

Niklas, K. J. (1994). Morphological evolution through complex domains of fitness. Proceedings of the National Academy of Sciences of the United States of America 91, 6772–6779.
CrossRef | CAS | PubMed |

Niklas, K. J. (1997). Effects of hypothetical developmental barriers and abrupt environmental changes on adaptive walks in a computer generated domain for early vascular land plants. Paleobiology 23, 63–76.

Niklas, K. J. (2004). Computer models of early land plant evolution. Annual Review of Earth and Planetary Sciences 32, 47–66.
CrossRef | CAS |

Pigliucci, M. (2012). Landscapes, surfaces, and morphospaces: what are they good for? (Eds E. I. Svenesson and R. Calsbeek.) pp. 26–38. (Oxford University Press: Oxford.)

Raup, D. M. (1966). Geometric analysis of shell coiling: general problems. Journal of Paleontology 40, 1178–1190.

Rice, S. H. (2004). ‘Evolutionary Theory: Mathematical and Conceptual Foundations.’ (Sinauer Associates: Sunderland, MA.)

Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
CrossRef | CAS | PubMed |

Ronquist, F., Teslenko, M., Van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L, Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
CrossRef | PubMed |

Salazar-Ciudad, I., and Jernvall, J. (2010). A computational model of teeth and the developmental origins of morphological variation. Nature 464, 583–586.
CrossRef | CAS | PubMed |

Schneider, I., and Shubin, N. H. (2013). The origin of the tetrapod limb: from expeditions to enhancers. Trends in Genetics 29, 419–426.
CrossRef | CAS | PubMed |

Simpson, G. G. (1944). ‘Tempo and Mode in Evolution.’ (Columbia University Press: New York.)

Simpson, G. G. (1953). ‘The Major Features of Evolution.’ (Columbia University Press: New York.)

Slater, G. J., Dumont, E. R., and Van Valkenburgh, B. (2009). Implications of predatory specialization for cranial form and function in canids. Journal of Zoology 278, 181–188.
CrossRef |

Thompson, J. N. (2005). ‘The Geographic Mosaic of Coevolution.’ (University of Chicago Press: Chicago.)

Tseng, Z. J. (2013). Testing adaptive hypotheses of convergence with functional landscapes: a case study of bone-cracking hypercarnivores. PLoS ONE 8, e65305.
CrossRef | CAS | PubMed |

Van Valen, L. (1973). Festschrift. Science 180, 488.

Van Valen, L. (1974). A natural model for the origin of some higher taxa. Journal of Herpetology 8, 109–121.
CrossRef |

Van Valkenburgh, B. (1995). Tracking ecology over geological time: evolution within guilds of vertebrates. Trends in Ecology & Evolution 10, 71–76.
CrossRef |

Vermeij, G. J. (1987). ‘Evolution and Escalation.’ (Princeton University Press: Princeton.)

Wade, M. J. (2012). Wright’s adaptive landscape: testing the predictions of his shifting balance theory. In ‘The Adaptive Landscape in Evolutionary Biology’. (Eds E. I. Svensson and R. Calsbeek.) pp. 58–73. (Oxford University Press: Oxford.)

Wagner, P. J. (2000). Exhaustion of morphological character states among fossil taxa. Evolution 54, 365–386.
| CAS | PubMed |

Wagner, A. (2011). ‘The Origins of Evolutionary Innovations: A Theory of Transformative Change in Living Systems.’ (Oxford University Press: Oxford.)

Wagner, P. J. (2012). Modelling rate distributions using character compatibility: implications for morphological evolution among fossil invertebrates. Biology Letters 8, 143–146.
CrossRef | PubMed |

Wagner, P. J., and Erwin, D. H. (2006). Patterns of convergence in general shell form among Paleozoic gastropods. Paleobiology 32, 316–337.
CrossRef |

Wagner, P. J., Ruta, M., and Coates, M. I. (2006). Evolutionary patterns in early tetrapods. II: Differing constraints on available character space among clades. Proceedings of the Royal Society of London. Series B, Biological Sciences 273, 2113–2118.
CrossRef |

West, K., and Cohen, A. (1996). Shell microstructure of gastropods from Lake Tanganyika, Africa: adaptation, convergent evolution, and escalation. Evolution 50, 672–681.
CrossRef |

West, K., Cohen, A., and Baron, M. (1991). Morphology and behavior of crabs and gastropods from Lake Tanganyika, Africa: implications for lacustrine predator–prey coevolution. Evolution 45, 589–607.
CrossRef |

Wolfram, S. (2002). ‘A New Kind of Science.’ (Wolfram Media: Champaign, IL.)

Wright, S. (1931). Evolution in Mendelian populations. Genetics 16, 97–159.
| CAS | PubMed |

Wright, S. (1932). The roles of mutation, inbreeding, crossbreeding and selection in evolution. In ‘Proceedings of the Sixth International Congress on Genetics. Volume 1’. (Ed. D. F. Jones.) pp. 356–366. (Austin, TX.)

Legal & Privacy | Contact Us | Help


© CSIRO 1996-2016