Skip to main content
Log in

Crossing fitness valleys during the evolution of limpet homing behaviour

  • Research Article
  • Published:
Central European Journal of Biology

Abstract

Evolution is often considered a gradual hill-climbing process, slowly increasing the fitness of organisms. Here I investigate evolution of homing behaviour in simulated intertidal limpets. While the simulation of homing is only a possible mechanism by which homing may have evolved, the process allows an investigation of how evolution may occur over different fitness landscapes. With some fitness landscapes, in order to evolve path integration as a homing mechanism, a temporary reduction in an organism’s fitness was required — since high developmental costs occurred before successful homing strategies evolved. Simple hill-climbing algorithms, therefore, only rarely resulted in the evolution of a functional homing behaviour. The inclusion of trail-following greatly increases the frequency of success of evolution of a path integration strategy. Initially an emergent homing behaviour is formed combining path integration with trail-following. This also demonstrates evolution through exaptation, since in the simulation, the original role of trail-following is likely to be unrelated to homing. Analysis of the fitness landscapes of homing in the presence of trail-following behaviour shows a high variability of fitness, which results in the formation of ‘stepping-stones’ of high fitness across fitness valleys. By using these stepping-stones, simple hill-climbing algorithms can reach the global maximum fitness value.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Gould S.J., Lewontin R.C., The spandrels of San Marco and the panglossian paradigm: a critique of the adaptationist programme, Proc. Royal Soc. B, 1979, 205, 581–598

    Article  CAS  Google Scholar 

  2. Holland J.H., Adaptation in natural and artificial systems: an introductory analysis with applications to biology, control, and artificial intelligence, M.I.T. Press, M.A., 1992

    Google Scholar 

  3. Gould S.J., The structure of evolutionary theory, Harvard University Press, Cambridge M.A., 2002

    Google Scholar 

  4. Dawkins R., Climbing Mount Improbable, W.W. Norton and Company Ltd, N.Y., 1996

    Google Scholar 

  5. Wright S., Evolution in Mendelian populations, Genetics, 1931, 16, 97–159

    CAS  PubMed  Google Scholar 

  6. Mitchell M., Forrest S., Genetic algorithms and artificial life, Artif. Life, 1994, 1, 267–289

    Article  Google Scholar 

  7. Wright S., Evolution in populations in approximate equilibrium, J. Genetics, 1935, 30, 257–266

    Article  Google Scholar 

  8. Fear K.K., Price T., The adaptive surface in ecology, Oikos, 1998, 82, 440–448

    Article  Google Scholar 

  9. Brodsky A., The evolution of insect flight, Oxford University Press, Oxford, U.K., 1994

    Google Scholar 

  10. Gould S.J., The meaning of punctuated equilibrium and its role in validating a hierarchical approach to macroevolution, In: Milkman R., (Ed), Perspectives on evolution, Sinauer Associates Inc., M.A., 1982

    Google Scholar 

  11. Watson R.A., Compositional evolution: interdisciplinary investigations in evolvability, modularity, and symbiosis, PhD thesis. Brandeis University, M.A., 2002

    Google Scholar 

  12. Cariani P.A., Extradimensional bypass, BioSystems, 2002, 64, 47–53

    Article  PubMed  Google Scholar 

  13. Mills R., Watson R.A., On crossing fitness valleys with the Baldwin effect, In: Rocha L.M., Yaeger L.S., Bedau M.A., Floreano D., Goldstone R.L., Vespignani A., (Eds), Artificial Life X. Proceedings of the Tenth International Conference on the Simulation and Synthesis of Living Systems, M.I.T. Press, M.A., 2006

    Google Scholar 

  14. Gould S.J., Vrba E., Exaptation-a missing term in the science of form, Paleobiology, 1982, 8, 4–15

    Google Scholar 

  15. Cook A., Bamford O.S., Freeman J.D.B., Teideman D.J., A study of the homing habit of the limpet, Anim. Behav., 1969, 17, 330–339

    Article  Google Scholar 

  16. Cook S.B., Experiments on homing in the limpet Siphonaria normalis, Anim. Behav., 1969, 17, 679–682

    Article  Google Scholar 

  17. Cook S.B., A study of homing behavior in the limpet Siphonaria alternate, Biol. Bull., 1971, 141, 449–457

    Article  Google Scholar 

  18. Chelazzi G., Santini G., Della Santina P., Route selection in the foraging of Patella vulgata (Mollusca: Gastropoda), J. Mar. Biol. Ass. U.K., 1998, 78, 1223–1232

    Article  Google Scholar 

  19. Müller M., Wehner R., Path integration in desert ants, Cataglyphis fortis, Proc. Nat. Acad. Sci. U.S.A., 1998, 85, 5287–5290

    Article  Google Scholar 

  20. Collett M., Collett T.S., Chameron S., Wehner R., Do familiar landmarks reset the global path integration system of desert ants?, J. Exp. Biol., 2003, 206, 877–882

    Article  CAS  PubMed  Google Scholar 

  21. Andel D., Wehner R., Path integration in desert ants, Cataglyphis: how to make a homing ant run away from home, Proc. Royal Soc. B, 2004, 271, 1485–1489

    Article  Google Scholar 

  22. Hölldobler B., Wilson E.O., The ants, Harvard University Press, Cambridge, M.A., 1990

    Google Scholar 

  23. Davies M.S., Hawkins S.J., Mucus from marine molluscs, Adv. Mar. Biol., 1998, 34, 1–71

    Article  Google Scholar 

  24. Stafford R., Davies M.S., Examining refuge location mechanisms in intertidal snails using artificial life simulation techniques, Lecture Notes Artif. Intell., 2005, 3630, 520–529

    Google Scholar 

  25. Davies M.S., Edwards M., Williams G.A., Movement patterns of the limpet Cellana grata (Gould) observed over a continuous period through a changing tidal regime, Mar. Biol., 2006, 149, 775–787

    Article  Google Scholar 

  26. Ng J.S.S., Williams G.A., Intraspecific variation in foraging behaviour: influence of shore height on temporal organisation of activity in the chiton Acanthopleura japonica, Mar. Ecol. Prog. Ser., 2006, 321, 183–192

    Article  Google Scholar 

  27. Edwards M., Davies M.S., Functional and ecological aspects of mucus trails of the intertidal prosobranch gastropod Littorina littorea, Mar. Ecol. Prog. Ser., 2002, 239, 129–137

    Article  Google Scholar 

  28. Stafford R., Davies M.S., Williams G.A., Computer simulations of high shore littorinids predict small-scale spatial and temporal distribution patterns on real rocky shores, Mar. Ecol. Prog. Ser., 2007, 342, 151–161

    Article  Google Scholar 

  29. Parker G.A., Maynard-Smith J., Optimality theory in evolutionary biology, Nature, 1990, 348, 27–33

    Article  Google Scholar 

  30. Hamilton W.D., Extraordinary sex ratios, Science, 1967, 156, 477–488

    Article  CAS  PubMed  Google Scholar 

  31. Herre E.A., Optimality, plasticity and selective regime in fig wasp sex ratios, Nature, 1987, 329, 627–629

    Article  Google Scholar 

  32. West S.A., Sheldon B.C., Constraints in the evolution of sex ratio adjustment, Science, 2002, 295, 1685–1689

    Article  CAS  PubMed  Google Scholar 

  33. Stafford R., Davies M.S., Williams G.A., Parameterization and Prediction of Community Interaction Models Using Stable-State Assumptions and Computational Techniques: an Example From the High Rocky Intertidal, Biol. Bull., 2008, 215, 155–163

    Article  PubMed  Google Scholar 

  34. Holland J.H., Emergence: from chaos to order, Oxford University Press, Oxford U.K., 1998

    Google Scholar 

  35. Tate J.A., Soltis D.E., Soltis P.S., Polyploidy in plants, In: Gregory T.R., (Ed), The evolution of the genome, Elsevier, C.A., 2005

    Google Scholar 

  36. Rieseberg L.H., Hybrid origins of plant species, Ann. Rev. Ecol. Syst., 1997, 28, 359–389

    Article  Google Scholar 

  37. Vrba E.S., Macroevolutionary trends: new perspectives on the roles of adaptation and incidental effect, Science, 1983, 221, 387–389

    Article  PubMed  CAS  Google Scholar 

  38. Camazine S., Deneubourg J.L., Franks N.R., Sneyd J., Theraulaz G., Bonabeau E., Self-organization in biological systems, Princeton University Press, Princeton, N.J., 2001

    Google Scholar 

  39. Resnick M., Turtles, termites, and traffic jams: explorations in massively parallel microworlds, M.I.T Press, M.A., 1997

    Google Scholar 

  40. Collett T.S., Graham P., Durier V., Route learning by insects, Curr. Opin. Neurobiol., 2003, 13, 718–725

    Article  CAS  PubMed  Google Scholar 

  41. Collett T.S., Graham P., Animal navigation: path integration, visual landmarks and cognitive maps, Curr. Biol., 2004, 14, R475–R477

    Article  CAS  PubMed  Google Scholar 

  42. Cannicci S., Fratini S., Vannini M., Short-range homing in fiddler crabs (Ocypodidae, genus Uca): A homing mechanism not based on local visual landmarks, Ethology, 1999, 105, 867–880

    Article  Google Scholar 

  43. Whitlock M.C., Variance-induced peak shifts, Evolution, 1995, 49, 252–259

    Article  Google Scholar 

  44. Price T.D., Qvarnström A., Irwin D.E., The role of phenotypic plasticity in driving genetic evolution, Proc. Royal Soc. B, 2003, 270, 1433–1440

    Article  Google Scholar 

  45. Price T.D., Phenotypic plasticity, sexual selection and the evolution of colour patterns, J. Exp. Biol., 2006, 209, 2368–2376

    Article  CAS  PubMed  Google Scholar 

  46. Behe M., Snoke D.W., Simulating evolution by gene duplication of protein features that require multiple amino acid residues, Protein Sci., 2004, 13, 2651–2664

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Richard Stafford.

About this article

Cite this article

Stafford, R. Crossing fitness valleys during the evolution of limpet homing behaviour. cent.eur.j.biol. 5, 274–282 (2010). https://doi.org/10.2478/s11535-010-0001-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11535-010-0001-9

Keywords

Navigation