Skip to main content
Log in

The role of behavior in evolution: a search for mechanism

  • Review Article
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Behavior has been viewed as a pacemaker of evolutionary change because changes in behavior are thought to expose organisms to novel selection pressures and result in rapid evolution of morphological, life history and physiological traits. However, the idea that behavior primarily drives evolutionary change has been challenged by an alternative view of behavior as an inhibitor of evolution. According to this view, a high level of behavioral plasticity shields organisms from strong directional selection by allowing individuals to exploit new resources or move to a less stressful environment. Here, I suggest that absence of clear mechanisms underlying these hypotheses impedes empirical evaluation of behavior’s role in evolution in two ways. First, both hypotheses focus on behavioral shifts as a key step in the evolutionary process but ignore the developmental mechanisms underlying these shifts and this has fostered unwarranted assumptions about the specific types of behavioral shifts that are important for evolutionary change. Second, neither hypothesis provides a means of connecting within-individual changes in behavior to population-level processes that lead to evolutionary diversification or stasis. To resolve these issues, I incorporate developmental and evolutionary mechanisms into a conceptual framework that generates predictions about the types of behavior and types of behavioral shifts that should affect both micro and macroevolutionary processes.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Arnold SJ (1988) Behavior, energy and fitness. Am Zool 28:815–827

    Google Scholar 

  • Arnold SJ (1994) Multivariate inheritance and evolution: a review of the concepts. In: Boake C (ed) Quantitative genetic studies of behavioral evolution. University of Chicago Press, Chicago, pp 17–48

    Google Scholar 

  • Avital E, Jablonka E (2000) Animal traditions: behavioural inheritance in evolution. Cambridge University Press, Cambridge

    Google Scholar 

  • Badyaev AV (2004) Developmental perspective on the evolution of sexual ornaments. Evol Ecol Res 6:975–991

    Google Scholar 

  • Badyaev AV (2005) Stress-induced variation in evolution: from behavioral plasticity to genetic assimilation. Proc R Soc Lond B 272:877–886

    Article  Google Scholar 

  • Badyaev AV (2007) Evolvability and robustness in color displays: bridging the gap between theory and data. Evol Biol 34:61–71

    Article  Google Scholar 

  • Baldwin JM (1896) A new factor in evolution. Am Nat 15:441–451

    Article  Google Scholar 

  • Barton N, Partridge L (2000) Limits to natural selection. BioEssays 22:1075–1084

    Article  PubMed  CAS  Google Scholar 

  • Bateson P (1988) The active role of behaviour in evolution. In: Ho M-W, Fox SW (eds) Evolutionary processes and metaphors. John Wiley and Sons, Ltd., New York

    Google Scholar 

  • Bearhop S, Fiedler W, Furness RW, Votier SC, Waldron S, Newton J, Bowen GJ, Berthold P, Farnsworth K (2005) Assortative mating as a mechanism for rapid evolution of a migratory divide. Science 310:502–504

    Article  PubMed  CAS  Google Scholar 

  • Behera N, Nanjundiah V (1995) An investigation into the role of phenotypic plasticity in evolution. J Theor Biol 172:225–234

    Article  PubMed  CAS  Google Scholar 

  • Bell AM (2005) Behavioural differences between individuals and two population of stickleback (Gasterosteus aculeatus). J Evol Biol 18:464–473

    Article  PubMed  CAS  Google Scholar 

  • Belliure J, Sorci G, Møller AP, Clober J (2000) Dispersal distances predict subspecies richness in birds. J Evol Biol 13:480–487

    Article  Google Scholar 

  • Berthold P, Helbig AJ, Mohr G, Querner U (1992) Rapid microevolution of migratory behaviour in a wild bird species. Nature 360:668–670

    Article  Google Scholar 

  • Boake CRB (1989) Repeatability: its role in evolutionary studies of mating behavior. Evol Ecol 3:173–182

    Article  Google Scholar 

  • Bogert CM (1949) Thermoregulation in reptiles, a factor in evolution. Evolution 3:195–211

    Article  PubMed  CAS  Google Scholar 

  • Cheverud JM (1982) Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution 36:499–516

    Article  Google Scholar 

  • Clobert J, Danchin E, Dhondt AA, Nichols JD (2001) Dispersal. Oxford University Press, New York

    Google Scholar 

  • Dall SRX, Houston AI, McNamara JM (2004) The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett 7:734–739

    Article  Google Scholar 

  • Dieckmann U, Doebeli M (1999) On the origin of species by sympatric speciation. Nature 400:354–357

    Article  PubMed  CAS  Google Scholar 

  • Dingemanse NJ, Both C, Drent PJ, van Oers K, Van Noordwijk AJ (2002) Repeatability and heritability of exploratory behaviour in great tits from the wild. Anim Behav 64:929–938

    Article  Google Scholar 

  • Dingemanse NJ, Both C, van Noordwijk AJ, Rutten AL, Drent PJ (2003) Natal dispersal and personalities in great tits (Parus major). Proc R Soc Lond B 270:741–747

    Article  Google Scholar 

  • Drent PJ, van Oers K, van Noordwijk AJ (2003) Realized heritability of personalities in the great tit (Parus major). Proc R Soc Lond B 270:45–51

    Article  Google Scholar 

  • Duckworth RA (2006a) Behavioral correlations across reproductive contexts provide a mechanism for a cost of aggression. Behav Ecol 17:1011–1019

    Article  Google Scholar 

  • Duckworth RA (2006b) Aggressive behavior affects selection on morphology by determining the environment of breeding in a passerine bird. Proc R Soc Lond B 273:1789–1795

    Article  Google Scholar 

  • Duckworth RA, Badyaev AV (2007) Coupling of aggression and dispersal facilitates the rapid range expansion of a passerine bird. Proc Natl Acad Sci USA 104:15017–15022

    Article  PubMed  CAS  Google Scholar 

  • Duckworth RA (2008) Adaptive dispersal strategies and the dynamics of a range expansion. American Naturalist 172 (In press)

  • Endler JA (1973) Gene flow and population differentiation. Science 179:243–250

    Article  PubMed  CAS  Google Scholar 

  • Forstmeier W, Birkhead TR (2004) Repeatability of mate choice in the zebra finch: consistency within and between females. Anim Behav 68:1017–1028

    Article  Google Scholar 

  • Forstmeier W, Coltman DW, Birkhead TR (2004) Maternal effects influence the sexual behavior of sons and daughters in the zebra finch. Evolution 58:2574–2583

    PubMed  Google Scholar 

  • Gabriel W, Luttbeg B, Sih A, Tollrian R (2005) Environmental tolerance, heterogeneity, and the evolution of reversible plastic responses. Am Nat 166:339–353

    Article  PubMed  Google Scholar 

  • Ghalambor CK, Martin TE (2002) Comparative manipulation of predation risk in incubating birds reveals variability in the plasticity of responses. Behav Ecol 13:101–108

    Article  Google Scholar 

  • Gordon DM (1986) The dynamics of the daily round of the harvester ant colony. Anim Behav 34:1402–1419

    Article  Google Scholar 

  • Gordon DM (1991) Variation and change in behavioral ecology. Ecology 72:1196–1203

    Article  Google Scholar 

  • Gottlieb G (2002) Developmental—behavioral initiation of evolutionary change. Psychol Rev 109:211–218

    Article  PubMed  Google Scholar 

  • Grant BR, Grant PR (1996) Cultural inheritance of song and its role in the evolution of Darwin’s finches. Evolution 50:2471–2487

    Article  Google Scholar 

  • Grant BR, Grant PR, Petran K (2001) A population founded by a single pair of individuals: establishment, expansion, and evolution. Genetica 112–113:359–382

    Article  PubMed  Google Scholar 

  • Hammer M, Menzel R (1995) Learning and memory in the honeybee. J Neurosci 15:1617–1630

    PubMed  CAS  Google Scholar 

  • Hedrick A (1994) The heritability of mate-attractive traits: a case study on field crickets. In: Boake C (ed) Quantitative genetic studies of behavioral evolution. University of Chicago Press, Chicago, pp 228–250

    Google Scholar 

  • Ho M-W (1988) On not holding nature still: evolution by process, not by consequence In: Ho M-W, Fox SW (eds) Evolutionary processes and metaphors. John Wiley and Sons, Ltd., New York

    Google Scholar 

  • Holt RD (1987) Population dynamics and evolutionary processes: the manifold roles of habitat selection. Evol Ecol 1:331–347

    Article  Google Scholar 

  • Huey RB, Hertz PE, Sinervo B (2003) Behavioral drive versus behavioral inertia in evolution: a null model approach. Am Nat 161:357–366

    Article  PubMed  Google Scholar 

  • Irwin DE, Price TD (1999) Sexual imprinting, learning and speciation. Heredity 82:347–354

    Article  PubMed  Google Scholar 

  • Jablonka E, Lamb M (1995) Epigenetic inheritance and evolution: the lamarckian dimension. Oxford University Press, Oxford

    Google Scholar 

  • Johnson JC, Sih A (2005) Precopulatory sexual cannibalism in fishing spiders (Dolomedes triton): a role for behavioral syndromes. Behav Ecol Sociobiol 58:390–396

    Article  Google Scholar 

  • Kimura M (1968) Evolutionary rate at the molecular level. Nature 217:624–626

    Article  PubMed  CAS  Google Scholar 

  • Laland KN, Odling-Smee FJ, Feldman MW (1996) The evolutionary consequences of niche construction: a theoretical investigation using two-locus theory. J Evol Biol 9:293–316

    Article  Google Scholar 

  • Laland KN, Odling-Smee FJ, Feldman MW (1999) Evolutionary consequences of niche construction and their implications for ecology. Proc Natl Acad Sci USA 96:10242–10247

    Article  PubMed  CAS  Google Scholar 

  • Laland KN, Odling-Smee FJ, Feldman MW (2000) Niche construction, biological evolution, and cultural change. Behav Brain Sci 23:131–175

    Article  PubMed  CAS  Google Scholar 

  • Lefebvre L, Whittle P, Lascaris E, Finkelstein A (1997) Feeding innovations and forebrain size in birds. Anim Behav 53:549–560

    Article  Google Scholar 

  • Lester SE, Ruttenberg BI, Gaines SD, Kinlan BP (2007) The relationship between dispersal ability and geographic range size. Ecol Lett 10:745–758

    Article  PubMed  Google Scholar 

  • Lewontin RC (1982) Organism and environment. In: Plotkin HC (ed) Learning, development, and culture. John Wiley and Sons, Ltd., New York

    Google Scholar 

  • Lewontin RC (1983) Gene, organism and environment. In: Bendall DS (ed) Evolution from molecules to men. Cambridge University Press, Cambridge

    Google Scholar 

  • Losos JB, Schoener TW, Spiller DA (2004) Predator-induced behaviour shifts and natural selection in field-experimental lizard populations. Nature 432:505–508

    Article  PubMed  CAS  Google Scholar 

  • Losos JB, Schoener TW, Langerhans RB, Spiller DA (2006) Rapid temporal reversal in predator-driven natural selection. Science 314:1111

    Article  PubMed  CAS  Google Scholar 

  • Lynch M (1990) The rate of morphological evolution in mammals from the standpoint of the neutral expectation. Am Nat 136:727–741

    Article  Google Scholar 

  • MacColl ADC, Hatchwell BJ (2003) Heritability of parental effort in a passerine bird. Evolution 57:2191–2195

    PubMed  Google Scholar 

  • Maddison WP, Midford PE, Otto SP (2007) Estimating a binary character’s effect on speciation and extinction. Syst Biol 56:701–710

    Article  PubMed  Google Scholar 

  • Mahler B, Tubaro PL (2001) Relationship between song characters and morphology in new world pigeons. Biol J Linn Soc 74:533–539

    Article  Google Scholar 

  • Maynard Smith J (1976) What determines the rate of evolution? Am Nat 110:331–338

    Article  Google Scholar 

  • Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge

    Google Scholar 

  • Merilä J, Björklund M (2004) Phenotypic integration as a constraint and adaptation. In: Pigliucci M, Preston K (eds) Phenotypic integration: studying the ecology and evolution of complex phenotypes. Oxford University Press, New York, pp 107–129

    Google Scholar 

  • Nicolakakis ND, Sol D, Lefebvre L (2003) Behavioral flexibility predicts species richness in birds, but not extinction risk. Anim Behav 65:445–452

    Article  Google Scholar 

  • Nijhout HF (1994) Developmental perspectives on evolution of butterfly mimicry. Bioscience 44:148–157

    Article  Google Scholar 

  • Odling-Smee FJ, Laland KN, Feldman MW (2003) Niche construction: the neglected process in evolution. Princeton University Press, Princeton

    Google Scholar 

  • Payne RB (1996) Song traditions in indigo buntings: origin, improvisation, dispersal, and extinction in cultural evolution. In: Kroodsma DE, Miller EH (eds) Ecology and evolution of acoustic communication in birds. Cornell University Press, London, pp 198–220

    Google Scholar 

  • Pereira HS, Sokolowski MB (1993) Mutations in the larval foraging gene affect adult locomotory behavior after feeding in Drosophila melanogaster. Proc Natl Acad Sci USA 90:5044–5046

    Article  PubMed  CAS  Google Scholar 

  • Pfennig DW, Rice AM, Martin RA (2006) Ecological opportunity and phenotypic plasticity interact to promote character displacement and species coexistence. Ecology 87:769–779

    Article  PubMed  Google Scholar 

  • Phillimore AB, Freckleton RP, Orme CDL, Owens IPF (2006) Ecology predicts large-scale patterns of phylogenetic diversification in birds. Am Nat 168:220–229

    Article  PubMed  Google Scholar 

  • Piaget J (1978) Behavior and evolution. Pantheon Books, New York

    Google Scholar 

  • Piersma T, Drent J (2003) Phenotypic flexibility and the evolution of organismal design. Trends Ecol Evol 18:228–233

    Article  Google Scholar 

  • Piersma T, Lindström Å (1997) Rapid reversible changes in organ size as a component of adaptive behavior. Trends Ecol Evol 12:134–138

    Article  Google Scholar 

  • Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Experimental Biol 209:2362–2367

    Article  Google Scholar 

  • Plotkin HC (1988a) Behavior and evolution. In: Plotkin HC (ed) The role of behavior in evolution. The MIT Press, Cambridge

    Google Scholar 

  • Plotkin HC (1988b) Learning and evolution. In: Plotkin HC (ed) The role of behavior in evolution. MIT Press, Cambridge

    Google Scholar 

  • Price TD (2007) Speciation in birds. Roberts and Company Publishers, Boulder

    Google Scholar 

  • Price TD, Qvarnström A, Irwin D (2003) The role of phenotypic plasticity in driving genetic evolution. Proc R Soc Lond B 270:1433–1440

    Article  Google Scholar 

  • Reader S, Laland K (2002) Social intelligence, innovation and enhanced brain size in primates. Proc Natl Acad Sci USA 99:4436–4441

    Article  PubMed  CAS  Google Scholar 

  • Roff DA (1994) Optimality modeling and quantitative genetics: a comparison of the two approaches. In: Boake C (ed) Quantitative genetic studies of behavioral evolution. University of Chicago Press, Chicago, pp 49–66

    Google Scholar 

  • Rosenzweig ML (1995) Species diversity in space and time. Cambridge University Press, Cambridge

    Google Scholar 

  • Sanderson MJ, Donoghue MJ (1996) Reconstructing shifts in diversification rates on phylogenetic trees. Trends Ecol Evol 11:15–20

    Article  Google Scholar 

  • Schluter D (1996) Ecological causes of adaptive radiation. Am Nat 148:S40–S64

    Article  Google Scholar 

  • Schluter D (2000) The ecology of adaptive radiation. Oxford University Press

  • Schwagmeyer PL, Mock DW (2003) How consistently are good parents good parents? Repeatability of parental care in the house sparrow, Passer domesticus. Ethology 109:303–313

    Article  Google Scholar 

  • Sih A, Kats LB, Maurer EF (2003) Behavioural correlations across situations and the evolution of antipredator behaviour in a sunfish-salamander system. Anim Behav 65:29–44

    Article  Google Scholar 

  • Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378

    Article  PubMed  Google Scholar 

  • Slagsvold T, Hansen BT, Johannessen LE, Lifjeld JT (2002) Mate choice and imprinting in birds studied by cross-fostering in the wild. Proc R Soc Lond B 269:1449–1455

    Article  Google Scholar 

  • Slatkin M (1985) Gene flow in natural populations. Annu Rev Ecol Syst 16:393–430

    Article  Google Scholar 

  • Slikas B (1998) Recognizing and testing homology of courtship displays in storks (aves: ciconiiformes: ciconiidae). Evolution 52:884–893

    Article  Google Scholar 

  • Sol D, Lefebvre L (2000) Behavioural flexibility predicts invasion success in birds introduced to New Zealand. Oikos 90:599–605

    Article  Google Scholar 

  • Sol D, Timmermans S, LeFebvre L (2002) Behavioural flexibility and invasion success in birds. Anim Behav 63:495–502

    Article  Google Scholar 

  • Sol D, Duncan RP, Blackburn TM, Cassey P, Lefebvre L (2005a) Big brains, enhanced cognition, and response of birds to novel environments. Proc Natl Acad Sci USA 102:5460–5465

    Article  PubMed  CAS  Google Scholar 

  • Sol D, Stirling DG, Lefebvre L (2005b) Behavioral drive or behavioral inhibition in evolution: subspecific diversification in holarctic passerines. Evolution 59:2669–2677

    PubMed  Google Scholar 

  • Suhling F, Göran S, Kasperski J, Gaedecke D (2005) Behavioural and life history traits in temporary and perennial waters: comparisons among three pairs of sibling dragonfly species. Oikos 108:609–617

    Article  Google Scholar 

  • ten Cate C (2000) How learning mechanisms might affect evolutionary processes. Trends Ecol Evol 15:179–181

    Article  PubMed  Google Scholar 

  • Thompson D (1999) Different spatial scales of natural selection and gene flow: the evolution of behavioral geographic variation and phenotypic plasticity. In: Foster S, Endler J (eds) Geographic variation in behavior. Oxford Univ. Press, New York, pp 33–51

    Google Scholar 

  • Tinbergen N (2005) On aims and methods of ethology. Anim Biol 55:297–321 (Reprinted from original)

    Article  Google Scholar 

  • Via S (2001) Sympatric speciation in animals: the ugly duckling grows up. Trends Ecol Evol 16:381–390

    Article  PubMed  Google Scholar 

  • Waddington CH (1960) Evolutionary adaptation. In: Sax S (ed) The evolution of life. University of Chicago Press

  • Wagner GP (2001) The character concept in evolutionary biology. Academic Press, San Diego

    Google Scholar 

  • Wares JP, Hughes AR, Grosberg RK (2005) Mechanisms that drive evolutionary change: insights from species introductions and invasions. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer Associates, Inc., Sunderland, pp 229–257

    Google Scholar 

  • Wcislo WT (1989) Behavioral environments and evolutionary change. Annu Rev Ecol Syst 20:137–169

    Article  Google Scholar 

  • West-Eberhard M (1983) Sexual selection, social competition, and speciation. Q Rev Biol 58:155–183

    Article  Google Scholar 

  • West-Eberhard M (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 20:249–278

    Article  Google Scholar 

  • West-Eberhard M (2003) Developmental plasticity and evolution. Oxford University Press, New York

    Google Scholar 

  • Wiens JJ (2004) Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species. Evolution 58:193–197

    PubMed  Google Scholar 

  • Wingfield JC (1987) Changes in reproductive function of free-living birds in direct response to environmental perturbations. In: Stetson MH (ed) Processing of environmental information in vertebrates. Springer-Verlag, New York, pp 121–148

    Google Scholar 

  • Wolf JB, Brodie ED, Cheverud JM, Moore AJ, Wade MJ (1998) Evolutionary consequences of indirect genetic effects. Trends Ecol Evol 13:64–69

    Article  Google Scholar 

  • Wolf JB, Brodie ED, Moore A (1999) Interacting phenotypes and the evolutionary process. II. Selection resulting from social interactions. Am Nat 153:254–266

    Article  Google Scholar 

  • Wyles JS, Kunkel JG, Wilson AC (1983) Birds, behavior, and anatomical evolution. Proc Natl Acad Sci USA 80:4394–4397

    Article  PubMed  CAS  Google Scholar 

  • Zuk M, Rotenberry JT, Tinghitella RM (2006) Silent night: adaptive disappearance of a sexual signal in a parasitized population of field crickets. Biol Lett 2:521–524

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

I thank Drs. Jonathan Losos, Fred Nijhout, Alex Badyaev, David Pfennig, Trevor Price, Steve Nowicki and two anonymous reviewers for discussions and comments on previous versions of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Renée A. Duckworth.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Duckworth, R.A. The role of behavior in evolution: a search for mechanism. Evol Ecol 23, 513–531 (2009). https://doi.org/10.1007/s10682-008-9252-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-008-9252-6

Keywords

Navigation