Skip to main content

More on how and why: cause and effect in biology revisited

Abstract

In 1961, Ernst Mayr published a highly influential article on the nature of causation in biology, in which he distinguished between proximate and ultimate causes. Mayr argued that proximate causes (e.g. physiological factors) and ultimate causes (e.g. natural selection) addressed distinct ‘how’ and ‘why’ questions and were not competing alternatives. That distinction retains explanatory value today. However, the adoption of Mayr’s heuristic led to the widespread belief that ontogenetic processes are irrelevant to evolutionary questions, a belief that has (1) hindered progress within evolutionary biology, (2) forged divisions between evolutionary biology and adjacent disciplines and (3) obstructed several contemporary debates in biology. Here we expand on our earlier (Laland et al. in Science 334:1512–1516, 2011) argument that Mayr’s dichotomous formulation has now run its useful course, and that evolutionary biology would be better served by a concept of reciprocal causation, in which causation is perceived to cycle through biological systems recursively. We further suggest that a newer evolutionary synthesis is unlikely to emerge without this change in thinking about causation.

This is a preview of subscription content, access via your institution.

References

  • Alcock J (1975) Animal behavior: an evolutionary approach, 1st edn. Sinauer, Sunderland

    Google Scholar 

  • Amundson R (2005) The changing role of the embryo in evolutionary thought. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Antonovics J (1987) The evolutionary dys-synthesis: which bottles for which wine? Am Nat 129:321–331

    Article  Google Scholar 

  • Ariew A (2003) Ernst Mayr’s ‘ultimate/proximate’ distinction reconsidered and reconstructed. Biol Philos 18:553–565

    Article  Google Scholar 

  • Arthur W (2004) Biased embryo and evolution. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Badyaev AV (2009) Evolutionary significance of phenotypic accommodation in novel environments: an empirical test of the Baldwin effect. Philos Trans R Soc B 364:1125–1141

    Article  Google Scholar 

  • Badyaev AV (2011) Origin of the fittest: link between emergent variation and evolutionary change as a critical question in evolutionary biology. Proc R Soc B 278:1921–1929

    Article  Google Scholar 

  • Badyaev AV, Uller T (2009) Parental effects in ecology and evolution: mechanisms, processes and implications. Philos Trans R Soc B 364:1169–1177

    Article  Google Scholar 

  • Baker J (1938) The evolution of breeding systems. In: de Beer (ed) Evolution: essays on aspects of evolutionary biology. Oxford University Press, Oxford

  • Baldwin JM (1896) A new factor in evolution. Am Nat 30(441–451):536–553

    Article  Google Scholar 

  • Bateson P (1988) The active role of behaviour in evolution. In: Ho, Fox (eds) Evolutionary processes and metaphors. Wiley, New York

  • Bateson P, Gluckman P (2011) Plasticity, robustness, development and evolution. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Berna F, Goldberg P, Kolska-Horwitz L, Brink J, Holt S, Bamford M, Chazan M (2012) Microstratigraphic evidence of in situ fire in the Acheulean strata of Wonderwerk Cave, Northern Cape province, South Africa. Proc Natl Acad Sci. doi:10.1073/pnas.1117620109

    Google Scholar 

  • Bickerton D (2009) Adam’s tongue: how humans made language, how language made humans. Hill and Wang, New York

    Google Scholar 

  • Bloch M (2000) A well-disposed social anthropologist’s problems with memes. In: Aunger (ed) Darwinizing culture: the status of memetics as a science. Oxford University Press, Oxford

  • Blute M (2010) Darwinian socioculture evolution: solutions to dilemmas in cultural and social theory. Cambridge University Press, Cambridge

  • Bolhuis JJ, Verhulst S (2009) (eds) Tinbergen’s legacy. Cambridge University Press, Cambridge

  • Bolhuis JJ, Brown GR, Richardson RC, Laland KN (2011) Darwin in mind: new opportunities for evolutionary psychology. PLoS Biol 9:e1001109

    Article  Google Scholar 

  • Boyd R, Richerson PJ (1985) Culture and the evolutionary process. Chicago University Press, Chicago

    Google Scholar 

  • Boyd R, Gintis H, Bowles S, Richerson PJ (2003) The evolution of altruistic punishment. PNAS 100:3531–3535

    Article  Google Scholar 

  • Brakefield P (2006) Evo-devo and constraints on selection. Trends Ecol Evol 21:362–368

    Article  Google Scholar 

  • Brown GR, Laland KN, Borgerhoff-Mulder M (2009) Bateman’s principles and human sex roles. Trends Ecol Evol 24:297–304

    Article  Google Scholar 

  • Brown GR, Dickins TE, Sear R, Laland KN (2011) Evolutionary accounts of human behavioural diversity. Philos Trans R Soc B 366:313–324

    Article  Google Scholar 

  • Campbell DT (1974) Evolutionary epistemology. In: Schilpp (ed) The philosophy of Karl R. Popper. Chicago, Open Court, pp 413–463

  • Cavalli-Sforza LL, Feldman MW (1981) Cultural transmission and evolution. University of Princeton Press, Princeton

    Google Scholar 

  • Chudek M, Henrich J (2011) Culture-gene coevolution, norm-psychology and the emergence of human prosociality. Trends Cogn Sci 15:218–226

    Article  Google Scholar 

  • Cornwallis CK, Uller T (2010) Towards an evolutionary ecology of sexual traits. Trends Ecol Evol 25:145–152

    Article  Google Scholar 

  • Davies NB, Krebs JR, West SA (2012) An introduction to behavioural ecology, 4th edn. Wiley-Blackwell, New York

  • Dawkins R (2004) Extended phenotype—but not too extended. A reply to Laland, Turner and Jablonka. Biol Physiol 19:377–396

    Article  Google Scholar 

  • Day T, Bonduriansky R (2011) A unified approach to the evolutionary consequences of genetic and nongenetic inheritance. Am Nat 178:E18–E36

    Article  Google Scholar 

  • De Jong G (2005) Evolution of phenotypic plasticity: patterns of plasticity and the emergence of ecotypes. New Phytol 166:101–117

    Article  Google Scholar 

  • De Jong G, Crozier RH (2003) Developmental plasticity and evolution. Nature 424:16–17

    Article  Google Scholar 

  • Dennett D (1995) Darwin’s dangerous idea: evolution and the meanings of life. Penguin, London

    Google Scholar 

  • Dewsbury D (1999) The proximate and the ultimate: past, present, and future. Behav Process 46:189–199

    Article  Google Scholar 

  • Dickins TE, Rahman Q (2012) The extended evolutionary synthesis and the role of soft inheritance in evolution. Proc R Soc B, doi:10.1098/rspb.2012.0273

  • Dingermanse NJ, Karem AJN, Reale D, Wright J (2009) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25:81–89

    Article  Google Scholar 

  • Duckworth RA (2009) The role of behavior in evolution: a search for mechanism. Evol Ecol 23:513–531

    Article  Google Scholar 

  • Durham WH (1991) Coevolution: genes, culture and human diversity. Stanford University Press, Palo Alto

    Google Scholar 

  • Efferson C, Lalive R, Fehr E (2008) The coevolution of cultural groups and in group favoritism. Science 321:1844–1849

    Article  Google Scholar 

  • Ehrlich PR (1986) The machinery of nature. Simon and Schuster, New York

    Google Scholar 

  • Ehrlich P, Feldman M (2003) Genes and culture. What creates our behavioral phenome? Curr Anthro 44:87–107

    Article  Google Scholar 

  • Endler JA (1986) Natural selection in the wild. Princeton University Press, Princeton

    Google Scholar 

  • Erwin DH (2008) Macroevolution of ecosystem engineering, niche construction and diversity. Trends Ecol Evol 23:304–310

    Article  Google Scholar 

  • Erwin DH, Tweedt S (2012) Ecological drivers of the Ediacaran diversification of metazoa. Evol Ecol 26:417–433

    Article  Google Scholar 

  • Ewald PW (1994) Evolution of infectious disease. Oxford University Press, New York

    Google Scholar 

  • Fawcett T, Hamblin S, Giraldeau LA (2012) Exposing the behavioral gambit: the evolution of learning and decision rules. Behav Ecol. doi:10.1093/beheco/ars085

  • Fehr E, Fischbacher U (2003) The nature of human altruism. Nature 425:785–791

    Article  Google Scholar 

  • Fisher RA (1958) The genetical theory of natural selection, 2nd edn. Dover, New York

    Google Scholar 

  • Ford EB (1964) Ecological genetics. Chapman and Hall, London

  • Francis RC (1990) Causes, proximate and ultimate. Biol Philos 5:401–415

    Article  Google Scholar 

  • Frank SA (2009) Natural selection maximizes fisher information. J Evol Biol 22:231–244

    Article  Google Scholar 

  • Fuentes A (2009) Evolution of human behavior. Oxford University Press, Oxford

  • Gilbert SF (2003) Developmental biology, 7th edn. Sinauer, Sunderland

    Google Scholar 

  • Gintis H (2003) The hitchhiker’s guide to altruism: gene-culture coevolution, and the internalization of norms. J Theor Biol 220:407–418

    Article  Google Scholar 

  • Godfrey-Smith P (1996) Complexity and the function of mind in nature. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Gordon DM (2011a) The fusion of behavioural ecology and ecology. Behav Ecol 22:225–230

    Article  Google Scholar 

  • Gordon DM (2011b) The fusion of behavioural ecology and ecology, response after commentary. Behav Ecol 22:225–230

    Article  Google Scholar 

  • Gottlieb G (1992) Individual development and evolution. The genesis of novel behavior. Oxford University Press, New York

    Google Scholar 

  • Griffiths PE, Gray RD (1994) Developmental systems and evolutionary explanation. J Philos 91:277–304

    Article  Google Scholar 

  • Hagen JB (1992) An entangled bank: the origins of ecosystem ecology. Rutgers University Press, New Brunswick

    Google Scholar 

  • Haig D (2007) Weismann rules! OK? Epigenetics and the Lamarckian temptation. Biol Philos 22:415–428

    Article  Google Scholar 

  • Hansen TF (2011) Epigenetics: adaptation or contingency? In: Hallgrímsson B, Hall BK (eds) Epigenetics: linking genotype and phenotype in development and evolution. University of California Press, Los Angeles

    Google Scholar 

  • Harjunmaa E, Kallonen A, Voutilainen M, Hamalainen K, Mikkola ML, Jernvall J (2012) On the difficulty of increasing dental complexity. Nature 483:324

    Google Scholar 

  • Henrich J (2004) Cultural group selection, coevolutionary processes and large-scale cooperation. J Econ Behav Org 53:3–35

    Article  Google Scholar 

  • Henrich J, Heine SJ, Norenzayan A (2010) The weirdest people in the world. Behav Brain Sci 33:61–135

    Article  Google Scholar 

  • Hogan JA (1994) The concept of cause in the study of behavior. In: Hogan, Bolhuis (eds) Causal mechanisms of behavioural development. Cambridge University Press, Cambridge, pp 3–15

    Chapter  Google Scholar 

  • Hogan JA, Bolhuis JJ (2009) Tinbergen’s four questions and contemporary behavioural biology. In: Bolhuis, Verhulst (eds) Tinbergen’s legacy. Cambridge University Press, Cambridge, pp 25–34

  • Hood KE, Halpern CT, Greenberg G, Lerner RM (2010) Developmental science, behaviour, and genetics. Wiley-Blackwell, Massachusetts

    Book  Google Scholar 

  • Howson C (2000) Hume’s problem: induction and the justification of belief. Oxford University Press, Oxford

  • Hull DL, Langman RE, Glenn SS (2001) A general account of selection: biology, immunology and behavior. Behav Brain Sci 24:511–573

    Article  Google Scholar 

  • Hume D (1910) [1748] An enquiry concerning human understanding. PF Collier & Son, New York

  • Ingold T (2007) The trouble with ‘evolutionary biology’. Anthropol Today 23:13–17

    Article  Google Scholar 

  • Jablonka E, Lamb MJ (2005) Evolution in four dimensions. MIT Press, Cambridge

    Google Scholar 

  • Jones CG, Lawton JH (eds) (1995) Linking species and ecosystems. Chapman and Hall, New York

    Google Scholar 

  • Kavanagh KD, Evans AR, Jernvall J (2007) Predicting evolutionary patterns of mammalian teeth from development. Nature 449:427-U1

    Article  Google Scholar 

  • Kendal J, Tehrani JJ, Odling-Smee FJ (eds) (2011) Human niche construction in interdisciplinary focus. Philos Trans R Soc B 366, special edition

  • Klopfer PH, Hailman JP (eds) (1972a) Function and evolution of behavior. Addison-Wesley, Reading

    Google Scholar 

  • Klopfer PH, Hailman JP (eds) (1972b) Control and development of behavior. Addison-Wesley, Reading

    Google Scholar 

  • Kuper A (2000) If memes are the answer, what is the question? In: Aunger (ed) Darwinizing culture: the status of memetics as a science. Oxford University Press, Oxford, pp 175–188

  • Lack D (1954) The natural regulation of animal numbers. Oxford University Press, Oxford

    Google Scholar 

  • Laland KN, Brown GR (2006) Niche construction, human behavior, and the adaptive-lag hypothesis. Evol Anthro 15:95–104

    Article  Google Scholar 

  • Laland KN, Brown GR (2011) Sense and nonsense, 2nd edn. Oxford University Press, Oxford

  • Laland KN, Sterelny K (2006) Seven reasons (not) to neglect niche construction. Evolution 60:1751–1762

    Google Scholar 

  • Laland KN, Odling-Smee FJ, Feldman MW (1996) On the evolutionary consequences of niche construction. 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. PNAS 96:10242–10247

    Article  Google Scholar 

  • Laland KN, Odling-Smee FJ, Gilbert SF (2008) EvoDevo and niche construction: building bridges. J Exp Zool B 310:549–566

    Article  Google Scholar 

  • Laland KN, Odling-Smee FJ, Myles S (2010) How culture has shaped the human genome: bringing genetics and the human sciences together. Nat Rev Gen 11:137–148

    Article  Google Scholar 

  • Laland KN, Sterelny K, Odling-Smee FJ, Hoppitt W, Uller T (2011) Cause and effect in biology revisited: is Mayr’s proximate–ultimate dichotomy still useful? Science 334:1512–1516

    Article  Google Scholar 

  • Layton R (2010.)Why social scientists don’t like Darwin and what can be done about it. J Evol Psychol 8:139–152

    Google Scholar 

  • Lehmann L (2007) The evolution of trans-generational altruism: Kin selection meets niche construction. J Evol Biol 20:181–189

    Article  Google Scholar 

  • Lehmann L (2008) The adaptive dynamics of niche constructing traits in spatially subdivided populations: evolving posthumous extended phenotypes. Evolution 62:549–566

    Article  Google Scholar 

  • Leimar O, Hammerstein P, Van Dooren TJM (2006) A new perspective on developmental plasticity and the principles of adaptive morph determination. Am Nat 167:367–376

    Article  Google Scholar 

  • Levins R (1966) The strategy of model building in population biology. Am Scientist 54:421–431

    Google Scholar 

  • Lewontin RC (1982) Organism and environment. In: Plotkin (ed) Learning, development and culture. Wiley, New York, pp 151–170

  • Lewontin RC (1983) Gene, organism and environment. In: Bendall (ed) Evolution from molecules to men. Cambridge University Press, Cambridge, pp 273–285

  • Lickliter R, Harshaw C (2010) Canalization and malleability revisited: the developmental basis of phenotypic stability and variability. In: Hood KE, Halpern CT, Greenberg G, Lerner RM (eds) Developmental science, behaviour, and genetics. Wiley-Blackwell, Massachusetts

    Google Scholar 

  • Likens GE (1995) Forward. In: Jones, Lawton (eds) Linking species and ecosystems. Chapman and Hall, New York

  • Loreau M (2010) From populations to ecosystems: theoretical foundations for a new ecological synthesis. Monographs in Population Biology. Princeton University Press, Princeton, vol 46

  • MacDougall-Shackleton (2011) The levels of analysis revisited. Philos Trans R Soc B 366:2076–2085

    Article  Google Scholar 

  • Maynard-Smith J (1982) Evolution and the theory of games. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Maynard-Smith J, Burian R, Kaufman S, Alberch P, Campbell J et al (1985) Developmental constraints and evolution. Q Rev Biol 60:265–287

    Article  Google Scholar 

  • Mayr E (1958) Change of genetic environment and evolution. In: Huxley, Hardy Ford (eds) Evolution as a Process. Allen and Unwin, London, pp 188–213

    Google Scholar 

  • Mayr E (1961) Cause and effect in biology. Science 134:1501–1506

    Article  Google Scholar 

  • Mayr E (1974) Teleological and teleonomic, a new analysis. Boston Stud Philos Sci 14:91–117

    Article  Google Scholar 

  • Mayr E (1980) Some thoughts on the history of the evolutionary synthesis. In: Mayr, Provine (eds) The evolutionary synthesis. Harvard University Press, Cambridge, pp 1–48

  • Mayr E (1984) The triumph of the evolutionary synthesis. Times Literary Suppl 2 November, pp 1261–1262

  • Mayr E (1992) Controversies in retrospect. Evol Biol 8:1–34

    Google Scholar 

  • Mayr E (1993) Proximate and ultimate causations. Biol Philos 8:93–94

    Article  Google Scholar 

  • McNamara JM, Dall SRX (2010) Information is a fitness enhancing resource. Oikos 119:231–236

    Article  Google Scholar 

  • McNamara JM, Houston AI (1980) The application of statistical decision theory to animal behaviour. J Theor Biol 85:673–690

    Article  Google Scholar 

  • McNamara JM, Houston AI (2009) Integrating function and mechanism. Trend Ecol Evol 24:670–675

    Article  Google Scholar 

  • McNamara JM, Stephens PA, Dall SRX, Houston AI (2009) Evolution of trust and trustworthiness: social awareness favours personality differences. Proc R Soc B 276:605–613

    Google Scholar 

  • Mesoudi A (2011) Cultural evolution: how Darwinian theory can explain human culture and synthesize the social sciences. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Mivart SG (1871) On the genesis of species. D Appleton and Co., New York

    Book  Google Scholar 

  • Moczek AP, Sultan S, Foster S, Ledon-Rettig C, Dworkin I, Nijhout HF, Abouheif E, Pfennig DW (2011) The role of developmental plasticity in evolutionary innovation. Proc R Soc B 278:2705–2713

    Article  Google Scholar 

  • Muller GB (2007) Evo-devo: extending the evolutionary synthesis. Nat Rev Genet 8:n953-946

    Article  Google Scholar 

  • Nowak M, Highfield R (2011) Super-cooperators: the mathematics of evolution, altruism and human behaviour (or why we need each other to succeed). Canongate, London

    Google Scholar 

  • Nowak MA, Tarnita CE, Wilson EO (2010) The evolution of eusociality. Nature 466:1057–1062

    Article  Google Scholar 

  • O’Brien M, Laland KN (2012) Genes, culture and agriculture: an example of human niche construction. Curr Anthro 53:434–470

    Google Scholar 

  • O’Neill RV, DeAngelis DL, Waide JB, Allen TFH (1986) A hierarchical concept of ecosystems. Princeton University Press, Princeton

    Google Scholar 

  • Odling-Smee FJ (1983) Multiple levels in evolution: an approach to the nature-nurture issue via ‘applied epistemology’. In: Davey (ed) Animal models of human behaviour. Wiley, Chichester, pp 135–158

  • Odling-Smee FJ (1988) Niche constructing phenotypes. In: Plotkin (ed) The role of behavior in evolution. MIT Press, Cambridge, pp 31–79

  • Odling-Smee FJ (2010) Niche inheritance In: Pigliucci, Muller (eds) Evolution: extended synthesis. MIT Press, Cambridge, pp 175–207

  • Odling-Smee FJ, Laland KN, Feldman MW (1996) Niche construction. Am Nat 147:641–648

    Article  Google Scholar 

  • Odling-Smee FJ, Laland KN, Feldman MW (2003) Niche construction: the neglected process in evolution, monographs in population biology, 37. Princeton University Press, Princeton

    Google Scholar 

  • Olson ME (2012) The renaissance of development in adaptationism. Trends Ecol Evol 27:278–287

    Article  Google Scholar 

  • Oyama S (1985) The ontogeny of information. Cambridge University Press, Cambridge

  • Oyama S, Griffiths PE, Gray RD (eds) (2001) Cycles of contingency: developmental systems and evolution. MIT Press, Cambridge

  • Pagel M (2012) Wired for culture: origins of the human social mind. WW Norton and Co., New York

  • Parker GA, Maynard-Smith J (1990) Optimality theory in evolutionary biology. Nature 348:27–33

    Article  Google Scholar 

  • Pelletier F, Garant D, Hendry AP (2009) Eco-evolutionary dynamics. Philos Trans R Soc B 364:1483–1489

    Article  Google Scholar 

  • Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP (2010) Phenotypic plasticity’s impacts on diversification and speciation. Trends Ecol Evol 25:459–467

    Article  Google Scholar 

  • Piersma T, van Gils JA (2011) The flexible phenotype. Oxford University Press, Oxford

  • Pigliucci M (2010) Genotype–phenotype mapping and the end of the ‘genes as blueprint’ metaphor. Philos Trans R Soc B 365:557–566

    Article  Google Scholar 

  • Pigliucci M, Muller GB (2010) Evolution. The Extended Synthesis. MIT Press, Cambridge

    Google Scholar 

  • Plotkin HC (1994) Darwin machines and the nature of knowledge. Penguin, New York

    Google Scholar 

  • Plotkin HC (2010) Evolutionary worlds without end. Oxford University Press, Oxford

    Book  Google Scholar 

  • Plotkin HC, Odling-Smee FJ (1981) A multiple-level model of evolution and its implications for sociobiology. Behav Brain Sci 4:225–268

    Article  Google Scholar 

  • Post DM, Palkovacs EP (2009) Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play. Philos Trans R Soc B 364:1629–1640

    Article  Google Scholar 

  • Pyne, Riel-Salvatore (eds) (2010) J Archaeol Method Theory, special edition

  • Richerson PJ, Boyd R (2005) Not by genes alone: how culture transformed human evolution. Chicago University Press, Chicago

    Google Scholar 

  • Richerson P, Boyd R, Henrich J (2010) Gene-culture coevolution in the age of genomics. Proc Natl Acad Sci USA 107:8985–8992

    Article  Google Scholar 

  • Roughgarden J (1979) Theory of population genetics and evolutionary ecology: an introduction. MacMillan, New York

  • Sahlins M (1976) The use and abuse of biology. An anthropological critique of sociobiology. University of Michigan Press, Ann Arbour

    Google Scholar 

  • Schmalhausen II (1949) Factors of evolution. Blakiston, Philadelphia

    Google Scholar 

  • Scott-Phillips T, Dickins T, West S (2011) Evolutionary theory and the ultimate-proximate distinction in the human behavioural sciences. Perspect Psychol Sci 6:38–47

    Article  Google Scholar 

  • Shea N, Pen I, Uller T (2011) Three epigenetic information channels and their different roles in evolution. J Evol Biol 24:1178–1187

    Article  Google Scholar 

  • Sherman PW (1988) The levels of analysis. Anim Behav 36:616–619

    Article  Google Scholar 

  • Shettleworth SJ (2010) Cognition, evolution, and behavior, 2nd edn. Oxford University Press, Oxford

  • Simpson GG (1949) The meaning of evolution. Yale University Press, New Haven

    Google Scholar 

  • Slobodkin L, Rapoport A (1974) An optimal strategy of evolution. Quart Rev Biol 49:187–200

    Google Scholar 

  • Smith BD (2007a) The ultimate ecosystem engineers. Science 315:1797–1798

    Article  Google Scholar 

  • Smith BD (2007b) Niche construction and the behavioral context of plant and animal domestication. Evol Anthro 16:188–199

    Article  Google Scholar 

  • Sober E (2000) Philosophy of biology, 2nd edn. Westview Press, Boulder

    Google Scholar 

  • Sterelny K (2012) The evolved apprentice: how evolution made humans unique. MIT Press, Cambridge

  • Sterelny K. Cooperation in a complex world. The role of proximate factors in ultimate explanations. Biol Theory (in press)

  • Stern DL (2010) Evolution, development and the predictable genome. Roberts & Company, Greenwood Village

    Google Scholar 

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

    Article  Google Scholar 

  • Thierry B (2005) Integrating proximate and ultimate causation: just one more go! Curr Sci 89:1180–1183

    Google Scholar 

  • Tinbergen N (1963) On aims and methods in ethology. Zeitschrift für Tierpsychologie 20:410–433

    Article  Google Scholar 

  • Tooby J, Cosmides L (1989) Evolutionary psychology and the generation of culture, part I: theoretical considerations. Ethol Sociobiol 10:29–49

    Article  Google Scholar 

  • Tooby J, Cosmides L (1992) The psychological foundations of culture. In: Barkow J, Cosmides L, Tooby J (eds) The adapted mind: evolutionary psychology and the generation of culture. Oxford University Press, Oxford, pp 137–159

  • Turner JS (2000) The extended organism: the physiology of animal-built structures. Harvard University Press, Cambridge

    Google Scholar 

  • Uller T (2012) Parental effects in development and evolution. In: Royle N, Smiseth P, Kölliker M (eds) Evolution of parental care. Oxford University Press, Oxford

  • Waddington CH (1962) Comment: on cause and effect in biology. Science 135:976

    Article  Google Scholar 

  • Waddington CH (1969) Paradigm for an evolutionary process. In: Waddington CH (ed) Towards a theoretical biology. Edinburgh University Press, Edinburgh

    Google Scholar 

  • Wagner GP, Altenberg L (1996) Perspective: complex adaptations and the evolution of evolvability. Evolution 50:967–976

    Article  Google Scholar 

  • Watt WB (2000) Avoiding paradigm-based limits to knowledge of evolution. Evol Biol 32:73–96

    Article  Google Scholar 

  • Watt WB (2004) Adaption, constraint, and neutrality: Mechanistic case studies with butterflies and their general implications. In: Singh, Uyenoyama (eds) The evolution of population biology. Cambridge University Press, Cambridge, pp 275–296

  • Waxman D, Gavrilets S (2005) 20 questions on adaptive dynamics. J Evol Biol 18:1139–1154

    Google Scholar 

  • West SA, El Mouden C, Gardner A (2011) 16 common misconceptions about the evolution of cooperation in humans. Evol Hum Behav 32:231–262

    Article  Google Scholar 

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

  • Westneat DF (2011) Behavioral ecology: 40 years of fusion with ecology. Behav Ecol 22:234–235

    Article  Google Scholar 

  • Wilson EO (1975) Sociobiology: the new synthesis. Harvard University Press, Cambridge

    Google Scholar 

Download references

Acknowledgments

We would like to thank Kim Sterelny who contributed substantially to the ideas presented in this article, and Tim Fawcett, Agustin Fuentes, Luc-Alain Giraldeau, Jerry Hogan, Kim Sterelny, Ward Watt, Stuart West, and two anonymous referees, who provided helpful comments on an earlier draft. Research supported in part by an ERC Advanced grant to KNL.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kevin N. Laland.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Laland, K.N., Odling-Smee, J., Hoppitt, W. et al. More on how and why: cause and effect in biology revisited. Biol Philos 28, 719–745 (2013). https://doi.org/10.1007/s10539-012-9335-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10539-012-9335-1

Keywords

  • Niche construction
  • Nongenetic inheritance
  • Evo-devo
  • Cultural evolution