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.
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References
Alcock J (1975) Animal behavior: an evolutionary approach, 1st edn. Sinauer, Sunderland
Amundson R (2005) The changing role of the embryo in evolutionary thought. Cambridge University Press, Cambridge
Antonovics J (1987) The evolutionary dys-synthesis: which bottles for which wine? Am Nat 129:321–331
Ariew A (2003) Ernst Mayr’s ‘ultimate/proximate’ distinction reconsidered and reconstructed. Biol Philos 18:553–565
Arthur W (2004) Biased embryo and evolution. Cambridge University Press, Cambridge
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
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
Badyaev AV, Uller T (2009) Parental effects in ecology and evolution: mechanisms, processes and implications. Philos Trans R Soc B 364:1169–1177
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
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
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
Bickerton D (2009) Adam’s tongue: how humans made language, how language made humans. Hill and Wang, New York
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
Boyd R, Richerson PJ (1985) Culture and the evolutionary process. Chicago University Press, Chicago
Boyd R, Gintis H, Bowles S, Richerson PJ (2003) The evolution of altruistic punishment. PNAS 100:3531–3535
Brakefield P (2006) Evo-devo and constraints on selection. Trends Ecol Evol 21:362–368
Brown GR, Laland KN, Borgerhoff-Mulder M (2009) Bateman’s principles and human sex roles. Trends Ecol Evol 24:297–304
Brown GR, Dickins TE, Sear R, Laland KN (2011) Evolutionary accounts of human behavioural diversity. Philos Trans R Soc B 366:313–324
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
Chudek M, Henrich J (2011) Culture-gene coevolution, norm-psychology and the emergence of human prosociality. Trends Cogn Sci 15:218–226
Cornwallis CK, Uller T (2010) Towards an evolutionary ecology of sexual traits. Trends Ecol Evol 25:145–152
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
Day T, Bonduriansky R (2011) A unified approach to the evolutionary consequences of genetic and nongenetic inheritance. Am Nat 178:E18–E36
De Jong G (2005) Evolution of phenotypic plasticity: patterns of plasticity and the emergence of ecotypes. New Phytol 166:101–117
De Jong G, Crozier RH (2003) Developmental plasticity and evolution. Nature 424:16–17
Dennett D (1995) Darwin’s dangerous idea: evolution and the meanings of life. Penguin, London
Dewsbury D (1999) The proximate and the ultimate: past, present, and future. Behav Process 46:189–199
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
Duckworth RA (2009) The role of behavior in evolution: a search for mechanism. Evol Ecol 23:513–531
Durham WH (1991) Coevolution: genes, culture and human diversity. Stanford University Press, Palo Alto
Efferson C, Lalive R, Fehr E (2008) The coevolution of cultural groups and in group favoritism. Science 321:1844–1849
Ehrlich PR (1986) The machinery of nature. Simon and Schuster, New York
Ehrlich P, Feldman M (2003) Genes and culture. What creates our behavioral phenome? Curr Anthro 44:87–107
Endler JA (1986) Natural selection in the wild. Princeton University Press, Princeton
Erwin DH (2008) Macroevolution of ecosystem engineering, niche construction and diversity. Trends Ecol Evol 23:304–310
Erwin DH, Tweedt S (2012) Ecological drivers of the Ediacaran diversification of metazoa. Evol Ecol 26:417–433
Ewald PW (1994) Evolution of infectious disease. Oxford University Press, New York
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
Fisher RA (1958) The genetical theory of natural selection, 2nd edn. Dover, New York
Ford EB (1964) Ecological genetics. Chapman and Hall, London
Francis RC (1990) Causes, proximate and ultimate. Biol Philos 5:401–415
Frank SA (2009) Natural selection maximizes fisher information. J Evol Biol 22:231–244
Fuentes A (2009) Evolution of human behavior. Oxford University Press, Oxford
Gilbert SF (2003) Developmental biology, 7th edn. Sinauer, Sunderland
Gintis H (2003) The hitchhiker’s guide to altruism: gene-culture coevolution, and the internalization of norms. J Theor Biol 220:407–418
Godfrey-Smith P (1996) Complexity and the function of mind in nature. Cambridge University Press, Cambridge
Gordon DM (2011a) The fusion of behavioural ecology and ecology. Behav Ecol 22:225–230
Gordon DM (2011b) The fusion of behavioural ecology and ecology, response after commentary. Behav Ecol 22:225–230
Gottlieb G (1992) Individual development and evolution. The genesis of novel behavior. Oxford University Press, New York
Griffiths PE, Gray RD (1994) Developmental systems and evolutionary explanation. J Philos 91:277–304
Hagen JB (1992) An entangled bank: the origins of ecosystem ecology. Rutgers University Press, New Brunswick
Haig D (2007) Weismann rules! OK? Epigenetics and the Lamarckian temptation. Biol Philos 22:415–428
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
Harjunmaa E, Kallonen A, Voutilainen M, Hamalainen K, Mikkola ML, Jernvall J (2012) On the difficulty of increasing dental complexity. Nature 483:324
Henrich J (2004) Cultural group selection, coevolutionary processes and large-scale cooperation. J Econ Behav Org 53:3–35
Henrich J, Heine SJ, Norenzayan A (2010) The weirdest people in the world. Behav Brain Sci 33:61–135
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
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
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
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
Jablonka E, Lamb MJ (2005) Evolution in four dimensions. MIT Press, Cambridge
Jones CG, Lawton JH (eds) (1995) Linking species and ecosystems. Chapman and Hall, New York
Kavanagh KD, Evans AR, Jernvall J (2007) Predicting evolutionary patterns of mammalian teeth from development. Nature 449:427-U1
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
Klopfer PH, Hailman JP (eds) (1972b) Control and development of behavior. Addison-Wesley, Reading
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
Laland KN, Brown GR (2006) Niche construction, human behavior, and the adaptive-lag hypothesis. Evol Anthro 15:95–104
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
Laland KN, Odling-Smee FJ, Feldman MW (1996) On the evolutionary consequences of niche construction. J Evol Biol 9:293–316
Laland KN, Odling-Smee FJ, Feldman MW (1999) Evolutionary consequences of niche construction and their implications for ecology. PNAS 96:10242–10247
Laland KN, Odling-Smee FJ, Gilbert SF (2008) EvoDevo and niche construction: building bridges. J Exp Zool B 310:549–566
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
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
Layton R (2010.)Why social scientists don’t like Darwin and what can be done about it. J Evol Psychol 8:139–152
Lehmann L (2007) The evolution of trans-generational altruism: Kin selection meets niche construction. J Evol Biol 20:181–189
Lehmann L (2008) The adaptive dynamics of niche constructing traits in spatially subdivided populations: evolving posthumous extended phenotypes. Evolution 62:549–566
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
Levins R (1966) The strategy of model building in population biology. Am Scientist 54:421–431
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
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
Maynard-Smith J (1982) Evolution and the theory of games. Cambridge University Press, Cambridge
Maynard-Smith J, Burian R, Kaufman S, Alberch P, Campbell J et al (1985) Developmental constraints and evolution. Q Rev Biol 60:265–287
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
Mayr E (1961) Cause and effect in biology. Science 134:1501–1506
Mayr E (1974) Teleological and teleonomic, a new analysis. Boston Stud Philos Sci 14:91–117
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
Mayr E (1993) Proximate and ultimate causations. Biol Philos 8:93–94
McNamara JM, Dall SRX (2010) Information is a fitness enhancing resource. Oikos 119:231–236
McNamara JM, Houston AI (1980) The application of statistical decision theory to animal behaviour. J Theor Biol 85:673–690
McNamara JM, Houston AI (2009) Integrating function and mechanism. Trend Ecol Evol 24:670–675
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
Mesoudi A (2011) Cultural evolution: how Darwinian theory can explain human culture and synthesize the social sciences. University of Chicago Press, Chicago
Mivart SG (1871) On the genesis of species. D Appleton and Co., New York
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
Muller GB (2007) Evo-devo: extending the evolutionary synthesis. Nat Rev Genet 8:n953-946
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
Nowak MA, Tarnita CE, Wilson EO (2010) The evolution of eusociality. Nature 466:1057–1062
O’Brien M, Laland KN (2012) Genes, culture and agriculture: an example of human niche construction. Curr Anthro 53:434–470
O’Neill RV, DeAngelis DL, Waide JB, Allen TFH (1986) A hierarchical concept of ecosystems. Princeton University Press, Princeton
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
Odling-Smee FJ, Laland KN, Feldman MW (2003) Niche construction: the neglected process in evolution, monographs in population biology, 37. Princeton University Press, Princeton
Olson ME (2012) The renaissance of development in adaptationism. Trends Ecol Evol 27:278–287
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
Pelletier F, Garant D, Hendry AP (2009) Eco-evolutionary dynamics. Philos Trans R Soc B 364:1483–1489
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
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
Pigliucci M, Muller GB (2010) Evolution. The Extended Synthesis. MIT Press, Cambridge
Plotkin HC (1994) Darwin machines and the nature of knowledge. Penguin, New York
Plotkin HC (2010) Evolutionary worlds without end. Oxford University Press, Oxford
Plotkin HC, Odling-Smee FJ (1981) A multiple-level model of evolution and its implications for sociobiology. Behav Brain Sci 4:225–268
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
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
Richerson P, Boyd R, Henrich J (2010) Gene-culture coevolution in the age of genomics. Proc Natl Acad Sci USA 107:8985–8992
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
Schmalhausen II (1949) Factors of evolution. Blakiston, Philadelphia
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
Shea N, Pen I, Uller T (2011) Three epigenetic information channels and their different roles in evolution. J Evol Biol 24:1178–1187
Sherman PW (1988) The levels of analysis. Anim Behav 36:616–619
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
Slobodkin L, Rapoport A (1974) An optimal strategy of evolution. Quart Rev Biol 49:187–200
Smith BD (2007a) The ultimate ecosystem engineers. Science 315:1797–1798
Smith BD (2007b) Niche construction and the behavioral context of plant and animal domestication. Evol Anthro 16:188–199
Sober E (2000) Philosophy of biology, 2nd edn. Westview Press, Boulder
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
ten Cate C (2000) How learning mechanisms might affect evolutionary processes. Trend Ecol Evol 15:179–181
Thierry B (2005) Integrating proximate and ultimate causation: just one more go! Curr Sci 89:1180–1183
Tinbergen N (1963) On aims and methods in ethology. Zeitschrift für Tierpsychologie 20:410–433
Tooby J, Cosmides L (1989) Evolutionary psychology and the generation of culture, part I: theoretical considerations. Ethol Sociobiol 10:29–49
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
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
Waddington CH (1969) Paradigm for an evolutionary process. In: Waddington CH (ed) Towards a theoretical biology. Edinburgh University Press, Edinburgh
Wagner GP, Altenberg L (1996) Perspective: complex adaptations and the evolution of evolvability. Evolution 50:967–976
Watt WB (2000) Avoiding paradigm-based limits to knowledge of evolution. Evol Biol 32:73–96
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
West SA, El Mouden C, Gardner A (2011) 16 common misconceptions about the evolution of cooperation in humans. Evol Hum Behav 32:231–262
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
Wilson EO (1975) Sociobiology: the new synthesis. Harvard University Press, Cambridge
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.
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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
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DOI: https://doi.org/10.1007/s10539-012-9335-1