Biology & Philosophy

, Volume 28, Issue 5, pp 719–745 | Cite as

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

  • Kevin N. Laland
  • John Odling-Smee
  • William Hoppitt
  • Tobias Uller


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.


Niche construction Nongenetic inheritance Evo-devo Cultural evolution 



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.


  1. Alcock J (1975) Animal behavior: an evolutionary approach, 1st edn. Sinauer, SunderlandGoogle Scholar
  2. Amundson R (2005) The changing role of the embryo in evolutionary thought. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  3. Antonovics J (1987) The evolutionary dys-synthesis: which bottles for which wine? Am Nat 129:321–331CrossRefGoogle Scholar
  4. Ariew A (2003) Ernst Mayr’s ‘ultimate/proximate’ distinction reconsidered and reconstructed. Biol Philos 18:553–565CrossRefGoogle Scholar
  5. Arthur W (2004) Biased embryo and evolution. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  6. Badyaev AV (2009) Evolutionary significance of phenotypic accommodation in novel environments: an empirical test of the Baldwin effect. Philos Trans R Soc B 364:1125–1141CrossRefGoogle Scholar
  7. 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 278:1921–1929CrossRefGoogle Scholar
  8. Badyaev AV, Uller T (2009) Parental effects in ecology and evolution: mechanisms, processes and implications. Philos Trans R Soc B 364:1169–1177CrossRefGoogle Scholar
  9. Baker J (1938) The evolution of breeding systems. In: de Beer (ed) Evolution: essays on aspects of evolutionary biology. Oxford University Press, OxfordGoogle Scholar
  10. Baldwin JM (1896) A new factor in evolution. Am Nat 30(441–451):536–553CrossRefGoogle Scholar
  11. Bateson P (1988) The active role of behaviour in evolution. In: Ho, Fox (eds) Evolutionary processes and metaphors. Wiley, New YorkGoogle Scholar
  12. Bateson P, Gluckman P (2011) Plasticity, robustness, development and evolution. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  13. 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
  14. Bickerton D (2009) Adam’s tongue: how humans made language, how language made humans. Hill and Wang, New YorkGoogle Scholar
  15. 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, OxfordGoogle Scholar
  16. Blute M (2010) Darwinian socioculture evolution: solutions to dilemmas in cultural and social theory. Cambridge University Press, CambridgeGoogle Scholar
  17. Bolhuis JJ, Verhulst S (2009) (eds) Tinbergen’s legacy. Cambridge University Press, CambridgeGoogle Scholar
  18. Bolhuis JJ, Brown GR, Richardson RC, Laland KN (2011) Darwin in mind: new opportunities for evolutionary psychology. PLoS Biol 9:e1001109CrossRefGoogle Scholar
  19. Boyd R, Richerson PJ (1985) Culture and the evolutionary process. Chicago University Press, ChicagoGoogle Scholar
  20. Boyd R, Gintis H, Bowles S, Richerson PJ (2003) The evolution of altruistic punishment. PNAS 100:3531–3535CrossRefGoogle Scholar
  21. Brakefield P (2006) Evo-devo and constraints on selection. Trends Ecol Evol 21:362–368CrossRefGoogle Scholar
  22. Brown GR, Laland KN, Borgerhoff-Mulder M (2009) Bateman’s principles and human sex roles. Trends Ecol Evol 24:297–304CrossRefGoogle Scholar
  23. Brown GR, Dickins TE, Sear R, Laland KN (2011) Evolutionary accounts of human behavioural diversity. Philos Trans R Soc B 366:313–324CrossRefGoogle Scholar
  24. Campbell DT (1974) Evolutionary epistemology. In: Schilpp (ed) The philosophy of Karl R. Popper. Chicago, Open Court, pp 413–463Google Scholar
  25. Cavalli-Sforza LL, Feldman MW (1981) Cultural transmission and evolution. University of Princeton Press, PrincetonGoogle Scholar
  26. Chudek M, Henrich J (2011) Culture-gene coevolution, norm-psychology and the emergence of human prosociality. Trends Cogn Sci 15:218–226CrossRefGoogle Scholar
  27. Cornwallis CK, Uller T (2010) Towards an evolutionary ecology of sexual traits. Trends Ecol Evol 25:145–152CrossRefGoogle Scholar
  28. Davies NB, Krebs JR, West SA (2012) An introduction to behavioural ecology, 4th edn. Wiley-Blackwell, New YorkGoogle Scholar
  29. Dawkins R (2004) Extended phenotype—but not too extended. A reply to Laland, Turner and Jablonka. Biol Physiol 19:377–396CrossRefGoogle Scholar
  30. Day T, Bonduriansky R (2011) A unified approach to the evolutionary consequences of genetic and nongenetic inheritance. Am Nat 178:E18–E36CrossRefGoogle Scholar
  31. De Jong G (2005) Evolution of phenotypic plasticity: patterns of plasticity and the emergence of ecotypes. New Phytol 166:101–117CrossRefGoogle Scholar
  32. De Jong G, Crozier RH (2003) Developmental plasticity and evolution. Nature 424:16–17CrossRefGoogle Scholar
  33. Dennett D (1995) Darwin’s dangerous idea: evolution and the meanings of life. Penguin, LondonGoogle Scholar
  34. Dewsbury D (1999) The proximate and the ultimate: past, present, and future. Behav Process 46:189–199CrossRefGoogle Scholar
  35. 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
  36. Dingermanse NJ, Karem AJN, Reale D, Wright J (2009) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25:81–89CrossRefGoogle Scholar
  37. Duckworth RA (2009) The role of behavior in evolution: a search for mechanism. Evol Ecol 23:513–531CrossRefGoogle Scholar
  38. Durham WH (1991) Coevolution: genes, culture and human diversity. Stanford University Press, Palo AltoGoogle Scholar
  39. Efferson C, Lalive R, Fehr E (2008) The coevolution of cultural groups and in group favoritism. Science 321:1844–1849CrossRefGoogle Scholar
  40. Ehrlich PR (1986) The machinery of nature. Simon and Schuster, New YorkGoogle Scholar
  41. Ehrlich P, Feldman M (2003) Genes and culture. What creates our behavioral phenome? Curr Anthro 44:87–107CrossRefGoogle Scholar
  42. Endler JA (1986) Natural selection in the wild. Princeton University Press, PrincetonGoogle Scholar
  43. Erwin DH (2008) Macroevolution of ecosystem engineering, niche construction and diversity. Trends Ecol Evol 23:304–310CrossRefGoogle Scholar
  44. Erwin DH, Tweedt S (2012) Ecological drivers of the Ediacaran diversification of metazoa. Evol Ecol 26:417–433CrossRefGoogle Scholar
  45. Ewald PW (1994) Evolution of infectious disease. Oxford University Press, New YorkGoogle Scholar
  46. 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
  47. Fehr E, Fischbacher U (2003) The nature of human altruism. Nature 425:785–791CrossRefGoogle Scholar
  48. Fisher RA (1958) The genetical theory of natural selection, 2nd edn. Dover, New YorkGoogle Scholar
  49. Ford EB (1964) Ecological genetics. Chapman and Hall, LondonGoogle Scholar
  50. Francis RC (1990) Causes, proximate and ultimate. Biol Philos 5:401–415CrossRefGoogle Scholar
  51. Frank SA (2009) Natural selection maximizes fisher information. J Evol Biol 22:231–244CrossRefGoogle Scholar
  52. Fuentes A (2009) Evolution of human behavior. Oxford University Press, OxfordGoogle Scholar
  53. Gilbert SF (2003) Developmental biology, 7th edn. Sinauer, SunderlandGoogle Scholar
  54. Gintis H (2003) The hitchhiker’s guide to altruism: gene-culture coevolution, and the internalization of norms. J Theor Biol 220:407–418CrossRefGoogle Scholar
  55. Godfrey-Smith P (1996) Complexity and the function of mind in nature. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  56. Gordon DM (2011a) The fusion of behavioural ecology and ecology. Behav Ecol 22:225–230CrossRefGoogle Scholar
  57. Gordon DM (2011b) The fusion of behavioural ecology and ecology, response after commentary. Behav Ecol 22:225–230CrossRefGoogle Scholar
  58. Gottlieb G (1992) Individual development and evolution. The genesis of novel behavior. Oxford University Press, New YorkGoogle Scholar
  59. Griffiths PE, Gray RD (1994) Developmental systems and evolutionary explanation. J Philos 91:277–304CrossRefGoogle Scholar
  60. Hagen JB (1992) An entangled bank: the origins of ecosystem ecology. Rutgers University Press, New BrunswickGoogle Scholar
  61. Haig D (2007) Weismann rules! OK? Epigenetics and the Lamarckian temptation. Biol Philos 22:415–428CrossRefGoogle Scholar
  62. 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 AngelesGoogle Scholar
  63. Harjunmaa E, Kallonen A, Voutilainen M, Hamalainen K, Mikkola ML, Jernvall J (2012) On the difficulty of increasing dental complexity. Nature 483:324Google Scholar
  64. Henrich J (2004) Cultural group selection, coevolutionary processes and large-scale cooperation. J Econ Behav Org 53:3–35CrossRefGoogle Scholar
  65. Henrich J, Heine SJ, Norenzayan A (2010) The weirdest people in the world. Behav Brain Sci 33:61–135CrossRefGoogle Scholar
  66. 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 3–15CrossRefGoogle Scholar
  67. 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 25–34Google Scholar
  68. Hood KE, Halpern CT, Greenberg G, Lerner RM (2010) Developmental science, behaviour, and genetics. Wiley-Blackwell, MassachusettsCrossRefGoogle Scholar
  69. Howson C (2000) Hume’s problem: induction and the justification of belief. Oxford University Press, OxfordGoogle Scholar
  70. Hull DL, Langman RE, Glenn SS (2001) A general account of selection: biology, immunology and behavior. Behav Brain Sci 24:511–573CrossRefGoogle Scholar
  71. Hume D (1910) [1748] An enquiry concerning human understanding. PF Collier & Son, New YorkGoogle Scholar
  72. Ingold T (2007) The trouble with ‘evolutionary biology’. Anthropol Today 23:13–17CrossRefGoogle Scholar
  73. Jablonka E, Lamb MJ (2005) Evolution in four dimensions. MIT Press, CambridgeGoogle Scholar
  74. Jones CG, Lawton JH (eds) (1995) Linking species and ecosystems. Chapman and Hall, New YorkGoogle Scholar
  75. Kavanagh KD, Evans AR, Jernvall J (2007) Predicting evolutionary patterns of mammalian teeth from development. Nature 449:427-U1CrossRefGoogle Scholar
  76. Kendal J, Tehrani JJ, Odling-Smee FJ (eds) (2011) Human niche construction in interdisciplinary focus. Philos Trans R Soc B 366, special editionGoogle Scholar
  77. Klopfer PH, Hailman JP (eds) (1972a) Function and evolution of behavior. Addison-Wesley, ReadingGoogle Scholar
  78. Klopfer PH, Hailman JP (eds) (1972b) Control and development of behavior. Addison-Wesley, ReadingGoogle Scholar
  79. 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 175–188Google Scholar
  80. Lack D (1954) The natural regulation of animal numbers. Oxford University Press, OxfordGoogle Scholar
  81. Laland KN, Brown GR (2006) Niche construction, human behavior, and the adaptive-lag hypothesis. Evol Anthro 15:95–104CrossRefGoogle Scholar
  82. Laland KN, Brown GR (2011) Sense and nonsense, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  83. Laland KN, Sterelny K (2006) Seven reasons (not) to neglect niche construction. Evolution 60:1751–1762Google Scholar
  84. Laland KN, Odling-Smee FJ, Feldman MW (1996) On the evolutionary consequences of niche construction. J Evol Biol 9:293–316CrossRefGoogle Scholar
  85. Laland KN, Odling-Smee FJ, Feldman MW (1999) Evolutionary consequences of niche construction and their implications for ecology. PNAS 96:10242–10247CrossRefGoogle Scholar
  86. Laland KN, Odling-Smee FJ, Gilbert SF (2008) EvoDevo and niche construction: building bridges. J Exp Zool B 310:549–566CrossRefGoogle Scholar
  87. 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 11:137–148CrossRefGoogle Scholar
  88. 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 334:1512–1516CrossRefGoogle Scholar
  89. Layton R (2010.)Why social scientists don’t like Darwin and what can be done about it. J Evol Psychol 8:139–152Google Scholar
  90. Lehmann L (2007) The evolution of trans-generational altruism: Kin selection meets niche construction. J Evol Biol 20:181–189CrossRefGoogle Scholar
  91. Lehmann L (2008) The adaptive dynamics of niche constructing traits in spatially subdivided populations: evolving posthumous extended phenotypes. Evolution 62:549–566CrossRefGoogle Scholar
  92. Leimar O, Hammerstein P, Van Dooren TJM (2006) A new perspective on developmental plasticity and the principles of adaptive morph determination. Am Nat 167:367–376CrossRefGoogle Scholar
  93. Levins R (1966) The strategy of model building in population biology. Am Scientist 54:421–431Google Scholar
  94. Lewontin RC (1982) Organism and environment. In: Plotkin (ed) Learning, development and culture. Wiley, New York, pp 151–170Google Scholar
  95. Lewontin RC (1983) Gene, organism and environment. In: Bendall (ed) Evolution from molecules to men. Cambridge University Press, Cambridge, pp 273–285Google Scholar
  96. 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, MassachusettsGoogle Scholar
  97. Likens GE (1995) Forward. In: Jones, Lawton (eds) Linking species and ecosystems. Chapman and Hall, New YorkGoogle Scholar
  98. Loreau M (2010) From populations to ecosystems: theoretical foundations for a new ecological synthesis. Monographs in Population Biology. Princeton University Press, Princeton, vol 46Google Scholar
  99. MacDougall-Shackleton (2011) The levels of analysis revisited. Philos Trans R Soc B 366:2076–2085CrossRefGoogle Scholar
  100. Maynard-Smith J (1982) Evolution and the theory of games. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  101. Maynard-Smith J, Burian R, Kaufman S, Alberch P, Campbell J et al (1985) Developmental constraints and evolution. Q Rev Biol 60:265–287CrossRefGoogle Scholar
  102. Mayr E (1958) Change of genetic environment and evolution. In: Huxley, Hardy Ford (eds) Evolution as a Process. Allen and Unwin, London, pp 188–213Google Scholar
  103. Mayr E (1961) Cause and effect in biology. Science 134:1501–1506CrossRefGoogle Scholar
  104. Mayr E (1974) Teleological and teleonomic, a new analysis. Boston Stud Philos Sci 14:91–117CrossRefGoogle Scholar
  105. Mayr E (1980) Some thoughts on the history of the evolutionary synthesis. In: Mayr, Provine (eds) The evolutionary synthesis. Harvard University Press, Cambridge, pp 1–48Google Scholar
  106. Mayr E (1984) The triumph of the evolutionary synthesis. Times Literary Suppl 2 November, pp 1261–1262Google Scholar
  107. Mayr E (1992) Controversies in retrospect. Evol Biol 8:1–34Google Scholar
  108. Mayr E (1993) Proximate and ultimate causations. Biol Philos 8:93–94CrossRefGoogle Scholar
  109. McNamara JM, Dall SRX (2010) Information is a fitness enhancing resource. Oikos 119:231–236CrossRefGoogle Scholar
  110. McNamara JM, Houston AI (1980) The application of statistical decision theory to animal behaviour. J Theor Biol 85:673–690CrossRefGoogle Scholar
  111. McNamara JM, Houston AI (2009) Integrating function and mechanism. Trend Ecol Evol 24:670–675CrossRefGoogle Scholar
  112. McNamara JM, Stephens PA, Dall SRX, Houston AI (2009) Evolution of trust and trustworthiness: social awareness favours personality differences. Proc R Soc B 276:605–613Google Scholar
  113. Mesoudi A (2011) Cultural evolution: how Darwinian theory can explain human culture and synthesize the social sciences. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  114. Mivart SG (1871) On the genesis of species. D Appleton and Co., New YorkCrossRefGoogle Scholar
  115. 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 278:2705–2713CrossRefGoogle Scholar
  116. Muller GB (2007) Evo-devo: extending the evolutionary synthesis. Nat Rev Genet 8:n953-946CrossRefGoogle Scholar
  117. Nowak M, Highfield R (2011) Super-cooperators: the mathematics of evolution, altruism and human behaviour (or why we need each other to succeed). Canongate, LondonGoogle Scholar
  118. Nowak MA, Tarnita CE, Wilson EO (2010) The evolution of eusociality. Nature 466:1057–1062CrossRefGoogle Scholar
  119. O’Brien M, Laland KN (2012) Genes, culture and agriculture: an example of human niche construction. Curr Anthro 53:434–470Google Scholar
  120. O’Neill RV, DeAngelis DL, Waide JB, Allen TFH (1986) A hierarchical concept of ecosystems. Princeton University Press, PrincetonGoogle Scholar
  121. 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 135–158Google Scholar
  122. Odling-Smee FJ (1988) Niche constructing phenotypes. In: Plotkin (ed) The role of behavior in evolution. MIT Press, Cambridge, pp 31–79Google Scholar
  123. Odling-Smee FJ (2010) Niche inheritance In: Pigliucci, Muller (eds) Evolution: extended synthesis. MIT Press, Cambridge, pp 175–207Google Scholar
  124. Odling-Smee FJ, Laland KN, Feldman MW (1996) Niche construction. Am Nat 147:641–648CrossRefGoogle Scholar
  125. Odling-Smee FJ, Laland KN, Feldman MW (2003) Niche construction: the neglected process in evolution, monographs in population biology, 37. Princeton University Press, PrincetonGoogle Scholar
  126. Olson ME (2012) The renaissance of development in adaptationism. Trends Ecol Evol 27:278–287CrossRefGoogle Scholar
  127. Oyama S (1985) The ontogeny of information. Cambridge University Press, CambridgeGoogle Scholar
  128. Oyama S, Griffiths PE, Gray RD (eds) (2001) Cycles of contingency: developmental systems and evolution. MIT Press, CambridgeGoogle Scholar
  129. Pagel M (2012) Wired for culture: origins of the human social mind. WW Norton and Co., New YorkGoogle Scholar
  130. Parker GA, Maynard-Smith J (1990) Optimality theory in evolutionary biology. Nature 348:27–33CrossRefGoogle Scholar
  131. Pelletier F, Garant D, Hendry AP (2009) Eco-evolutionary dynamics. Philos Trans R Soc B 364:1483–1489CrossRefGoogle Scholar
  132. 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 25:459–467CrossRefGoogle Scholar
  133. Piersma T, van Gils JA (2011) The flexible phenotype. Oxford University Press, OxfordGoogle Scholar
  134. Pigliucci M (2010) Genotype–phenotype mapping and the end of the ‘genes as blueprint’ metaphor. Philos Trans R Soc B 365:557–566CrossRefGoogle Scholar
  135. Pigliucci M, Muller GB (2010) Evolution. The Extended Synthesis. MIT Press, CambridgeGoogle Scholar
  136. Plotkin HC (1994) Darwin machines and the nature of knowledge. Penguin, New YorkGoogle Scholar
  137. Plotkin HC (2010) Evolutionary worlds without end. Oxford University Press, OxfordCrossRefGoogle Scholar
  138. Plotkin HC, Odling-Smee FJ (1981) A multiple-level model of evolution and its implications for sociobiology. Behav Brain Sci 4:225–268CrossRefGoogle Scholar
  139. 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 364:1629–1640CrossRefGoogle Scholar
  140. Pyne, Riel-Salvatore (eds) (2010) J Archaeol Method Theory, special editionGoogle Scholar
  141. Richerson PJ, Boyd R (2005) Not by genes alone: how culture transformed human evolution. Chicago University Press, ChicagoGoogle Scholar
  142. Richerson P, Boyd R, Henrich J (2010) Gene-culture coevolution in the age of genomics. Proc Natl Acad Sci USA 107:8985–8992CrossRefGoogle Scholar
  143. Roughgarden J (1979) Theory of population genetics and evolutionary ecology: an introduction. MacMillan, New YorkGoogle Scholar
  144. Sahlins M (1976) The use and abuse of biology. An anthropological critique of sociobiology. University of Michigan Press, Ann ArbourGoogle Scholar
  145. Schmalhausen II (1949) Factors of evolution. Blakiston, PhiladelphiaGoogle Scholar
  146. Scott-Phillips T, Dickins T, West S (2011) Evolutionary theory and the ultimate-proximate distinction in the human behavioural sciences. Perspect Psychol Sci 6:38–47CrossRefGoogle Scholar
  147. Shea N, Pen I, Uller T (2011) Three epigenetic information channels and their different roles in evolution. J Evol Biol 24:1178–1187CrossRefGoogle Scholar
  148. Sherman PW (1988) The levels of analysis. Anim Behav 36:616–619CrossRefGoogle Scholar
  149. Shettleworth SJ (2010) Cognition, evolution, and behavior, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  150. Simpson GG (1949) The meaning of evolution. Yale University Press, New HavenGoogle Scholar
  151. Slobodkin L, Rapoport A (1974) An optimal strategy of evolution. Quart Rev Biol 49:187–200Google Scholar
  152. Smith BD (2007a) The ultimate ecosystem engineers. Science 315:1797–1798CrossRefGoogle Scholar
  153. Smith BD (2007b) Niche construction and the behavioral context of plant and animal domestication. Evol Anthro 16:188–199CrossRefGoogle Scholar
  154. Sober E (2000) Philosophy of biology, 2nd edn. Westview Press, BoulderGoogle Scholar
  155. Sterelny K (2012) The evolved apprentice: how evolution made humans unique. MIT Press, CambridgeGoogle Scholar
  156. Sterelny K. Cooperation in a complex world. The role of proximate factors in ultimate explanations. Biol Theory (in press)Google Scholar
  157. Stern DL (2010) Evolution, development and the predictable genome. Roberts & Company, Greenwood VillageGoogle Scholar
  158. ten Cate C (2000) How learning mechanisms might affect evolutionary processes. Trend Ecol Evol 15:179–181CrossRefGoogle Scholar
  159. Thierry B (2005) Integrating proximate and ultimate causation: just one more go! Curr Sci 89:1180–1183Google Scholar
  160. Tinbergen N (1963) On aims and methods in ethology. Zeitschrift für Tierpsychologie 20:410–433CrossRefGoogle Scholar
  161. Tooby J, Cosmides L (1989) Evolutionary psychology and the generation of culture, part I: theoretical considerations. Ethol Sociobiol 10:29–49CrossRefGoogle Scholar
  162. 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 137–159Google Scholar
  163. Turner JS (2000) The extended organism: the physiology of animal-built structures. Harvard University Press, CambridgeGoogle Scholar
  164. Uller T (2012) Parental effects in development and evolution. In: Royle N, Smiseth P, Kölliker M (eds) Evolution of parental care. Oxford University Press, OxfordGoogle Scholar
  165. Waddington CH (1962) Comment: on cause and effect in biology. Science 135:976CrossRefGoogle Scholar
  166. Waddington CH (1969) Paradigm for an evolutionary process. In: Waddington CH (ed) Towards a theoretical biology. Edinburgh University Press, EdinburghGoogle Scholar
  167. Wagner GP, Altenberg L (1996) Perspective: complex adaptations and the evolution of evolvability. Evolution 50:967–976CrossRefGoogle Scholar
  168. Watt WB (2000) Avoiding paradigm-based limits to knowledge of evolution. Evol Biol 32:73–96CrossRefGoogle Scholar
  169. 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 275–296Google Scholar
  170. Waxman D, Gavrilets S (2005) 20 questions on adaptive dynamics. J Evol Biol 18:1139–1154Google Scholar
  171. West SA, El Mouden C, Gardner A (2011) 16 common misconceptions about the evolution of cooperation in humans. Evol Hum Behav 32:231–262CrossRefGoogle Scholar
  172. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, OxfordGoogle Scholar
  173. Westneat DF (2011) Behavioral ecology: 40 years of fusion with ecology. Behav Ecol 22:234–235CrossRefGoogle Scholar
  174. Wilson EO (1975) Sociobiology: the new synthesis. Harvard University Press, CambridgeGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Kevin N. Laland
    • 1
  • John Odling-Smee
    • 2
  • William Hoppitt
    • 1
  • Tobias Uller
    • 3
  1. 1.School of BiologyUniversity of St AndrewsSt AndrewsUK
  2. 2.Mansfield CollegeUniversity of OxfordOxfordUK
  3. 3.Department of Zoology, Edward Grey InstituteUniversity of OxfordOxfordUK

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