Beyond DNA: Integrating inclusive inheritance into an extended theory of evolution

Nature Reviews Genetics

Volumn 12, Issue 7, 2011, Pages 475-486

  Danchin, Étienne ^a,b,c,d   Charmantier, Anne ^e   Champagne, Frances A ^f   Mesoudi, Alex ^g   Pujol, Benoit ^a,b,d   Blanchet, Simon ^a,b,c,d,h,i  

^a Centre National de la Recherce Scientifique (CNRS)   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c École Nationale de Formation Agronomique ENFA   (France)

^d École Nationale de Formation Agronomique   (France)

^e CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^f Och Spine at New York Presbyterian Hospitals   (United States)

^g QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^h CNRS   (France)

ⁱ Centre National de la Recherche Scientifique and Paul Sabatier University   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CULTURAL FACTOR; ECOLOGY; EPIGENETICS; EVOLUTION; HERITABILITY; HUMAN; INHERITANCE; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; REVIEW;

ANIMALS; BIOLOGICAL EVOLUTION; DNA; ECOLOGY; EPIGENESIS, GENETIC; HUMANS; INHERITANCE PATTERNS; MODELS, BIOLOGICAL; MODELS, THEORETICAL; SYSTEMS INTEGRATION;

EID: 79959439333     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg3028     Document Type: Review

References (162)

1. Lamarck, J. B. P. A. Phylosophie Zoologique (Dentus, Paris, 1809).
2. Darwin, C. On the Origin of Species by Means of Natural Selection (John Murray, London, 1859).
3. West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford Univ. Press, Oxford, 2003).
4. Danchin, É., Giraldeau, L. A., Valone, T. J. & Wagner, R. H. Public information: from nosy neighbors to cultural evolution. Science 305, 487-491 (2004). (Pubitemid 38971332)
5. Mameli, M. Nongenetic selection an nongenetic inheritance. Br. J. Philos. Sci. 55, 35-71 (2004).
6. Johannes, F., Colot, V. & Jansen, R. C. Epigenome dynamics: a quantitative genetics perspective. Nature Rev. Genet. 9, 883-890 (2008).
7. Helanterä, H. & Uller, T. The Price equation and extended inheritance. Philos.Theory Biol. 2, 1-17 (2010).
8. Jablonka, E. & Lamb, M. J. in Evolution: The Extended Synthesis (eds Pigliucci, M. & Müller, G. B.) 137-174 (MIT Press, Cambridge, Massachusetts, 2010).
9. Danchin, É. & Wagner, R. H. Inclusive heritability: combining genetic and nongenetic information to study animal culture. Oikos 119, 210-218 (2010).
10. Maher, B. Personal genomes: the case of the missing heritability. Nature 456, 18-21 (2008).
11. Bird, A. Perceptions of epigenetics. Nature 447, 396-398 (2007). (Pubitemid 46816744)
12. Bonduriansky, R. & Day, T. Nongenetic inheritance and its evolutionary implications. Ann. Rev. Ecol. Evol. Syst. 40, 103-125 (2009).
13. Pigliucci, M. & Müller, G. B. Evolution: The Extended Synthesis (MIT Press, Cambridge, Massachusetts, 2010).
14. Tal, O., Kisdi, E. & Jablonka, E. Epigenetic contribution to covariance between relatives. Genetics 184, 1037-1050 (2010).
15. McElreath, R. & Henrich, J. in Oxford Handbook of Evolutionary Psychology (eds Dunbar, R. & Barrett, L.) 571-585 (Oxford Univ. Press, Oxford, 2009).
16. Ellegren, H. & Sheldon, B. C. Genetic basis of fitness differences in natural populations. Nature 452, 169-175 (2008). (Pubitemid 351380250)
17. Cubas, P., Vincent, C. & Coen, E. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401, 157-161 (1999). (Pubitemid 29436317)
18. Richards, E. J. Inherited epigenetic variation - revisiting soft inheritance. Nature Rev. Genet. 7, 395-401 (2006).
19. Bossdorf, O., Richards, C. L. & Pigliucci, M. Epigenetics for ecologists. Ecol. Lett. 11, 106-115 (2008).
20. Riddihough, G. & Zahan, L. M. What is epignenetics? Science 330, 611 (2010).
21. Wilkinson, L. S., Davies, W. & Isles, A. R. Genomic imprinting effects on brain development and function. Nature Rev. Neurosci. 8, 832-843 (2007). (Pubitemid 350006217)
22. Anway, M. D., Cupp, A. S., Uzumcu, M. & Skinner, M. K. Epigenetic transgenerational actions of endocrine disruptors and mate fertility. Science 308, 1466-1469 (2005). (Pubitemid 40791300)
23. Champagne, F. A. & Meaney, M. J. Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biol. Psychiatry 59, 1227-1235 (2006). (Pubitemid 43949142)
24. Champagne, F. A. et al. Maternal care associated with methylation of the estrogen receptor-α 1b promoter and estrogen receptor-α expression in the medial preoptic area of female offspring. Endocrinol. 147, 2909-2915 (2006). (Pubitemid 43764626)
25. Champagne, F. A. & Meaney, M. J. Transgenerational effects of social environment on variations in maternal care and behavioural response to novelty. Behav. Neurosci. 121, 1353-1363 (2007).
26. Champagne, F. A. Epigenetic mechanisms and the transgenerational effects of maternal care. Front. Neuroendocrinol. 29, 386-397 (2008).
27. Morgan, H. D., Sutherland, H. G. E., Martin, D. I. K. & Whitelaw, E. Epigenetic inheritance at the agouti locus in the mouse. Nature Genet. 23, 314-318 (1999). (Pubitemid 29526429)
28. Rosenfeld, C. S. Animal models to study environmental epigenetics. Biol. Reprod. 82, 473-488 (2010).
29. Crews, D. et al. Transgenerational epigenetic imprints on mate preference. Proc. Natl Acad. Sci. USA 104, 5942-5946 (2007). (Pubitemid 47175638)
30. Heijmans, B. T. et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl Acad. Sci. USA 105, 17046-17049 (2008).
31. Halfmann, R. & Lindquist, S. Epigenetics in the extreme: prions and the inheritance of environmentally acquired traits. Science 330, 629-632 (2010).
32. Smits, G. et al. Conservation of the H19 noncoding RNA and H19-IGF2 imprinting mechanism in therians. Nature Genet. 40, 971-976 (2008).
33. Mousseau, T. A. & Fox, C. W. The adaptive significance of maternal effects. Trends Ecol. Evol. 13, 403-407 (1998). (Pubitemid 28430680)
34. Galloway, L. F. & Etterson, J. R. Transgenerational plasticity is adaptive in the wild. Science 318, 1134-1136 (2007). (Pubitemid 350134895)
35. Falconer, D. S. Introduction to Quantitative Genetics (Longman, New York, 1981).
36. Kirkpatrick, M. & Lande, R. The evolution of maternal characters. Evolution 43, 485-503 (1989). (Pubitemid 20419131)
37. Wilson, A. J. et al. Maternal genetic effects set the potential for evolution in a free-living vertebrate population. J. Evol. Biol. 18, 405-414 (2005). (Pubitemid 40350935)
38. Rossiter, M. C. Incidence and consequences of inherited environmental effects. Ann. Rev. Ecol. Syst. 27, 451-476 (1996). (Pubitemid 27079292)
39. Wolf, J. B., Brodie, E. D., Cheverud, J. M., Moore, A. J. & Wade, M. J. Evolutionary consequences of indirect genetic effects. Trends Ecol. Evol. 13, 64-69 (1998). (Pubitemid 28081009)
40. McGlothlin, J. W., Moore, A. J., Wolf, J. B. & Brodie, E. D. Interacting phenotypes and the evolutionary process. III. Social selection. Evolution 64, 2558-2574 (2010).
41. Wilson, A. J., Gelin, U., Perron, M.-C. & Rale, D. Indirect genetic effects and the evolution of aggression in a vertebrate system. Proc. R. Soc. B 276, 533-541 (2009).
42. McGlothlin, J. W. & Brodie, E. D. How to measure indirect genetic effects: the congruence of trait-based and variance-partitioning approaches. Evolution 63, 1785-1795 (2009).
43. Hager, R., Cheverud, J. M. & Wolf, J. B. Maternal effects as the cause of parent-of-origin effects that mimic genomic imprinting. Genetics 178, 1755-1762 (2008).
44. Qvarnstrom, A. & Price, T. D. Maternal effects, paternal effects and sexual selection. Trends Ecol. Evol. 16, 95-100 (2001). (Pubitemid 32126268)
45. Andersson, M. & Simmons, L. W. Sexual selection and mate choice. Trends Ecol. Evol. 21, 296-302 (2006). (Pubitemid 43850058)
46. Griffith, S. C., Owens, I. P. F. & Burke, T. Environmental determination of a sexually selected trait. Nature 400, 358-360 (1999). (Pubitemid 29344199)
47. Kendrick, K. M., Hinton, M. R., Atkins, K., Haupt, M. A. & Skinner, J. D. Mothers determine sexual preferences. Nature 395, 229-230 (1998).
48. Mazer, S. J. & Gorchov, D. L. Parental effects on progeny phenotype in plants: distinguishing genetic and environmental causes. Evolution 50, 44-53 (1996).
49. Gasparini, J., McCoy, K. D., Haussy, C., Tveraa, T. & Boulinier, T. Induced maternal response to the Lyme disease spirochaete Borrelia burgdorferi senus lato in a colonial seabird, the kittiwake, Rissa tridactyla. Proc. R. Soc. Lond. B 268, 647-650 (2001). (Pubitemid 32269854)
50. Gasparini, J., McCoy, K., Staszewski, V., Haussy, C. & Boulinier, T. Dynamics of anti-Borrelia antibodies in Black-legged Kittiwakes (Rissa tridactyla) chicks suggest a maternal educational effect. Can. J. Zool. 84, 623-627 (2006). (Pubitemid 44049538)
51. Curley, J. P., Davidson, S., Bateson, P. & Champagne, F. A. Social enrichment during postnatal development induces transgenerational effects on emotional and reproductive behaviour in mice. Front. Behav. Neurosci. 3, 1-14 (2009).
52. Curley, J. P., Champagne, F. A., Bateson, P. & Keverne, E. B. Transgenerational effects of impaired maternal care on behaviour of offspring and grandoffspring. Anim. Behav. 75, 1551-1561 (2008).
53. Kruuk, L. E. B. Estimating genetic parameters in natural populations using the 'animal model'. Phil. Trans. R. Soc. Lond. B 359, 873-890 (2004). (Pubitemid 38784077)
54. Kruuk, L. E. B. & Hadfield, J. D. How to separate genetic and environmental causes of similarity between relatives. J. Evol. Biol. 20, 1890-1903 (2007). (Pubitemid 47262852)
55. Darwin, C. The Formation of Vegetable Mould Through the Action of Worms, with Observations on their Habits (John Murray, London, 1881).
56. Odling Smee, F. J., Laland, K. N. & Feldman, M. Niche Construction (Princeton Univ. Press, Princeton, New Jersey, 2003).
57. Odling-Smee, J. in Evolution: The Extended Synthesis (eds Pigliucci, M. & M?ller, G. B.) 175-207 (MIT Press, Cambridge, Massachusetts, 2010).
58. Turner, J. S. The Extended Organism: The Physiology of Animal-Built Structures (Harvard Univ. Press, Cambridge, Massachusetts, 2000).
59. Erwin, D. H. Macroevolution of ecosystem engineering, niche construction and diversity. Trends Ecol. Evol. 23, 304-310 (2008). (Pubitemid 351699269)
60. Krakauer, D. C., Page, K. M. & Erwin, D. H. Diversity, dilemmas, and monopolies of niche construction. Am. Nat. 173, 26-40 (2009).
61. Laland, K. N. & Sterelny, K. Seven reasons (not) to neglect niche construction. Evolution 60, 1751-1762 (2006). (Pubitemid 44808227)
62. Lehmann, L. The adaptive dynamics of niche constructing traits in spatially subdivided populations: evolving posthumous extended phenotypes. Evolution 62, 549-566 (2008). (Pubitemid 351348246)
63. Laland, K. N. & Brown, G. R. Niche construction, human behaviour, and the adaptive-lag hypothesis. Evol. Anthropol. 15, 95-104 (2006). (Pubitemid 44085995)
64. Jaffee, S. R. & Price, T. S. Gene-environment correlations: a review of the evidence and implications for prevention of mental illness. Mol. Psychiatry 12, 432-442 (2007). (Pubitemid 46652458)
65. Cavalli-Sforza, L. L. & Feldman, M. W. Cultural Transmission and Evolution: A Quantitative Approach (Princeton Univ. Press, Princeton, New Jersey, 1981).
66. Boyd, R. & Richerson, P. J. Culture and the Evolutionary Process (Univ. Chicago Press, Chicago, Illinois, 1985).
67. Mesoudi, A., Whiten, A. & Laland, K. N. Is human cultural evolution Darwinian? Evidence reviewed from the perspective of The Origin of Species. Evolution 58, 1-11 (2004). (Pubitemid 38355633)
68. Mesoudi, A. Cultural Evolution (Univ. Chicago Press, Chicago, Illinois, 2011).
69. Whiten, A. The second inheritance system of chimpanzees and humans. Nature 437, 52-55 (2005). (Pubitemid 41613424)
70. Laland, K. N. & Galef, B. G. The Question of Animal Culture (Harvard Univ. Press, Cambridge, Massachusetts, 2009).
71. Horner, V., Whiten, A., Flynn, E. & de Waal, F. B. M. Faithful replication of foraging techniques along cultural transmission chains by chimpanzees and children. Proc. Natl Acad. Sci. USA 103, 13878-13883 (2006). (Pubitemid 44414001)
72. Whiten, A. & Mesoudi, A. An experimental science of culture: animal social diffusion experiments. Phil. Trans. R. Soc. B 363, 3477-3488 (2008).
73. Wagner, R. H. & Danchin, É. A taxonomy of biological information. Oikos 119, 203-209 (2010).
74. Coolen, I., van Bergen, Y., Day, R. L. & Laland, K. N. Species difference in adaptive use of public information in stickleblacks. Proc. R. Soc. Lond. B 270, 2413-2419 (2003). (Pubitemid 37464027)
75. Doligez, B., Danchin, É. & Clobert, J. Public information and breeding habitat selection in a wild bird population. Science 297, 1168-1170 (2002). (Pubitemid 36193349)
76. Doligez, B., Cadet, C., Danchin, É. & Boulinier, T. When to use public information for breeding habitat selection? The role of environmental predictability and density dependence. Anim. Behav. 66, 973-988 (2003). (Pubitemid 37457993)
77. Parejo, D., White, J. F., Clobert, J., Dreiss, A. N. & Danchin, É. Blue tits use fledging quantity and quality as public information in breeding habitat choice. Ecology 88, 2373-2382 (2007). (Pubitemid 351345145)
78. Dugatkin, L. A. Interface between culturally based preferences and genetic preferences: female mate choice in Poecilia reticulata. Proc. Natl Acad. Sci. USA 93, 2770-2773 (1996). (Pubitemid 26114322)
79. Pöysä, H. Public information and conspecific nest parasitism in goldeneyes: targeting safe nests by parasites. Behav. Ecol. 17, 459-465 (2006).
80. Parejo, D. & Avilés, J. M. Do avian brood parasites eavesdrop on heterospecific sexual signals revealing host quality? A review of the evidence. Anim. Cogn. 10, 81-88 (2007). (Pubitemid 46465354)
81. Coolen, I., Dangles, O. & Casas, J. Social learning in noncolonial insects? Curr. Biol. 15, 1931-1935 (2005). (Pubitemid 41566140)
82. Mery, F. et al. Public versus personal information for mate copying in an invertebrate. Curr. Biol. 19, 730-734 (2009).
83. Danchin, É., Blanchet, S., Mery, F. & Wagner, R. H. Do invertebrates have culture? Commun. Integr. Biol. 3, 303-305 (2010).
84. Halloy, J. et al. Social integration of robots into groups of cockroaches to control self-organized choices. Science 318, 1155-1158 (2007). (Pubitemid 350134901)
85. White, D. J. & Galef, B. G. 'Culture' in quail: social influences on mate choices of female Coturnix coturnix. Anim. Behav. 59, 975-979 (2000). (Pubitemid 30656572)
86. Fitch, W. T. Birdsong normalized by culture. Nature 459, 519-520 (2009).
87. Boyd, R. & Richerson, P. J. Why is culture adaptive? Q. Rev. Biol. 58, 209-214 (1983).
88. Feldman, M. W. & Cavalli-Sforza, L. L. Cultural and biological evolutionary processes: gene-culture disequilibrium. Proc. Natl Acad. Sci. USA 81, 1604-1607 (1984). (Pubitemid 14174552)
89. Hochberg, M. E., Sinervo, B. & Brown, S. P. Socially mediated speciation. Evolution 57, 154-158 (2003). (Pubitemid 36234335)
90. Henrich, J. & McElreath, R. The evolution of cultural evolution. Evol. Anthropol. 12, 123-135 (2003).
91. Jansen, V. A. A. & Van Baalen, M. Altruism through beard chromodynamics. Nature 440, 663-666 (2006).
92. Grant, P. R. & Grant, B. R. The secondary contact phase of allopatric speciation in Darwin's finches. Proc. Natl Acad. Sci. USA 106, 20141-20148 (2009).
93. Haesler, M. P. & Seehausen, O. Inheritance of female mating preference in a sympatric sibling species pair of Lake Victoria cichlids: implications for speciation. Proc. R. Soc. Lond. B 272, 237-245 (2005). (Pubitemid 40731830)
94. Verzijden, M. N. & ten Cate, C. Early learning influences species assortative mating preferences in Lake Victoria cichlid fish. Biol. Lett. 3, 134-136 (2007). (Pubitemid 351878146)
95. Hochberg, M. E. A theory of modern cultural shifts and meltdowns. Biol. Lett. 271, S313-S316 (2004). (Pubitemid 38998735)
96. Henrich, J. & Boyd, R. The evolution of conformist transmission and the emergence of between-group differences. Evol. Hum. Behav. 19, 215-241 (1998). (Pubitemid 128339988)
97. Dindo, M., Whiten, A. & de Waal, F. B. M. In-group conformity sustains different foraging traditions in capuchin monkeys (Cebus apella). PLoS ONE 4, 1-7 (2009).
98. Franz, M. & Nunn, C. L. Rapid evolution of social learning. J. Evol. Biol. 22, 1914-1922 (2009).
99. Laland, K. N., Odling-Smee, J. & Myles, S. How culture shaped the human genome: bringing genetics and the human sciences together. Nature Rev. Genet. 11, 137-148 (2010).
100. Henrich, J., Boyd, R. & Richerson, P. J. Five misunderstandings about cultural evolution. Hum. Nat. 19, 119-137 (2008).
101. Weaver, I. C. G. et al. Epigenetic programming by maternal behaviour. Nature Neurosci. 7, 847-854 (2004).
102. Gintis, H., Bowles, S., Boyd, R. & Fehr, E. Explaining altruistic behaviour in humans. Evol. Hum. Behav. 24, 153-172 (2003).
103. Henrich, J. Cultural group selection, co-evolutionary processes and large-scale cooperation. J. Econ. Behav. Organ. 53, 3-35 (2004). (Pubitemid 37544805)
104. Lehmann, L. & Feldman, M. W. The co-evolution of culturally inherited altruistic helping and cultural transmission under random group formation. Theor. Popul. Biol. 4, 506-516 (2008).
105. Lehmann, L., Feldman, M. W. & Foster, K. Cultural transmission can inhibit the evolution of altruistic helping. Am. Nat. 172, 12-24 (2008). (Pubitemid 351920308)
106. Boyd, R. & Richerson, P. J. Culture and the evolution of human cooperation. Phil. Trans. R. Soc. B 364, 3281-3288 (2009).
107. Kendal, R. L., Coolen, I. & Laland, K. N. The role of conformity in foraging when personal and social information conflict. Behav. Ecol. 15, 269-277 (2004). (Pubitemid 38492729)
108. Ehrlich, P. R. & Levin, S. A. The evolution of norm. PLoS Biol. 3, 943-948 (2005).
109. Frere, C. H. et al. Social and genetic interactions drive fitness variation in a free-living dolphin population. Proc. Natl Acad. Sci. USA 107, 19949-19954 (2010).
110. Bentley, R. A., Hahn, M. W. & Shennan, S. J. Random drift and culture change. Proc. R. Soc. Lond. B 271, S353-S356 (2004).
111. Herzog, H. A., Bentley, R. A. & Hahn, M. W. Random drift and large shifts in popularity of dog breeds. Proc. R. Soc. Lond. B 271, S353-S356 (2004). (Pubitemid 38998746)
112. Pujol, B. & Pannell, J. R. Reduced responses to selection after species range expansion. Science 321, 96 (2008). (Pubitemid 351956238)
113. Knott, S. A., Sibly, R. M., Smith, R. H. & Moller, H. Maximum-likelihood-estimation of genetic-parameters in life-history studies using the animal-model. Funct. Ecol. 9, 122-126 (1995).
114. Mesoudi, A., Whiten, A. & Laland, K. N. Towards a unified science of cultural evolution. Behav. Brain Sci. 29, 329-383 (2006).
115. Lynch, A. & Baker, A. J. A population memetics approach to cultural-evolution in chaffinch song - meme diversity within populations. Am. Nat. 141, 597-620 (1993).
116. Lycett, S. J., Collard, M. & McGrew, W. C. Phylogenetic analyses of behaviour support existence of culture among wild chimpanzees. Proc. Natl Acad. Sci. USA 104, 17588-17592 (2007). (Pubitemid 350210879)
117. Mesoudi, A. & Whiten, A. The multiple roles of cultural transmission experiments in understanding human cultural evolution. Phil. Trans. R. Soc. B 363, 3489-3501 (2008).
118. Kenward, B., Weir, A. A. S., Rutz, C. & Kacelnik, A. Tool manufacture by naive juvenile crows. Nature 433, 121 (2005).
119. Lynch, M. & Walsh, B. Genetics and Analysis of Quantitative Traits (Sinauer Associates, Sunderland, Massachusetts, 1998).
120. Charmantier, A. et al. Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320, 800-803 (2008). (Pubitemid 351929630)
121. Wilson, A. J. et al. An ecologist's guide to the animal model. J. Anim. Ecol. 79, 13-26 (2010).
122. Muller, G. B. Evo-devo: extending the evolutionary synthesis. Nature Rev. Genet. 8, 943-949 (2007). (Pubitemid 350129171)
123. Caroll, S. B. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134, 25-36 (2008).
124. Landry, C. R. Systems biology spins off a new model for the study of canalization. Trends Ecol. Evol. 24, 63-66 (2009).
125. Hoekstra, H. E. & Coyne, J. A. The locus of evolution: evo devo and the genetics of adaptation. Evolution 61, 995-1016 (2007). (Pubitemid 46699436)
126. Goldenfeld, N. & Woese, C. Biology's next revolution. Nature 445, 369-369 (2007).
127. Wilson, D. S. in Evolution: The Extended Synthesis (eds Pigliucci, M. & Müller, G. B.) 81-93 (MIT Press, Cambridge, Massachusetts, 2010).
128. Feldman, M. W. & Cavalli-Sforza, L. L. in Mathematical Evolutionary Theory (ed. Feldman, M. W.) 145-173 (Princeton Univ. Press, Princeton, New Jersey, 1989).
129. Mesoudi, A. & Laland, K. N. Culturally transmitted paternity beliefs and the evolution of human mating behaviour. Proc. R. Soc. B 274, 1273-1278 (2007). (Pubitemid 47056700)
130. Jablonka, E. & Lamb, M. J. The evolution of information in the major transitions. J. Theor. Biol. 239, 236-246 (2006).
131. Szathmàry, E. & Maynard Smith, J. The major evolutionary transitions. Nature 374, 227-232 (1995).
132. Maynard Smith, J. & Szathmáry, E. The Major Transitions in Evolution (Freeman, Oxford, 1995).
133. Newman, S. A. & Bhat, R. Dynamical patterning modules: a "pattern language" for development and evolution of multicellular form. Int. J. Dev. Biol. 53, 693-705 (2009).
134. Urushihara, H. The cellular slime mold: eukaryotic model microorganism. Exp. Anim. 58, 97-104 (2009).
135. West, S. A., Griffin, A. S., Gardner, A. & Diggle, S. P. Social evolution theory for microorganisms. Nature Rev. Microbiol. 4, 597-607 (2006). (Pubitemid 44317022)
136. Zavilgelsky, G. B. & Manukhov, I. V. Quorum sensing, or how bacteria 'talk' to each other. Mol. Biol. 35, 224-232 (2001).
137. Richerson, P. J. & Boyd, R. Not By Genes Alone (Univ. Chicago Press, Chicago, Illinois, 2005).
138. Holden, C. J. & Mace, R. Phylogenetic analysis of the evolution of lactose digestion in adults. Hum. Biol. 69, 605-628 (1997).
139. Beja-Pereira, A. et al. Gene-culture co-evolution between cattle milk protein genes and human lactase genes. Nature Genet. 35, 311-313 (2003). (Pubitemid 37486911)
140. Wilson, D. S. in The Innate Mind: Culture and Cognition (eds Carruthers, P., Laurence, S. & Stich, S.) 1-21 (Oxford Univ. Press, Oxford, 2007).
141. Chilton, G. & Lein, M. R. Long-term changes in songs and song dialect boundaries of puget sound white-crowned sparrows. Condor 98, 567-580 (1996). (Pubitemid 26351279)
142. Warren, P. S. Winter dialects in the bronzed cowbird and their relationship to breeding-season dialects. Anim. Behav. 65, 1169-1178 (2003). (Pubitemid 36914330)
143. MacDougall-Shackleton, E. A. & MacDougall- Shackleton, S. A. Cultural and genetic evolution in mountain white-crowned sparrows: song dialects are associated with population structure. Evolution 55, 2568-2575 (2001). (Pubitemid 34115686)
144. Chilton, G., Lein, M. R. & Baptista, L. F. Mate choice by female white-crowned sparrows in a mixed-dialect population. Behav. Ecol. Sociobiol. 27, 223-227 (1990).
145. Brenowitz, E. A. & Beecher, M. D. Song learning in birds: diversity and plasticity, opportunities and challenges. Trends Neurosci. 28, 127-132 (2005). (Pubitemid 40320757)
146. Beecher, M. D. & Brenowitz, E. A. Functional aspects of song learning in songbirds. Trends Ecol. Evol. 20, 143-149 (2005). (Pubitemid 40257095)
147. Whitehead, H. Cultural selection and genetic diversity in matrilineal whales. Science 282, 1708-1711 (1998). (Pubitemid 28549286)
148. Nicholls, J. A., Austin, J. J., Moritz, C. & Goldizen, A. W. Genetic population structure and call variation in a passerine bird, the satin bowerbird, Ptilonorhynchus violaceus. Evolution 60, 1279-1290 (2006). (Pubitemid 44804485)
149. Slabbekoorn, H. & Smith, T. B. Bird song, ecology and speciation. Phil. Trans. R. Soc. Lond. B 357, 493-503 (2002). (Pubitemid 34489861)
150. Boyd, R. & Richerson, P. J. in Social-Learning. Psychological and Biological Perspectives (eds Zentall, T. R. & Galef, B. G. J.) 29-48 (Lawrence Erlbaum Associates, Hillsdale (New Jersey), Hove and London, 1988).
151. Whiten, A., McGuigan, N., Marshall-Pescini, S. & Hopper, L. M. Emulation, imitation, over-imitation and the scope of culture for child and chimpanzee. Phil. Trans. R. Soc. B 364, 2417-2428 (2009).
152. Heyes, C. M. & Galef, B. G. J. Social Learning and Imitation: The Roots of Culture (Academic Press, New York, 1996).
153. Galef, B. G. & Giraldeau, L. A. Social influences on foraging in vertebrates: causal mechanisms and adaptive functions. Anim. Behav. 51, 3-15 (2001).
154. Whiten, A. & van Schaik, C. P. The evolution of animal 'cultures' and social intelligence. Phil. Trans. R. Soc. B 362, 603-620 (2007). (Pubitemid 47056829)
155. Lefebvre, L. The opening of milk bottles by birds - evidence for accelerating learning rates, but against the wave-of-advance model of cultural transmission. Behav. Processes 34, 43-53 (1995).
156. Avital, E. & Jablonka, E. Animal Traditions. Behavioural Inheritance in Evolution (Cambridge Univ. Press, Cambridge, 2000).
157. Hirata, S., Watanabe, K. & Kawai, M. in Primate Origins of Human Cognition and Behaviour (ed. Matsuzawa, T.) 487-508 (Springer Japan, Tokyo, 2001).
158. Brooks, R. The importance of mate copying and cultural inheritance of mating preferences. Trends Ecol. Evol. 13, 45-46 (1998).
159. Witte, K. & Noltemeier, B. The role of information in mate-choice copying in female sailfin mollies (Poecilia latipinna). Behav. Ecol. Sociobiol. 52, 194-202 (2002). (Pubitemid 36064228)
160. White, B. N. & Galef, B. G. Differences between the sexes in direction and duration of response to seeing a potential sex partner mate with another. Anim. Behav. 59, 1235-1240 (2000).
161. Godin, J.-G. J., Herdman, E. J. E. & Dugatkin, L. A. Social influences on female mate choice in the guppy, Poecilia reticulata: generalized and repeatable trait-copying behaviour. Anim. Behav. 69, 999-1005 (2005). (Pubitemid 40413329)
162. Frigaard, N. U., Martinez, A., Mincer, T. J. & DeLong, E. F. Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea. Nature 439, 847-850 (2006). (Pubitemid 43255702)