Biology & Philosophy

, Volume 29, Issue 6, pp 781–806 | Cite as

Homology across inheritance systems

  • Russell Powell
  • Nicholas Shea


Recent work on inheritance systems can be divided into inclusive conceptions, according to which genetic and non-genetic inheritance are both involved in the development and transmission of nearly all animal behavioral traits, and more demanding conceptions of what it takes for non-genetic resources involved in development to qualify as a distinct inheritance system. It might be thought that, if a more stringent conception is adopted, homologies could not subsist across two distinct inheritance systems. Indeed, it is commonly assumed that homology relations cannot survive a shift between genetic and cultural inheritance systems, and substantial reliance has been placed on that assumption in debates over the phylogenetic origins of hominin behavioral traits, such as male-initiated intergroup aggression. However, in the homology literature it is widely accepted that a trait can be homologous—that is, inherited continuously in two different lineages from a single common ancestor—despite divergence in the mechanisms involved in the trait’s development in the two lineages. In this paper, we argue that even on an extremely stringent understanding of what it takes for developmental resources to form a separate inheritance system, homologies can nonetheless subsist across shifts between distinct inheritance systems. We argue that this result is a merit of this way of characterizing what it is to be an inheritance system, that it has implications for adjudicating between alternative accounts of homology, and that it offers an important cautionary lesson about how (not) to reason with the homology concept, particularly in the context of cultural species.


Inheritance system Homology Genetic inheritance Cultural inheritance Genetic assimilation Genetic accommodation 



We would like to thank Gerd Müller, Grant Ramsey, Louise Roth, Tobias Uller, Günter Wagner, and two anonymous reviewers for helpful comments on an earlier draft of this manuscript. Russell Powell would like to thank the Konrad Lorenz Institute for Evolution and Cognition Research, as well as the Templeton Foundation Grant #43160, for support of this research.


  1. Adams D, Buchanan J (1990) The seville statement on violence. Am Psychol 45(10):1167–1168CrossRefGoogle Scholar
  2. Bertossa RC (2011) Morphology and behaviour: functional links in development and evolution. Philos Trans R Soc B 366:2056–2068CrossRefGoogle Scholar
  3. Bock K (1980) Human nature and history: A response to sociobiology. Columbia University Press, New YorkGoogle Scholar
  4. Boyd R, Borgerhoff-Mulder M, Durham WH, Richerson PJ (1997) Are cultural phylogenies possible? In: Weingart P, Mitchell SD, Richerson PJ, Maasen S (eds) Human by nature. Lawrence Erlbaum, Hillsdale, pp 355–386Google Scholar
  5. Brandon R (1990) Adaptation and environment. Princeton University Press, PrincetonGoogle Scholar
  6. Buchanan B, Collard M (2007) Investigating the peopling of North America through cladistic analyses of early paleoindian projectile points. J Anthropol Archaeol 26:366–393CrossRefGoogle Scholar
  7. Carmody RN, Wrangham RW (2009) The energetic significance of cooking. J Hum Evol 57:379–391CrossRefGoogle Scholar
  8. Currie AM (2013) Venomous dinosaurs and rear-fanged snakes: homology and homoplasy characterized. Erkenntnis. doi: 10.1007/s10670-013-9533-5
  9. de Visser JA et al (2003) Evolution and detection of genetic robustness. Evolution 57(9):1959–1972Google Scholar
  10. De Waal F (1997) Forward to Mitchell RW, Thompson NS, Miles H (eds.), Anthropomorphism, anecdotes, and animals, SUNY Press, pp. xiii–xivGoogle Scholar
  11. Deacon TW (2003) Multilevel selection in a complex adaptive system: the problem of language origins. In: Weber B, Depew D (eds) Evolution and learning: the Baldwin effect reconsidered. MIT Press, Cambridge, pp 81–106Google Scholar
  12. Ehrlich PR (2000) Human natures: genes, cultures, and the human prospect. Penguin, HarmondsworthGoogle Scholar
  13. Freeland SJ, Hurst LD (1998) The genetic code is one in a million. J Mol Evol 47:238–248CrossRefGoogle Scholar
  14. Gers M (2011) As we build our world we build our minds: the causal role of technology in the development and evolution of human psychological traits. Doctoral Thesis, Victoria University of WellingtonGoogle Scholar
  15. Godfrey-Smith P (2009) Darwinian populations and natural selection. Oxford University Press, New YorkGoogle Scholar
  16. Godfrey-Smith P (2013) Darwinism and cultural change. Philos Trans R Soc B 367(1599):2160–2170Google Scholar
  17. Gottlieb G, Lickliter R (2004) The various roles of animal models in understanding human development. Soc Dev 13(2):311–325CrossRefGoogle Scholar
  18. Gray RD, Drummond AJ, Greenhill SJ (2009) Language phylogenies reveal expansion pulses and pauses in Pacific settlement. Science 323:479–483CrossRefGoogle Scholar
  19. Griffiths PE (2001) Genetic information: a metaphor in search of a theory. Philos Sci 68(3):394–412CrossRefGoogle Scholar
  20. Hall BK (2003) Descent with modification: the unity underlying homology and homoplasy as seen through an analysis of development and evolution. Biol Rev 78:409–433CrossRefGoogle Scholar
  21. Hall BK (2013) ‘Homology, homoplasy, novelty, and behavior. Dev Psychobiol 55:4–12CrossRefGoogle Scholar
  22. Henrich J, Boyd R, Richerson PJ (2008) Five misunderstandings about cultural evolution. Hum Nat 19(2):119–137CrossRefGoogle Scholar
  23. Jablonka E, Lamb MJ (2005) Evolution in four dimensions: genetic, epigenetic, behavioral, and symbolic variation in the history of life. MIT Press, CambridgeGoogle Scholar
  24. Jordan FM (2011) A phylogenetic analysis of the evolution of Austronesian sibling terminologies. Hum Biol 83(2):297–321CrossRefGoogle Scholar
  25. Keeling PJ, Palmer JD (2008) Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9:605–618Google Scholar
  26. Kitcher P (1987) Précis of vaulting ambition: sociobiology and the quest for human nature. Behav Brain Sci 10:61–71CrossRefGoogle Scholar
  27. Laland KN (2008) Exploring gene–culture interactions: insights from handedness, sexual selection and niche-construction case studies. Phil Trans R Soc B 363:3577–3589CrossRefGoogle Scholar
  28. Laland KN, Brown G (2011) Sense and nonsense: evolutionary perspectives on human behaviour. Oxford University Press, OxfordGoogle Scholar
  29. Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290(5494):1151–1155CrossRefGoogle Scholar
  30. Mace R, Jordan FM (2011) Macro-evolutionary studies of cultural diversity: a review of empirical studies of cultural transmission and cultural adaptation. Proc R Soc Lond B Biol Sci 366:402–411CrossRefGoogle Scholar
  31. Machery E, Mallon R (2011) The evolution of morality. In: Doris JM (ed) Moral psychology handbook. Oxford University Press, Oxford, pp 3–46Google Scholar
  32. Maestripieri D, Roney JR (2006) Evolutionary developmental psychology: contributions from comparative research with nonhuman primates. Dev Rev 26:120–137CrossRefGoogle Scholar
  33. Manson JH, Wrangham RW (1991) Intergroup aggression in chimpanzees and humans. Curr Anthropol 32(4):369–390CrossRefGoogle Scholar
  34. Marks J (2002) What it means to be 98% chimpanzee: apes, people, and their genes. University of California Press, CaliforniaGoogle Scholar
  35. Müller G (2003) Homology: the evolution of morphological organization. In Gerd Müller and Stuart Newman (eds.), Origination of organismal form, MIT Press, pp. 51–70Google Scholar
  36. Oyama S (2000) The ontogeny of information: Developmental systems and evolution, Duke University PressGoogle Scholar
  37. Pagel M (2009) Human language as a culturally transmitted replicator. Nat Rev Genet 10:405–415Google Scholar
  38. Papineau D (2005) Social learning and the Baldwin effect. In: Zilhão A (ed) Evolution and rationality, and cognition. Routledge, London/New York, pp 40–60Google Scholar
  39. Pigliucci M (2010) Genotype–Phenotype mapping and the end of the ‘genes as blueprint’ metaphor. Phil Trans R Soc B 365:557–566CrossRefGoogle Scholar
  40. Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209:2362–2367CrossRefGoogle Scholar
  41. Powell R (2012) The future of human evolution. Br J Philos Sci 63:145–175CrossRefGoogle Scholar
  42. Prinz J (2008) Is morality innate? In Sinnott Armstrong W (ed) Moral psychology, MIT Press, Cambridge, vol 1, pp. 367-406Google Scholar
  43. Ramsey G, Peterson A (2012) Sameness in biology. Philos Sci 79(2):255–275CrossRefGoogle Scholar
  44. Rendall D, Di Fiore A (2007) Homoplasy, homology, and the perceived special status of behavior in evolution. J Hum Evol 52(5):504–521CrossRefGoogle Scholar
  45. Richerson P, Boyd R (2005) Not by genes alone: How culture transformed human evolution. University of Chicago Press, ChicagoGoogle Scholar
  46. Rieppel O (1992) Homology and logical fallacy. J Evol Biol 5:701–715CrossRefGoogle Scholar
  47. Robert JS (2004) Embryology, epigenesis and evolution. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  48. Rogers DS, Feldman MS, Ehrlich PR (2009) Inferring population histories using cultural data. Proc R Soc B 276:3835–3843CrossRefGoogle Scholar
  49. Roth VL (1988) The biological basis of homology. In: Humphries CJ (ed) Ontogeny and systematics. Columbia University Press, Columbia, pp 1–26Google Scholar
  50. Roth VL (1991) Homologies and hierarchies: problems solved and unresolved. Evol Biol 4:167–194CrossRefGoogle Scholar
  51. Roth VL (2001) Character replication. In: Wagner GP (ed) The character concept in evolutionary biology. Academic Press, London, pp 81–107CrossRefGoogle Scholar
  52. Shea N (2007) Representation in the genome and in other inheritance systems. Biol Philos 22:313–331CrossRefGoogle Scholar
  53. Shea N (2009) Imitation as an inheritance system. Phil Trans R Soc B 364:2429–2443Google Scholar
  54. Shea N (2013) Inherited representations are read in development. Br J Philos Sci 64(1):1–31. doi: 10.1093/bjps/axr050 Google Scholar
  55. Shea N, Pen I, Uller T (2011) Three epigenetic information channels and their different roles in evolution. J Evol Biol 24:1178–1187CrossRefGoogle Scholar
  56. Sperber D (1996) Explaining culture: a naturalistic approach. Blackwell, OxfordGoogle Scholar
  57. Sponsel LE (2010) Reflections on the possibilities of a nonkilling society and a nonkilling anthropology. In Pim JE (ed.), Nonkilling societies, creative commons, pp. 17–54Google Scholar
  58. Sussman RW (1999) The myth of man the hunter, man the killer and the evolution of human morality. Zygon 34(3):453–471CrossRefGoogle Scholar
  59. Tehrani J, Collard M (2002) Investigating cultural evolution through biological phylogenetic analyses of Turkmen textiles. J Anthropol Archaeol 21:443–463CrossRefGoogle Scholar
  60. Tishkoff et al (2006) Convergent adaptation of human lactase persistence in Africans and Europeans. Nat Genet 39:31–40CrossRefGoogle Scholar
  61. Van Valen LM (1982) Homology and Causes. J Morphol 173(3):305–312CrossRefGoogle Scholar
  62. Van Vugt M (2009) Sex differences in intergroup competition, aggression, and warfare: the male warrior hypothesis. Ann NY Acad Sci 1167:124–134CrossRefGoogle Scholar
  63. Waddington C (1953) Genetic assimilation of an acquired character. Evolution 4:118–126CrossRefGoogle Scholar
  64. Wagner GP (1989) The biological homology concept. Annual Rev Ecol Syst 20(1):51–69CrossRefGoogle Scholar
  65. Wagner GP (2007) The developmental genetics of homology. Nat Rev Genet 8:473–479CrossRefGoogle Scholar
  66. Wagner A (2008) Gene duplications, robustness, and evolutionary innovations. BioEssays 30:367–373CrossRefGoogle Scholar
  67. Weiss KM, Fullerton SM (2000) Phenogenetic drift and the evolution of genotype–phenotype relationships. Theor Popul Biol 57:187–195CrossRefGoogle Scholar
  68. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, OxfordGoogle Scholar
  69. Wiley EO, Lieberman BS (2011) Phylogenetics: theory and practice of phylogenetic systematics. Wiley-BlackwellGoogle Scholar
  70. Wilkins JF, Godfrey-Smith P (2009) Adaptationism and the adaptive landscape. Biol Philos 24:199–214CrossRefGoogle Scholar
  71. Wilson ML, Wrangham RW (2003) Intergroup relations in chimpanzees. Annu Rev Anthropol 32:363–392CrossRefGoogle Scholar
  72. Wrangham RW (1995) Ape culture and missing links, Symbols (2–9), Repr. In Sussman RW (1997) (ed.), The biological basis of human behavior, Simon and SchusterGoogle Scholar
  73. Wrangham RW (2010) Chimpanzee violence is a serious topic, Global Nonkilling Working Papers 1:29–50Google Scholar
  74. Wrangham RW, Peterson D (1996) Demonic males: apes and the origins of human violence. Houghton Mifflin Co, MAGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  1. 1.Department of PhilosophyBoston UniversityBostonUSA
  2. 2.Department of PhilosophyKing’s College LondonLondonUK
  3. 3.National Humanities Center, Research Triangle ParkDurhamUSA

Personalised recommendations