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Commun Integr Biol. 2010 Jul-Aug; 3(4): 303–305.
PMCID: PMC2928304

Do invertebrates have culture?

Abstract

A recent paper in Current Biology1 showed for the first time that female invertebrates (Drosophila melanogaster) can perform mate choice copying. Here, we discuss how female mating preferences in this species may be transmitted culturally. If culture occurs in invertebrates, it may be a relatively ancient evolutionary process that may have contributed to the evolution of many different taxa. This would considerably broaden the taxonomic range of cultural processes and suggest the need to include cultural inheritance in all animals into the general theory of evolution.24

Key words: cultural evolution, animal culture, mate choice copying, evolutionary theory, behavior

From an evolutionary perspective, culture can be defined as the part of phenotypic variance that is inherited through social learning.2 When defined in this way, cultural variation becomes part of inclusive heritability2 and is thus open to evolution through natural selection in ways similar to genetic variation. In this context, cultural transmission may thus be viewed as an important process of evolution. The actual impact of culture, however, may be restricted by a limited prevalence across species with well developed cognitive abilities. Apart from humans, evidence of cultural variation has been reported in a restricted set of mammals, such as chimpanzees,58 orangutans,9 whales1012 and some songbirds.1317

However, the paucity of evidence for cultural variance may result from the lack of methods to identify it. We have recently proposed four testable criteria on which to rely to demonstrate that a trait is at least partially culturally inherited.2,4 The expression of the trait must first result from social learning, which is learning from others1822 (reviews in refs. 3 and 2325). This is the essence of culture. Second, variation in the social information possessed by individuals must be socially transmitted across generations or at least from older to younger individuals.7,2629 This criterion establishes that the inheritance of behavioral variation across generations results from social learning. Third, social learning must modify the phenotype of the learning individual for sufficient time to allow other individuals to observe and learn its behavior.3032 The idea is that if a social influence only persists for a short period of time, it may be too labile to be transmitted to younger individuals. We only transmit attitudes to which we stick. Fourth, individuals should generalize socially learned information using it in new contexts.1,31,33,34 This is because only general rules (such as preferences for large over small mates, or deciduous over coniferous forests), not specific situations, can be transmitted across generations.

In our recent paper in Current Biology,1 we studied the role of social learning in female mating preferences in an invertebrate, Drosophila melanogaster. Our results showed surprisingly that in an invertebrate, tactics of female mate choice fulfill three of the four criteria that demonstrate that a trait is transmitted culturally.

Our first two-choice experiment showed that social information can affect female preference for poor condition males. Females naturally tend to prefer good over poor condition males. However, that preference can be modified by manipulating the apparent mating success of the poor condition male. After having had the opportunity to witness a poor condition male mating with a model female, while a good condition male remained alone, 24 hours later virgin prospector females increase the proportion of time they spend near the poor condition male. Male mating success thus constitutes public information35 that can influence a young prospector female’s associative preference for a poor condition male. This social influence lasted for at least 24 hours, which comprises a substantial proportion of a fruit fly’s life.

Our second experiment used artificial phenotypic variation whereby males were dusted with green or pink powder to study the role of social information on male mating success. We first presented green and pink males to a prospector virgin female and found no significant preference for copulating with males of either color. We then, through a glass partition, showed a prospector female a green male with a virgin female. Because virgin females rapidly copulate with the first male they encounter, this treatment provided positive public information about green males. Then in the next hour we showed a pink male with a recently mated female. Because recently mated females systematically reject males, this provided negative public information about the pink male. These trials were repeated with males of reversed male colors. We repeated this sequence three times and then presented the prospector female with a dyad of new green and pink males and recorded the male with which she copulated. When, during the demonstration, the glass partition was opaque so that the prospector female could not see the demonstration, the prospector female was equally likely to copulate with the green or pink male. However, when the glass partition was transparent, we found that the prospector female copulated significantly more often with the type of male she had seen copulating than with the type she had seen being rejected by other females.

Altogether our experiments provide the first evidence that female invertebrate can perform mate copying. More surprisingly, they also show that female mating preferences are at least partly socially learned (Criterion 1 of culture), that this influence lasts for a significant portion of a female’s lifespan (Criterion 3), and that Drosophila females are able to extract general rules from the observation of specific situations (e.g., green are better than pink males; Criterion 4). Hence female sexual preference in Drosophila fulfills three of the four criteria of cultural transmission.

Further experiments are needed to demonstrate that this form of social learning fulfills the second criterion, i.e., that it can lead to the transmission of sexual preferences from older to younger individuals. If this were the case, it would mean that female mating preferences in this invertebrate are at least partly transmitted culturally. This seems surprising because Drosophila have a miniature brain and are not usually considered to possess cognitive abilities compatible with cultural transmission (reviewed in refs. 25 and 36). However, this may not be so surprising in view of the pervasive occurrence of social learning, social and sexual imprinting, imitation, copying and teaching3,4,8 (review in refs. 23, 24, 29 and 3739) in many different contexts and in taxa as varied as birds,31,4043 mammals,44 fish32,45,46 and insects.1,47 Even plants48 show characteristics akin to social learning. These results suggest that more species may possess the cognitive abilities necessary to transmit social information across generations.

In conclusion, evidence for culture in invertebrates should encourage further research to test the generality of our results. Subsequently, a study of Drosophila serrata found no evidence for social learning in a mate choice context.49 However, that study differed from ours in many important ways that potentially may have hampered the detection of social learning. For instance, in that study, attractor females were of another species (D. birchii “of similar age”). It may well be that prospector females detected that these females were not conspecifics and they thus may have not considered the demonstration as providing useful information about male attractiveness. We now need to test multiple species with reliable designs. We also need to determine whether the second criterion of transmission across generations is fulfilled in Drosophila melanogaster. In case of a positive result, as suggested by Ellouise Leadbeater, it would introduce “a mainstream model species to the study of how animals use social information”50 and how such cultural transmission may affect evolution in general. This would also suggest that cultural evolution may be a relatively ancient evolutionary process that may have contributed to the evolution of many different taxa. This would considerably broaden the taxonomic range of cultural processes, and beg for the inclusion of cultural inheritance into the general theory of evolution, and not only for human evolution.24

Acknowledgements

This work was supported by the French “Agence Nationale de la Recherche” (ANR-05-BLAN-0265, EVO-INF-ECOL) to E.D., by a postdoc grant from the French “Fondation Fyssen” to S.B. and by the Austrian Science Foundation (FWF) grants P17468 and P20401 to R.H.W.

Footnotes

References

1. Mery F, Varela SA, Danchin E, Blanchet S, Parejo D, Coolen I, et al. Public versus personal information for mate copying in an invertebrate. Curr Biol. 2009;19:730–734. [PubMed]
2. Danchin É, Wagner RH. “Inclusive Heritability”: combining genetic and nongenetic information to study animal culture. Oikos. 2010;119:210–218.
3. Danchin É, Giraldeau LA, Valone TJ, Wagner RH. Public information: from nosy neighbors to cultural evolution. Science. 2004;305:487–491. [PubMed]
4. Danchin É, Wagner RH. In: Behavioural Ecology. Danchin É, Giraldeau L-A, Cézilly F., editors. Oxford: Oxford University Press,; 2008. pp. 693–726.
5. Whiten A. The second inheritance system of chimpanzees and humans. Nature. 2006;437:52–55. [PubMed]
6. Lycett SJ, Collard M, McGrew WC. Phylogenetic analyses of behavior support existence of culture among wild chimpanzees. Proc Natl Acad Sci USA. 2007;104:17588–17592. [PubMed]
7. Whiten A, Mesoudi A. An experimental science of culture: Animal social diffusion experiments. Phil Transact Royal Soc London B Biol Sci. 2008;363:3477–34788. [PMC free article] [PubMed]
8. Whiten A, McGuigan N, Marshall-Pescini S, Hopper LM. Emulation, imitation, over-imitation and the scope of culture for child and chimpanzee. Phil Transact Royal Soc B Biol Sci. 2009;364:2417–2428. [PMC free article] [PubMed]
9. Vogel G. Orangutans, like chimps, heed the cultural call of the collective. Science. 2003;299:27–28. [PubMed]
10. Whitehead H, Rendell L. Movements, habitat use and feeding success of cultural clans of South Pacific sperm whales. J Anim Ecol. 2004;73:190–196.
11. Whitehead H. Cultural selection and genetic diversity in matrilineal whales. Science. 1998;282:1708–1711. [PubMed]
12. Rosenbaum HC, Weinrich MT, Stoleson SA, Gibbs JP, Baker CS, DeSalle R. The effect of differential reproductive success on population genetic structure: correlations of life history with matrilines in humpback whales of the gulf of Maine. J Hered. 2002;93:389–399. [PubMed]
13. Slabbekoorn H, Smith TB. Bird song, ecology and speciation. Phil Transact Royal Soc London B Biol Sci. 2002;357:493–503. [PMC free article] [PubMed]
14. Beecher MD, Brenowitz EA. Functional aspects of song learning in songbirds. Trends Ecol Evol. 2005;20:143–149. [PubMed]
15. Brenowitz EA, Beecher MD. Song learning in birds: diversity and plasticity, opportunities and challenges. Trends Neurosci. 2005;28:127–132. [PubMed]
16. Putland DA, Nicholls JA, Noad MJ, Goldizen AW. Imitating the neighbours: vocal dialect matching in a mimic-model system. Biol Lett. 2006;2:367–370. [PMC free article] [PubMed]
17. Fitch WT. Birdsong normalized by culture. Nature. 2009;459:519–520. [PubMed]
18. Boyd R, Richerson PJ. In: In Social-learning. Psychological and Biological Perspectives. Zentall TR, Galef BGJ, editors. Hillsdale, New Jersey, Hove and London: Lawrence Erlbaum Associates, Publishers,; 1988. pp. 29–48.
19. Henrich J, McElreath R. The wvolution of cultural evolution. Evol Anthropol. 2003;12:123–135.
20. Richerson PJ, Boyd R. Not by Genes Alone. Chicago: University of Chicago Press,; 2005.
21. Henrich J, Boyd R, Richerson PJ. Five misunderstandings about cultural evolution. Hum Nat. 2008;19:119–137. [PubMed]
22. McElreath R, Henrich J. In: Oxford Handbook of Evolutionary Psychology. Dunbar R, Barrett L, editors. Oxford: Oxford Univ Press,; 2009. pp. 571–585.
23. Heyes CM, Galef BGJ. Social learning and Imitation: the Roots of Culture. New York: Academic Press,; 1996.
24. Galef BG, Giraldeau LA. Social influences on foraging in vertebrates: causal mechanisms and adaptive functions. Anim Behav. 2001;51:3–15. [PubMed]
25. Leadbeater E, Chittka L. Social learning in insects—From miniature brains to consensus building. Curr Biol. 2007;17:703–713. [PubMed]
26. 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 Proc. 1995;34:43–53. [PubMed]
27. Avital E, Jablonka E. Animal Traditions. Behavioural Inheritance in Evolution. Cambridge: Cambridge University Press,; 2000. [PubMed]
28. Hirata S, Watanabe K, Kawai M. In: Primate Origins of Human Cognition and Behavior. Matsuzawa T, editor. Tokyo: Springer Verlag Japan,; 2001. pp. 487–508.
29. Horner V, Whiten A, Flynn E, de Waal FBM. Faithful replication of foraging techniques along cultural transmission chains by chimpanzees and children. Proc Natl Acad Sci USA. 2006;103:13878–13883. [PubMed]
30. Brooks R. The importance of mate copying and cultural inheritance of mating preferences. Trends Ecol Evol. 1998;13:45–46. [PubMed]
31. White DJ, Galef BG. ‘Culture’ in quail: social influences on mate choices of female Coturnix coturnix. Anim Behav. 2000;59:975–979. [PubMed]
32. Witte K, Noltemeier B. The role of information in mate-choice copying in female sailfin mollies (Poecilia latipinna) Behav Ecol Sociobiol. 2002;52:194–202.
33. White BN, Galef BG. Differences between the sexes in direction and duration of response to seeing a potential sex partner mate with another. Anim Behav. 2000;59:1235–1240. [PubMed]
34. Godin J-GJ, Herdman EJE, Dugatkin LA. Social influences on female mate choice in the guppy, Poecilia reticulata: generalized and repeatable trait-copying behaviour. Anim Behav. 2005;69:999–1005.
35. Wagner RH, Danchin É. A taxonomy of biological information. Oikos. 2010;119:203–209.
36. Chittka L, Niven J. Are bigger brians better? Curr Biol. 2010;19:R995–R1000. [PubMed]
37. Franks NR, Richardson T. Teaching in tandem-running ants. Nature. 2006;439:153. [PubMed]
38. Thornton A, McAuliffe K. Teaching in wild Meerkats. Science. 2006;313:227–229. [PubMed]
39. Boesch C. Teaching among wild chimpanzees. Anim Behav. 1991;41:530–532.
40. Galef BGJ, White DJ. Evidence of social effects on mate choice in vertebrates. Behav Process. 2000;51:167–175. [PubMed]
41. Galef BGJ, Whikin EE. Interaction of social and individual learning in food preferences of Norway rats. Anim Behav. 2001;62:41–46.
42. Ophir AG, Galef BGJ. Female Japanese quail affiliate with live males that they have seen mate on video. Anim Behav. 2003;66:369–375.
43. Galef BG, Lim TCW, Gilbert GS. Evidence of mate choice copying in Norway rats, Rattus norvegicus. Anim Behav. 2008;75:1117–1123.
44. Deutsch JC, Nefdt RJC. Olfactory cues influence female choice in two lek-breeding antelopes. Nature. 1992;356:596–598. [PubMed]
45. van Bergen Y, Coolen I, Laland KN. Nine-spined sticklebacks exploit the most reliable source when public and private information conflict. Proc Royal Soc London B. 2003;271:957–962. [PMC free article] [PubMed]
46. Coolen I, Ward AJW, Hart PJB, Laland KN. Foraging nine-spined sticklebacks prefer to rely on public information over simpler social cues. Behav Ecol. 2005;16:865–870.
47. Coolen I, Dangles O, Casas J. Social learning in noncolonial insects? Curr Biol. 2005;15:1931–1935. [PubMed]
48. Karban R, Maron J. The fitness consequences of interspecific eavesdropping between plants. Ecology. 2000;83:1209–1213.
49. Auld HL, Punzalan D, Godin J-GJ, Rundle HD. Do female fruit flies (Drosophila serrata) copy the mate choice of others? Behav Proc. 2009;82:78–80. [PubMed]
50. Leadbeater E. Social learning: what do Drosophila have to offer? Curr Biol. 2009;19:378–380. [PubMed]

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