Behavior Genetics

, Volume 40, Issue 5, pp 706–714 | Cite as

Genes or Culture: Are Mitochondrial Genes Associated with Tool Use in Bottlenose Dolphins (Tursiops sp.)?

  • K. Bacher
  • S. Allen
  • A. K. Lindholm
  • L. Bejder
  • M. Krützen
ORIGINAL RESEARCH

Abstract

Some bottlenose dolphins use marine sponges as foraging tools (‘sponging’), which appears to be socially transmitted from mothers mainly to their female offspring. Yet, explanations alternative to social transmission have been proposed. Firstly, the propensity to engage in sponging might be due to differences in diving ability caused by variation of mitochondrial genes coding for proteins of the respiratory chain. Secondly, the cultural technique of sponging may have selected for changes in these same genes (or other autosomal ones) among its possessors. We tested whether sponging can be predicted by mitochondrial coding genes and whether these genes are under selection. In 29 spongers and 54 non-spongers from two study sites, the non-coding haplotype at the HVRI locus was a significant predictor of sponging, whereas the coding mitochondrial genes were not. There was no evidence of selection in the investigated genes. Our study shows that mitochondrial gene variation is unlikely to be a viable alternative to cultural transmission as a primary driver of tool use in dolphins.

Keywords

Social learning Gene culture co-evolution Bottlenose dolphins Tool use 

References

  1. Ackermann C (2008) Contrasting vertical skill transmission patterns of a tool use behaviour in two groups of wild bottlenose dolphins (Tursiops sp.), as revealed by molecular genetic analyses. MSc thesis, University of Zurich, SwitzerlandGoogle Scholar
  2. Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Second international symposium on information theory. Akademiai Kiado, Budapest, Hungary, pp 267–281Google Scholar
  3. Altmann J (1974) Observational study of behavior—sampling methods. Behaviour 49(3-4):227–267CrossRefPubMedGoogle Scholar
  4. Amos H, Hoelzel AR (1991) Long-term preservation of whale skin for DNA analysis. In: Hoelzel AR, Donovan GP (eds) Genetic ecology of whales and dolphins. International Whaling Commission, Cambridge, pp 99–103Google Scholar
  5. Andreu AL, Hanna MG, Reichmann H, Bruno C, Penn AS, Tanji K, Pallotti F, Iwata S, Bonilla E, Lach B, Morgan-Hughes J, DiMauro S (1999) Exercise intolerance due to mutations in the cytochrome b gene of mitochondrial DNA. N Engl J Med 341(14):1037–1044CrossRefPubMedGoogle Scholar
  6. Baker CS, Perry A, Bannister JL, Weinrich MT, Abernethy RB, Calambokidis J, Lien J, Lambertsen RH, Ramirez JU, Vasquez O, Clapham PJ, Alling A, Obrien SJ, Palumbi SR (1993) Abundant mitochondrial-DNA variation and worldwide population-structure in humpback whales. Proc Natl Acad Sci USA 90(17):8239–8243CrossRefPubMedGoogle Scholar
  7. Bard KA (1992) Intentional behavior and intentional communication in young free-ranging orangutans. Child Dev 63(5):1186–1197CrossRefPubMedGoogle Scholar
  8. Bauer GB, Johnson CM (1994) Trained motor imitation by bottle-nosed dolphins (Tursiops truncatus). Percept Mot Skills 79(3):1307–1315PubMedGoogle Scholar
  9. Boyd R, Richerson PJ (2005) The origin and evolution of cultures. Oxford University Press, New YorkGoogle Scholar
  10. Capaldi RA (1990) Structure and function of cytochrome-c-oxidase. Annu Rev Biochem 59:569–596CrossRefPubMedGoogle Scholar
  11. Castellini MA, Somero GN (1981) Buffering capacity of vertebrate muscle—correlations with potentials for anaerobic function. J Comp Physiol 143(2):191–198Google Scholar
  12. Connor RC (2001) Individual foraging specializations in marine mammals: culture and ecology. Behav Brain Sci 24(2):329–330CrossRefGoogle Scholar
  13. Connor RC, Smolker RS (1985) Habituated dolphins (Tursiops sp.) in Western Australia. J Mammal 66(2):398–400CrossRefGoogle Scholar
  14. Crawley MJ (2007) The R book. Wiley, Chichester, West Sussex, UKCrossRefGoogle Scholar
  15. De Waal FBM (2001) The ape and the sushi master. Basic Books, New YorkGoogle Scholar
  16. Dugatkin LA (2000) The imitation factor. Free Press, New YorkGoogle Scholar
  17. Feldman MW, Laland KN (1996) Gene-culture coevolutionary theory. Trends Ecol Evol 11(11):453–457CrossRefGoogle Scholar
  18. Ford JKB, Ellis GM, Barrett-Lennard LG, Morton AB, Palm RS, Balcomb KC (1998) Dietary specialization in two sympatric populations of killer whales (Orcinus orca) in coastal British Columbia and adjacent waters. Can J Zool 76(8):1456–1471CrossRefGoogle Scholar
  19. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133(3):693–709PubMedGoogle Scholar
  20. Galef BG (1992) The question of animal culture. Human Nature 3(2):157–178CrossRefGoogle Scholar
  21. Guinet C, Bouvier J (1995) Development of intentional stranding hunting techniques in killer whale (Orcinus orca) calves at Crozet Archipelago. Can J Zool 73(1):27–33CrossRefGoogle Scholar
  22. Heyes CM (1993) Imitation, culture and cognition. Anim Behav 46(5):999–1010CrossRefGoogle Scholar
  23. Howell N (1989) Evolutionary conservation of protein regions in the protonmotive cytochrome-b and their possible roles in redox catalysis. J Mol Evol 29(2):157–169CrossRefPubMedGoogle Scholar
  24. Howell N, Appel J, Cook JP, Howell B, Hauswirth WW (1987) The molecular-basis of inhibitor resistance in a mammalian mitochondrial cytochrome-b mutant. J Biol Chem 262(5):2411–2414PubMedGoogle Scholar
  25. Hurvich CM, Tsai CL (1989) Regression and time series models in small samples. Biometrika 76:297–307CrossRefGoogle Scholar
  26. Jaeggi AV, van Noordwijk MA, van Schaik CP (2008) Begging for information: mother-offspring food sharing among wild Bornean orangutans. Am J Primat 70(6):533–541CrossRefGoogle Scholar
  27. Janik VM (2000) Whistle matching in wild bottlenose dolphins (Tursiops truncatus). Science 289(5483):1355–1357CrossRefPubMedGoogle Scholar
  28. Kimura M (1985) The neutral theory of molecular evolution. Cambridge University Press, CambridgeGoogle Scholar
  29. Krakauer E, van Schaik CP (2005) Independent and social learning in the development of aye-aye tap-foraging skills. Am J Phys Anthropol 126(S40):132–133Google Scholar
  30. Kreicker S (2010) Culturally transmitted tool use in bottlenose dolphins (Tursiops sp.)—utilization of an unexploited niche? MSc thesis, University of Zurich, SwitzerlandGoogle Scholar
  31. Krützen M (2009) A cultured debate. Trends Ecol Evol 24:530–531CrossRefGoogle Scholar
  32. Krützen M, Barré LM, Möller LM, Heithaus MR, Simms C, Sherwin BW (2002) A biopsy system for small cetaceans: darting success and wound healing in Tursiops spp. Marine Mamm Sci 18(4):863–878CrossRefGoogle Scholar
  33. Krützen M, Barre LM, Connor RC, Mann J, Sherwin WB (2004a) ‘O father: where are thou?’-Paternity assessment in an open fission-fusion society of wild bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia. Mol Ecol 13(7):1975–1990CrossRefPubMedGoogle Scholar
  34. Krützen M, Sherwin WB, Berggren P, Gales NJ (2004b) Population structure in an inshore cetacean revealed by microsatellite and mtDNA analysis: bottlenose dolphins (Tursiops sp) in Shark Bay, Western Australia. Marine Mamm Sci 20(1):28–47CrossRefGoogle Scholar
  35. Krützen M, Mann J, Heithaus MR, Connor RC, Bejder L, Sherwin WB (2005) Cultural transmission of tool use in bottlenose dolphins. Proc Natl Acad Sci USA 102(25):8939–8943CrossRefPubMedGoogle Scholar
  36. Krützen M, van Schaik C, Whiten A (2007) The animal cultures debate: response to Laland and Janik. Trends Ecol Evol 22(1):6 (author reply 7)CrossRefPubMedGoogle Scholar
  37. Kuczaj SA, Gory JD, Xitco MJ (1998) Using programs to solve problems: imitation versus insight. Behav Brain Sci 21(5):695–696CrossRefGoogle Scholar
  38. Laland KN, Hoppitt W (2003) Do animals have culture? Evol Anthropol 12(3):150–159CrossRefGoogle Scholar
  39. Laland KN, Janik VM (2006) The animal cultures debate. Trends Ecol Evol 21(10):542–547CrossRefPubMedGoogle Scholar
  40. Laland KN, Odling-Smee J, Myles S (2010) How culture shaped the human genome: bringing genetics and the human sciences together. Nature Rev Genet 11(2):137–148CrossRefPubMedGoogle Scholar
  41. Mann J (1999) Behavioral sampling methods for cetaceans: a review and critique. Marine Mamm Sci` 15(1):102–122CrossRefGoogle Scholar
  42. Mann J, Sargeant BL (2003) Like mother, like calf; the ontogeny of foraging traditions in wild bottlenose dolphins (Tursiops sp.). In: Fragaszy DM, Perry S (eds) The biology of tradition; models and evidence. Cambridge University Press, Cambridge, pp 236–266CrossRefGoogle Scholar
  43. Mann J, Sargeant BL, Minor M (2007) Calf inspections of fish catches in bottlenose dolphins (Tursiops sp.): opportunities for oblique social learning? Marine Mamm Sci 23(1):197–202CrossRefGoogle Scholar
  44. Mann J, Sargeant BL, Watson-Capps JJ, Gibson QA, Heithaus MR, Connor RC, Patterson E (2008) Why do dolphins carry sponges? PLoS ONE 3(12):1–7CrossRefGoogle Scholar
  45. Michel H, Behr J, Harrenga A, Kannt A (1998) Cytochrome c oxidase: structure and spectroscopy. Annu Rev Biophys Biomol Struct 27:329–356CrossRefPubMedGoogle Scholar
  46. Nishida T (1973) Ant-gathering behaviour by use of tools among wild chimpanzees of Mahali Mountains. J Hum Evol 2(5):357–370CrossRefGoogle Scholar
  47. Noren SR, Williams TM (2000) Body size and skeletal muscle myoglobin of cetaceans: adaptations for maximizing dive duration. Comp Biochem Physiol 126(2):181–191CrossRefGoogle Scholar
  48. Palumbi SR, Martin A, Romano S, McMilian WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR. University of Hawaii, HonoluluGoogle Scholar
  49. Prusak B, Grzybowski T (2004) Non-random base composition in codons of mitochondrial cytochrome b gene in vertebrates. Acta Biochim Pol 51(4):897–905PubMedGoogle Scholar
  50. R Core Development Team (2009) In: Team RCD (ed): R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  51. Rendell L, Whitehead H (2001) Culture in whales and dolphins. Behav Brain Sci 24(2):309–324 discussion 324-382PubMedGoogle Scholar
  52. Roubertoux PL, Sluyter F, Carlier M, Marcet B, Maarouf-Veray F, Chérif C, Marican C, Arrechi P, Godin F, Jamon M, Verrier B, Cohen-Salmon C (2003) Mitochondrial DNA modifies cognition in interaction with the nuclear genome and age in mice. Nat Genet 35(1):65–69CrossRefPubMedGoogle Scholar
  53. Sargeant BL, Wirsing AJ, Heithaus MR, Mann J (2007) Can environmental heterogeneity explain individual foraging variation in wild bottlenose dolphins (Tursiops sp.)? Behav Ecol Sociobiol 61:679–688CrossRefGoogle Scholar
  54. Schneider S, Roessli D, Excoffier L (2000) Arlequin, ver.2.000: a software for population genetic data analysis. Genetics and Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  55. Smolker RA, Richards A, Connor RC, Mann J, Berggren P (1997) Sponge carrying by dolphins (Delphinidae, Tursiops sp): a foraging specialization involving tool use? Ethology 103(6):454–465CrossRefGoogle Scholar
  56. Southern SO, Southern PJ, Dizon AE (1988) Molecular characterization of a cloned dolphin mitochondrial genome. J Mol Evol 28(1–2):32–42CrossRefPubMedGoogle Scholar
  57. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–595PubMedGoogle Scholar
  58. Tomasello M (1993) It’s imitation, not mimesis. Behav Brain Sci 16(4):771–772CrossRefGoogle Scholar
  59. van Schaik CP, Ancrenaz M, Borgen G, Galdikas B, Knott CD, Singleton I, Suzuki A, Utami SS, Merrill M (2003) Orangutan cultures and the evolution of material culture. Science 299(5603):102–105CrossRefPubMedGoogle Scholar
  60. Weilgart L, Whitehead H (1997) Group-specific dialects and geographical variation in coda repertoire in South Pacific sperm whales. Behav Ecol Sociobiol 40(5):277–285CrossRefGoogle Scholar
  61. Whitehead H (1998) Cultural selection and genetic diversity in matrilineal whales. Science 282(5394):1708–1711CrossRefPubMedGoogle Scholar
  62. Whitehead H (2009) How might we study culture? A perspective from the ocean. In: Laland KN, Galef BG (eds) The question of animal culture. Harvard University Press, Cambridge, pp 125–151Google Scholar
  63. Whiten, van Schaik CP (2007) The evolution of animal ‘cultures’ and social intelligence. Philos Trans R Soc B-Biol Sci 362(1480):603–620CrossRefGoogle Scholar
  64. Whiten, Goodall J, McGrew WC, Nishida T, Reynolds V, Sugiyama Y, Tutin CE, Wrangham RW, Boesch C (1999) Cultures in chimpanzees. Nature 399(6737):682–685CrossRefPubMedGoogle Scholar
  65. Wursig B, Wursig M (1977) Photographic determination of group-size, composition, and stability of coastal porpoises (Tursiops truncatus). Science 198(4318):755–756CrossRefGoogle Scholar
  66. Yurk H (2003) Do killer whales have culture? In: de Waal FBM, Tyack PL (eds) Animal social complexity: intelligence, culture, and individualized societies. Harvard University Press, Cambridge, MA, pp 465–467Google Scholar
  67. Yurk H, Barrett-Lennard LG, Ford JKB, Matkin CO (2002) Cultural transmission within maternal lineages: vocal clans in resident killer whales in southern Alaska. Anim Behav 63:1103–1119CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • K. Bacher
    • 1
  • S. Allen
    • 2
  • A. K. Lindholm
    • 3
  • L. Bejder
    • 2
  • M. Krützen
    • 1
    • 2
  1. 1.Evolutionary Genetics Group, Anthropological Institute and MuseumUniversity of ZurichZurichSwitzerland
  2. 2.Murdoch University Cetacean Research Unit, Centre for Fish and Fisheries Research, School of Biological Sciences and BiotechnologyMurdoch UniversityMurdochAustralia
  3. 3.Animal Behavior Group, Institute for Evolutionary Biology and Environmental StudiesUniversity of ZurichZurichSwitzerland

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