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Can Genetic Differences Explain Vocal Dialect Variation in Sperm Whales, Physeter macrocephalus?

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Abstract

Sperm whale social groups can be assigned to vocal clans based on their production of codas, short stereotyped patterns of clicks. It is currently unclear whether genetic variation could account for these behavioural differences. We studied mitochondrial DNA (mtDNA) variation among sympatric vocal clans in the Pacific Ocean, using sequences extracted from sloughed skin samples. We sampled 194 individuals from 30 social groups belonging to one of three vocal clans. As in previous studies of sperm whales, mtDNA control region diversity was low (π = 0.003), with just 14 haplotypes present in our sample. Both hierarchical AMOVAs and partial Mantel tests showed that vocal clan was a more important factor in matrilineal population genetic structure than geography, even though our sampling spanned thousands of kilometres. The variance component attributed to vocal dialects (7.7%) was an order of magnitude higher than those previously reported in birds, while the variance component attributed to geographic area was negligible. Despite this, the two most common haplotypes were present in significant quantities in each clan, meaning that variation in the control region cannot account for behavioural variation between clans, and instead parallels the situation in humans where parent-offspring transmission of language variation has resulted in correlations with neutral genes. Our results also raise questions for the management of sperm whale populations, which has traditionally been based on dividing populations into geographic ‘stocks’, suggesting that culturally-defined vocal clans may be more appropriate management units.

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References

  • Amos W, Whitehead H, Ferrari MJ, Glockner-Ferrari DA, Payne R, Gordon J (1992) Restrictable DNA from sloughed cetacean skin; its potential for use in population analysis. Mar Mammal Sci 8:275–283

    Article  Google Scholar 

  • Arnbom T (1987) Individual identification of sperm whales. Rep Int Whal Commn 37:201–204

    Google Scholar 

  • Bacher K, Allen S, Lindholm A, Bejder L, Krützen M (2010) Genes or culture: are mitochondrial genes associated with tool use in bottlenose dolphins (Tursiops sp.). Behav Genet 40(5):706–714. doi:10.1007/s10519-010-9375-8

    Article  PubMed  Google Scholar 

  • Baker MC (1982) Vocal dialect recognition and population genetic consequences. Am Zool 22:561–569

    Google Scholar 

  • Baker MC, Cunningham MA (1985) The biology of bird-song dialects. Behav Brain Sci 8:85–133

    Article  Google Scholar 

  • Baker CS, Palumbi SR, Lambertsen RH, Weinrich MT, Calambokidis J, O’Brien SJ (1990) Influence of seasonal migration on geographic distribution of mitochondrial DNA haplotypes in humpback whales. Nature 344:238–240

    Article  PubMed  Google Scholar 

  • Barrett-Lennard L (2000) Population structure and mating patterns of killer whales (Orcinus orca) as revealed by DNA analysis. Ph.D., University of British Columbia, Canada

  • Boyd R, Richerson PJ (1985) Culture and the evolutionary process. University of Chicago Press, Chicago

    Google Scholar 

  • Catchpole CK, Slater PJB (1995) Bird song: biological themes and variations. Cambridge University Press, Cambridge

    Google Scholar 

  • Cavalli-Sforza LL (1997) Genes, peoples and languages. Proc Natl Acad Sci USA 94:7719–7724

    Article  PubMed  Google Scholar 

  • Chao A, Jost L, Chiang SC, Jiang YH, Chazdon RL (2008) A two-Stage probabilistic approach to multiple-community similarity indices. Biometrics 64(4):1178–1186. doi:10.1111/j.1541-0420.2008.01010.x

    Article  PubMed  Google Scholar 

  • Chepko-Sade DB, Halpin ZT (eds) (1987) Mammalian dispersal patterns: the effects of social structure on population genetics. University of Chicago Press, Chicago

    Google Scholar 

  • Christal J, Whitehead H, Lettevall E (1998) Sperm whale social units: variation and change. Can J Zool 76:1431–1440

    Article  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9(10):1657–1660. doi:10.1046/j.1365-294x.2000.01020

    Article  PubMed  Google Scholar 

  • Dillon MC (1996) Genetic structure of sperm whale populations assessed by mitochondrial DNA sequence variation. PhD Thesis, Dalhousie University, Halifax

  • Dillon MC, Wright JM (1993) Nucleotide sequence of the D-loop region of the sperm whale (Physeter macrocephalus) mitochondrial genome. Mol Biol Evol 10(2):296–305

    PubMed  Google Scholar 

  • Dillon MC, Richard KR, Whitehead H, Wright JM (2002) Social and population genetic structure of sperm whales assessed by molecular genetic analyses. In: Pfeiffer C (ed) Molecular and cell biology of marine mammals. Krieger, Malabar, pp 43–52

    Google Scholar 

  • Donovan GP (1991) A review of IWC stock boundaries. Rep Int Whal Comm 13:39–68

    Google Scholar 

  • Duchene S, Archer FI, Vilstrup J, Caballero S, Morin PA (2011) Mitogenome phylogenetics: the impact of using single regions and partitioning schemes on topology, substitution rate and divergence time estimation. PLoS One

  • Dufault S, Whitehead H, Dillion M (1999) An examination of the current knowledge on the stock structure of sperm whales (Physter macrocephalus) worldwide. J Cetacean Res Manage 1(1):1–10

    Google Scholar 

  • Engelhaupt D, Rus Hoelzel A, Nicholson C, Frantzis A, Mesnick S, Gero S, Whitehead H, Rendell L, Miller P, De Stefanis R, Cañadas A, Airoldi S, Mignucci-Giannoni AA (2009) Female philopatry in coastal basins and male dispersion across the North Atlantic in a highly mobile marine species, the sperm whale (Physeter macrocephalus). Mol Ecol 18(20):4193–4205. doi:10.1111/j.1365-294X.2009.04355.x

    Article  PubMed  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  Google Scholar 

  • Ford JKB (1991) Vocal traditions among resident killer whales (Orcinus orca) in coastal waters of British Columbia. Can J Zool 69:1454–1483

    Article  Google Scholar 

  • Ford MJ, Hanson MB, Hempelmann JA, Ayres KL, Emmons CK, Schorr GS, Baird RW, Balcomb KC, Wasser SK, Parsons KM, Balcomb-Bartok K (2011) Inferred paternity and male reproductive success in a killer whale (Orcinus orca) population. J Hered. doi:10.1093/jhered/esr067

  • Gerlach G, Jueterbock A, Kraemer P, Deppermann J, Harmand P (2010) Calculations of population differentiation based on GST and D: forget GST but not all of statistics! Mol Ecol 19(18):3845–3852. doi:10.1111/j.1365-294X.2010.04784.x

    Article  PubMed  Google Scholar 

  • Grant BR, Grant PR (1996) Cultural inheritance of song and its role in the evolution of Darwin’s finches. Evolution 50:2471–2487

    Article  Google Scholar 

  • Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28(4):1140–1162

    Article  Google Scholar 

  • Hoelzel AR, Natoli A, Dahlheim M, Olavarria C, Baird RW, Black N (2002) Low worldwide genetic diversity in the killer whale (Orcinus orca): implications for demographic history. Proc Roy Soc Lond B 269:1467–1473. doi:10.1098/rspb.2002.2033

    Article  Google Scholar 

  • Janik VM, Slater PJB (1997) Vocal learning in mammals. Adv Study Behav 26:59–99

    Article  Google Scholar 

  • Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17(18):4015–4026. doi:10.1111/j.1365-294X.2008.03887.x

    Article  PubMed  Google Scholar 

  • Knaus B, Cronn R, Liston A, Pilgrim K, Schwartz M (2011) Mitochondrial genome sequences illuminate maternal lineages of conservation concern in a rare carnivore. BMC Ecology 11(1):10

    Article  PubMed  Google Scholar 

  • Krützen M, Mann J, Heithaus MR, Connor RC, Bejder L, Sherwin WB (2005) Cultural transmission of tool use in bottlenose dolphins. PNAS 102(25):8939–8943. doi:10.1073/pnas.0500232102

    Article  PubMed  Google Scholar 

  • Lachlan RF, Slater PJB (1999) The maintenance of vocal learning by gene-culture interaction: the cultural trap hypothesis. Proc Roy Soc Lond B 266:701–706. doi:10.1098/rspb.1999.0692

    Article  Google Scholar 

  • Laland KN (1992) A theoretical investigation of the role of social transmission in evolution. Ethol Sociobiol 13:87–113

    Article  Google Scholar 

  • Laland KN, Janik VM (2006) The animal cultures debate. Trends Ecol Evol 21:542–547. doi:10.1016/j.tree.2006.06.005

    Article  PubMed  Google Scholar 

  • Langergraber KE, Boesch C, Inoue E, Inoue-Murayama M, Mitani JC, Nishida T, Pusey A, Reynolds V, Schubert G, Wrangham RW, Wroblewski E, Vigilant L (2010) Genetic and ‘cultural’ similarity in wild chimpanzees. Proc Roy Soc Lond B 278:408–416. doi:10.1098/rspb.2010.1112

    Article  Google Scholar 

  • Lougheed SC, Handford P, Baker AJ (1993) Mitochondrial DNA hyper diversity and vocal dialects in a subspecies transition of the rufous-collared sparrow. Condor 95:889–895

    Article  Google Scholar 

  • Lyrholm T, Gyllensten U (1998) Global matrilineal population structure in sperm whales as indicated by mitochondrial DNA sequences. Proc Roy Soc Lond B 265:1679–1684. doi:10.1098/rspb.1998.0488

    Article  Google Scholar 

  • Lyrholm T, Leimar O, Johanneson B, Gyllensten U (1999) Sex-biased dispersal in sperm whales: contrasting mitochondrial and nuclear genetic structure of global populations. Proc Roy Soc Lond B 266:347–354. doi:10.1098/rspb.1999.0644

    Article  Google Scholar 

  • MacDougall-Shackleton EA, MacDougall-Shackleton SA (2001) Cultural and genetic evolution in mountain white-crowned sparrows: song dialects are associated with population structure. Evolution 55(12):2568–2575. doi:10.1111/j.0014-3820.2001.tb00769.x

    PubMed  Google Scholar 

  • Marcoux M, Rendell L, Whitehead H (2007) Indications of fitness differences among vocal clans of sperm whales. Behav Ecol Sociobiol 61(7):1093–1098. doi:10.1007/s00265-006-0342-6

    Article  Google Scholar 

  • Mesnick SL (2001) Genetic relatedness in sperm whales: evidence and cultural implications. Behav Brain Sci 24(2):346–347

    Article  Google Scholar 

  • Mesnick SL, Taylor BL, Archer FI, Martien KK, Treviño SE, Hancock-Hanser BL, Medina SCM, Pease VL, Robertson KM, Straley JM, Baird RW, Calambokidis J, Schorr GS, Wade P, Burkanov V, Lunsford CR, Rendell L, Morin PA (2011) Sperm whale population structure in the eastern and central north pacific inferred by the use of single nucleotide polymorphisms (SNPs), microsatellites and mitochondrial DNA. Mol Ecol Res 11:278–298. doi:10.1111/j.1755-0998.2010.02973.x

    Article  Google Scholar 

  • Morin PA, Archer FI, Foote AD, Vilstrup J, Allen EE, Wade P, Durban J, Parsons K, Pitman R, Li L, Bouffard P, Abel Nielsen SC, Rasmussen M, Willerslev E, Gilbert MTP, Harkins T (2010) Complete mitochondrial genome phylogeographic analysis of killer whales (Orcinus orca) indicates multiple species. Genome Res 20(7):908–916. doi:10.1101/gr.102954.109

    Article  PubMed  Google Scholar 

  • Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9:373–375

    Article  PubMed  Google Scholar 

  • Palsbøll PJ, Clapham PJ, Matilla DK, Larsen F, Sears R, Siegismund HR, Sigurjønsson J, Vasquez O, Arctander P (1995) Distribution of mtDNA haplotypes in North Atlantic humpback whales: the influence of behaviour on population structure. Mar Ecol Prog Ser 116:1–10

    Article  Google Scholar 

  • Posada D (2009) Selection of models of DNA evolution with JModelTest. In: Posada D (ed) Bioinformatic analysis of DNA sequences. Humana Press, New York, pp 93–112

    Chapter  Google Scholar 

  • Raufaste N, Rousset F (2001) Are partial mantel tests adequate. Evolution 55(8):1703–1705. doi:10.1111/j.0014-3820.2001.tb00689.x

    PubMed  Google Scholar 

  • Rendell LE, Whitehead H (2001) Culture in whales and dolphins. Behav Brain Sci 24(2):309–382

    Article  PubMed  Google Scholar 

  • Rendell LE, Whitehead H (2003a) Vocal clans in sperm whales (Physeter macrocephalus). Proc Roy Soc Lond B 270:225–231. doi:10.1098/rspb.2002.2239

    Article  Google Scholar 

  • Rendell LE, Whitehead H (2003b) Comparing repertoires of sperm whales: a multiple methods approach. Bioacoustics 14(1):61–81

    Google Scholar 

  • Rendell L, Whitehead H, Coakes A (2005) Do breeding male sperm whales show preferences among vocal clans of females? Mar Mammal Sci 21(2):317–322. doi:10.1111/j.1748-7692.2005.tb01231.x

    Article  Google Scholar 

  • Ryan SJ (2006) Diversity: the role of culture in conservation planning for small or endangered populations. Conserv Biol 20(4):1321–1324. doi:10.1111/j.1523-1739.2006.00347.x

    Article  PubMed  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pair-wise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089

    PubMed  Google Scholar 

  • Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562

    PubMed  Google Scholar 

  • Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Zool 35:627–632

    Article  Google Scholar 

  • Soha JA, Nelson DA, Parker PP (2004) Genetic analysis of song dialect populations in Puget Sound white-crowned sparrows. Behav Ecol 15(4):636–646. doi:10.1093/beheco/arh055

    Article  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10(3):512–526

    PubMed  Google Scholar 

  • Tiedemann R, Milinkovitch MC (1999) Culture and genetic evolution in whales. Science 284:2055a

    Article  Google Scholar 

  • Watkins WA, Schevill WE (1977) Sperm whale codas. J Acoust Soc Am 62:1486–1490

    Article  Google Scholar 

  • Weilgart L, Whitehead H (1997) Group-specific dialects and geographical variation in coda repertoire in South Pacific sperm whales. Behav Ecol Sociobiol 40:277–285

    Article  Google Scholar 

  • Whitehead H (1998) Cultural selection and genetic diversity in matrilineal whales. Science 282:1708–1711. doi:10.1126/science.282.5394.1708

    Article  PubMed  Google Scholar 

  • Whitehead H (2003) Sperm whales: social evolution in the ocean. University of Chicago Press, Chicago

    Google Scholar 

  • Whitehead H (2005) Genetic diversity in the matrilineal whales: models of cultural hitchhiking and group-specific non-heritable demographic variation. Mar Mammal Sci 21:58–79. doi:10.1111/j.1748-7692.2005.tb01208.x

    Article  Google Scholar 

  • Whitehead H, Rendell L (2004) Movements, habitat use and feeding success of cultural clans of South Pacific sperm whales. J Anim Ecol 73(1):190–196. doi:10.1111/j.1365-2656.2004.00798.x

    Article  Google Scholar 

  • Whitehead H, Gordon J, Mathews EA, Richard KR (1990) Obtaining skin samples from living sperm whales. Mar Mammal Sci 6:316–326

    Article  Google Scholar 

  • Whitehead H, Dillon M, Dufault S, Weilgart L, Wright J (1998) Non-geographically based population structure of South Pacific sperm whales: dialects, fluke-markings and genetics. J Anim Ecol 67:253–262. doi:10.1046/j.1365-2656.1998.00187.x

    Article  Google Scholar 

  • Whitehead H, Rendell L, Osborne RW, Würsig B (2004) Culture and conservation of non-humans with reference to whales and dolphins: review and new directions. Biol Conserv 120:427–437. doi:10.1016/j.biocon.2004.03.017

    Article  Google Scholar 

  • Wright TF, Wilkinson GS (2001) Population genetic structure and vocal dialects in an amazon parrot. Proc Roy Soc Lond B 268:609–616. doi:10.1098/rspb.2000.1403

    Article  Google Scholar 

  • Yurk H, Barrett-Lennard L, Ford JKB, Matkin CO (2002) Cultural transmission within maternal lineages: Vocal clans in resident killer whales in southern Alaska. Anim Behav 63:1103–1119. doi:10.1006/anbe.2002.3012

    Article  Google Scholar 

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Acknowledgments

The National Geographic Society and the Natural Sciences and Engineering Research Council of Canada provided funding for fieldwork. L.R. was supported by a NERC Postdoctoral Fellowship and M.L.D. was supported by a Killam Memorial Postdoctoral Fellowship and a Vice-Chancellor’s Postdoctoral Fellowship (UNSW). Mary Dillon and Jenny Christal kindly shared the results of their genetic and photographic analyses respectively. Mike Ritchie, Jeff Graves, Kelly Stewart and Valentina Islas provided analytical advice and support. We thank Jeff Graves, Karen Martien, Kelly Stewart and two anonymous reviewers for comments that improved the manuscript.

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  1. Merel L. Dalebout

    Present address: School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW, 2052, Australia

Authors and Affiliations

  1. Centre for Social Learning and Cognitive Evolution, School of Biology, University of St Andrews, St Andrews, Fife, KY16 8LB, UK

    Luke Rendell

  2. Southwest Fisheries Science Center, National Marine Fisheries Service, NOAA, 8604 La Jolla Shores Drive, La Jolla, CA, 92037-1508, USA

    Sarah L. Mesnick & Jessica Burtenshaw

  3. Center for Marine Biodiversity and Conservation, Scripps Institution of Oceanography University of California, San Diego, La Jolla, CA, 92093-0202, USA

    Sarah L. Mesnick & Jessica Burtenshaw

  4. Department of Biology, Dalhousie University, Halifax, NS, B3H 4J1, Canada

    Merel L. Dalebout & Hal Whitehead

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Correspondence to Luke Rendell.

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Rendell, L., Mesnick, S.L., Dalebout, M.L. et al. Can Genetic Differences Explain Vocal Dialect Variation in Sperm Whales, Physeter macrocephalus?. Behav Genet 42, 332–343 (2012). https://doi.org/10.1007/s10519-011-9513-y

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