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Restricted gene flow and fine-scale population structuring in tool using New Caledonian crows

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Abstract

New Caledonian crows Corvus moneduloides are the most prolific avian tool users. It has been suggested that some aspects of their complex tool use behaviour are under the influence of cultural processes, involving the social transmission—and perhaps even progressive refinement—of tool designs. Using microsatellite and mt-haplotype profiling of crows from three distinct habitats (dry forest, farmland and beachside habitat), we show that New Caledonian crow populations can exhibit significant fine-scale genetic structuring. Our finding that some sites of <10 km apart were highly differentiated demonstrates considerable potential for genetic and/or cultural isolation of crow groups. Restricted movement of birds between local populations at such small spatial scales, especially across habitat boundaries, illustrates how specific tool designs could be preserved over time, and how tool technologies of different crow groups could diverge due to drift and local selection pressures. Young New Caledonian crows have an unusually long juvenile dependency period, during which they acquire complex tool-related foraging skills. We suggest that the resulting delayed natal dispersal drives population-divergence patterns in this species. Our work provides essential context for future studies that examine the genetic makeup of crow populations across larger geographic areas, including localities with suspected cultural differences in crow tool technologies.

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References

  • Bluff LA, Weir AAS, Rutz C, Wimpenny JH, Kacelnik A (2007) Tool-related cognition in New Caledonian crows. Comp Cogn Behav Rev 2:1–25

    Google Scholar 

  • Bluff LA, Kacelnik A, Rutz C (2010a) Vocal culture in New Caledonian crows Corvus moneduloides. Biol J Linn Soc 101:767–776

    Article  Google Scholar 

  • Bluff LA, Troscianko J, Weir AAS, Kacelnik A, Rutz C (2010b) Tool use by wild New Caledonian crows Corvus moneduloides at natural foraging sites. Proc R Soc B 277:1377–1385

    Article  PubMed  Google Scholar 

  • Boyd R, Richerson PJ (2005) The origin and evolution of cultures. Oxford University Press, Oxford

    Google Scholar 

  • Caldwell CA, Millen AE (2008) Studying cumulative cultural evolution in the laboratory. Phil Trans R Soc B 363:3529–3539

    Article  PubMed  Google Scholar 

  • Caldwell CA, Millen AE (2010) Human cumulative culture in the laboratory: effects of (micro) population size. Learn Behav 38:310–318

    Article  PubMed  Google Scholar 

  • Coulon A, Fitzpatrick JW, Bowman R, Smith BM, Makarewich A, Stenzler LM, Lovette IJ (2008) Congruent population structure inferred from dispersal behaviour and intensive genetic surveys of the threatened Florida scrub-jay (Aphelocoma coerulescens). Mol Ecol 17:1685–1701

    Article  PubMed  CAS  Google Scholar 

  • Earl DA (2011) Structure harvester v0.6.1. Available at http://taylor0.biology.ucla.edu/structureHarvester/

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620

    Article  PubMed  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  CAS  Google Scholar 

  • Fleischer RC, Boarman WI, Gonzalez EG, Godinez A, Omland KE, Young S, Helgen L, Syed G, Mcintosh CE (2007) As the raven flies: using genetic data to infer the history of invasive common raven (Corvus corax) populations in the Mojave Desert. Mol Ecol 17:464–474

    Article  PubMed  Google Scholar 

  • Goodnight KF, Queller DC (1999) Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol Ecol 8:1231–1234

    Article  Google Scholar 

  • Haas F, Pointer MA, Saino N, Brodin A, Mundy NI, Hansson B (2009) An analysis of population genetic differentiation and genotype-phenotype association across the hybrid zone of carrion and hooded crows using microsatellites and MC1R. Mol Ecol 18:294–305

    Article  PubMed  CAS  Google Scholar 

  • Hedrick PW (1999) Perspective: highly variable genetic loci and their interpretation in evolution and conservation. Evolution 53:313–318

    Article  Google Scholar 

  • Henrich J (2004) Demography and cultural evolution: how adaptive cultural processes can produce maladaptive losses. Am Antiquity 69:197–214

    Article  Google Scholar 

  • Holzhaider JC, Hunt GR, Gray RD (2010a) The development of pandanus tool manufacture in wild New Caledonian crows. Behaviour 147:553–586

    Article  Google Scholar 

  • Holzhaider JC, Hunt GR, Gray RD (2010b) Social learning in New Caledonian crows. Learn Behav 38:206–219

    Article  PubMed  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332

    Article  Google Scholar 

  • Hunt GR (1996) Manufacture and use of hook-tools by New Caledonian crows. Nature 379:249–251

    Article  CAS  Google Scholar 

  • Hunt GR, Gray RD (2003) Diversification and cumulative evolution in New Caledonian crow tool manufacture. Proc R Soc B 270:867–874

    Article  PubMed  Google Scholar 

  • Hunt GR, Gray RD (2006) Tool manufacture by New Caledonian crows: chipping away at human uniqueness. Act Zool Sinica 52(Suppl):622–625

    Google Scholar 

  • Hunt GR, Abdelkrim J, Anderson MG, Holzhaider JC, Marshall AJ, Gemmell NJ, Gray RD (2007) Innovative pandanus-tool folding by New Caledonian crows. Austr J Zool 55:291–298

    Article  Google Scholar 

  • Jakobbson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program with label switching and multimodality in analysis of population structure. Bioinformatics 3:1801–1806

    Article  Google Scholar 

  • Kaplan H, Hill K, Lancaster J, Magdalena Hurtado A (2000) A theory of human life history evolution: diet, intelligence, and longevity. Evol Anthropol 9:156–185

    Article  Google Scholar 

  • Kenward B, Rutz C, Weir AAS, Chappell J, Kacelnik A (2004) Morphology and sexual dimorphism of the New Caledonian crow Corvus moneduloides, with notes on its behaviour and ecology. Ibis 146:652–660

    Article  Google Scholar 

  • Kenward B, Weir AAS, Rutz C, Kacelnik A (2005) Tool manufacture by naive juvenile crows. Nature 433:121

    Article  PubMed  CAS  Google Scholar 

  • Kenward B, Rutz C, Weir AAS, Kacelnik A (2006) Development of tool use in New Caledonian crows: inherited action patterns and social influence. Anim Behav 72:1329–1343

    Article  Google Scholar 

  • Kenward B, Schlögl C, Rutz C, Weir AAS, Bugnyar T, Kacelnik A (2011) On the evolutionary and ontogenetic origins of tool-oriented behaviour in New Caledonian crows (Corvus moneduloides). Biol J Linn Soc 102:870–877

    Article  Google Scholar 

  • Laland KN (2008) Animal cultures. Curr Biol 18:R366–R370

    Article  PubMed  CAS  Google Scholar 

  • Laland KN, Hoppitt W (2003) Do animals have culture? Evol Anthropol 12:150–159

    Article  Google Scholar 

  • Laland KN, Janik VM (2006) The animal cultures debate. Trends Ecol Evol 21:542–547

    Article  PubMed  Google Scholar 

  • Laland KN, Galef BG (eds) (2009) The question of animal culture. Harvard University Press, Harvard

    Google Scholar 

  • Langergraber KE et al. (2011) Genetic and ‘cultural’ similarity in wild chimpanzees. Proc R Soc B 278:408–416

    Article  PubMed  Google Scholar 

  • Langergraber KE, Vigilant L (2011) Genetic differences cannot be excluded from generating behavioural differences among chimpanzee groups. Proc R Soc B 278:2094–2095

    Article  Google Scholar 

  • Li S-H, Huang Y-J, Brown JL (1997) Isolation of tetranucleotide microsatellites from the Mexican jay Aphelocoma ultramarina. Mol Ecol 6:499–501

    Article  PubMed  CAS  Google Scholar 

  • Lycett SJ, Collard M, McGrew WC (2007) Phylogenetic analyses of behavior support existence of culture among wild chimpanzees. Proc Natl Acad Sci USA 104:17588–17592

    Article  CAS  Google Scholar 

  • Lycett SJ, Collard M, McGrew WC (2011) Correlations between genetic and behavioural dissimilarities in wild chimpanzees (Pan troglodytes) do not undermine the case for culture. Proc R Soc B 278:2091–2093

    Article  PubMed  Google Scholar 

  • McDonald DB, Potts WK, Fitzpatrick JW, Woolfenden GE (1999) Contrasting genetic structures in sister species of North American scrub-jays. Proc R Soc B 266:1117–1125

    Article  Google Scholar 

  • Peterson AT (1993) Adaptive geographical variation in bill shape of scrub-jays (Aphelocoma coerulescens). Am Nat 142:508–527

    Article  Google Scholar 

  • Powell A, Shennan S, Thomas MG (2009) Late Pleistocene demography and the appearance of modern human behavior. Science 324:1298–1301

    Article  PubMed  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly PJ (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimation of genetic relatedness using allozyme data. Evolution 43:258–275

    Article  Google Scholar 

  • Richerson PJ, Boyd R (2006) Not by genes alone: how culture transformed human evolution. University of Chicago Press, Chicago

    Google Scholar 

  • Rutz C, Bluff LA, Weir AAS, Kacelnik A (2007) Video cameras on wild birds. Science 318:765

    Article  PubMed  CAS  Google Scholar 

  • Rutz C, Bluff LA, Reed N, Troscianko J, Newton J, Inger R, Kacelnik A, Bearhop S (2010) The ecological significance of tool use in New Caledonian crows. Science 329:1523–1526

    Article  PubMed  CAS  Google Scholar 

  • Rutz C, St Clair JJH (2012) The evolutionary origins and ecological context of tool use in New Caledonian crows. Behav Processes 89:153–165

    Article  PubMed  Google Scholar 

  • Schoenle LA, Townsend AK, Lovette IJ (2007) Isolation and characterization of microsatellite loci in a cooperatively breeding corvid, the American crow (Corvus brachyrhynchos). Mol Ecol Notes 7:46–48

    Article  CAS  Google Scholar 

  • Tarr CL, Fleischer RC (1998) Primers for polymorphic GT microsatellites isolated from the Mariana crow, Corvus kubaryi. Mol Ecol 7:253–255

    Article  PubMed  CAS  Google Scholar 

  • Tarr CL, Fleischer RC (1999) Population boundaries and genetic diversity in the endangered Mariana crow (Corvus kubaryi). Mol Ecol 8:941–949

    Article  PubMed  CAS  Google Scholar 

  • Troscianko J, Bluff LA, Rutz C (2008) Grass-stem tool use in New Caledonian crows Corvus moneduloides. Ardea 96:283–285

    Article  Google Scholar 

  • van Schaik CP, Acrenaz M, Borgen G, Galdikas B, Knott CD, Singleton I, Suziki A, Utami SS, Merrill M (2003) Orangutan cultures and the evolution of material culture. Science 299:102–105

    Article  PubMed  Google Scholar 

  • Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V, Sugiyama Y, Tutin CEG, Wrangham RW, Boesch C (1999) Cultures in chimpanzees. Nature 399:682–685

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

Special thanks to L.A. Bluff who set up the field project together with C.R. in 2005, and to A. Weir and A. Kacelnik for sharing its early stages. We are also grateful to L.A. Bluff, J. Troscianko, A. Bayern and several field volunteers for assistance with crow trapping over the years; C. Lambert, T. Mennesson, J.-Y. Lemenant, S. Blancher, J. Bourget, N. Barré, J.-P. Richard and J. Paimbou-Ayouma for support in New Caledonia; N. McInerney for help with lab work; and three anonymous referees for excellent comments on the manuscript. This research was funded through a BBSRC (Biotechnology and Biological Sciences Research Council) David Phillips Fellowship to C.R. (BB/G023913/1), with additional generous support in New Caledonia from the Province Sud, the Direction de l'Environnement (DENV) and SEM Mwe Ara (Gouaro-Déva). Research was carried out with permissions from the DENV and the Direction de Resources Naturelles (Province Sud, New Caledonia) and was approved by Oxford University's local ethical review committee.

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Correspondence to C. Rutz.

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Communicated by: Pamela Rasmussen

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Fig. S1

Changes in ∆K suggest that the sampled New Caledonian crow population is structured into three genetically distinct subpopulations (K = 3; cf. Fig. 2); for details, see main text (PDF 64.2 kb)

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Rutz, C., Ryder, T.B. & Fleischer, R.C. Restricted gene flow and fine-scale population structuring in tool using New Caledonian crows. Naturwissenschaften 99, 313–320 (2012). https://doi.org/10.1007/s00114-012-0904-6

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  • DOI: https://doi.org/10.1007/s00114-012-0904-6

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