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Applying Quantitative Genetic Methods to Primate Social Behavior

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Abstract

Increasingly, behavioral ecologists have applied quantitative genetic methods to investigate the evolution of behaviors in wild animal populations. The promise of quantitative genetics in unmanaged populations opens the door for simultaneous analysis of inheritance, phenotypic plasticity, and patterns of selection on behavioral phenotypes all within the same study. In this article, we describe how quantitative genetic techniques provide studies of the evolution of behavior with information that is unique and valuable. We outline technical obstacles for applying quantitative genetic techniques that are of particular relevance to studies of behavior in primates, especially those living in noncaptive populations, e.g., the need for pedigree information, non-Gaussian phenotypes, and demonstrate how many of these barriers are now surmountable. We illustrate this by applying recent quantitative genetic methods to spatial proximity data, a simple and widely collected primate social behavior, from adult rhesus macaques on Cayo Santiago. Our analysis shows that proximity measures are consistent across repeated measurements on individuals (repeatable) and that kin have similar mean measurements (heritable). Quantitative genetics may hold lessons of considerable importance for studies of primate behavior, even those without a specific genetic focus.

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References

  • Adams, M. J. (2011). Evolutionary genetics of personality in nonhuman primates. In M. Inoue-Murayama, S. Kawamura, & A. Weiss (Eds.), From genes to animal behavior (pp. 137–164). New York: Springer.

    Chapter  Google Scholar 

  • Adams, M. J., King, J. E., & Weiss, A. (2012). The majority of genetic variation in orangutan personality and subjective well-being is nonadditive. Behavior Genetics, 42, 675–686.

    Article  PubMed  Google Scholar 

  • Arnold, S. J. (1994). Multivariate inheritance and evolution: A review of concepts. In C. R. B. Boake (Ed.), Quantitative genetic studies of behavioral evolution (pp. 17–48). Chicago: University of Chicago Press.

    Google Scholar 

  • Bell, A. M., Hankison, S. J., & Laskowski, K. L. (2009). The repeatability of behaviour: A meta-analysis. Animal Behaviour, 77(4), 771–783.

    Article  Google Scholar 

  • Bennett, A. J., & Pierre, P. J. (2010). Nonhuman primate research contributions to understanding genetic and environmental influences on phenotypic outcomes across development. In K. E. Hood, C. T. Halpern, G. Greenberg, & R. M. Lerner (Eds.), Handbook of developmental science, behavior, and genetics (pp. 353–399). New York: Blackwell.

    Chapter  Google Scholar 

  • Blomquist, G. E. (2009a). Environmental and genetic causes of maturational differences among rhesus macaque matrilines. Behavioral Ecology and Sociobiology, 63(9), 1345–1352.

    Article  Google Scholar 

  • Blomquist, G. E. (2009b). Fitness-related patterns of genetic variation in rhesus macaques. Genetica, 135, 209–219.

    Article  PubMed  Google Scholar 

  • Boake, C. R. B. (1994). Quantitative genetic studies of behavioral evolution. Chicago: University of Chicago Press.

    Google Scholar 

  • Boake, C. R. B., Arnold, S. J., Breden, F., Meffert, L. M., Ritchie, M. G., Taylor, B. J., Wolf, J. B., & Moore, A. J. (2002). Genetic tools for studying adaptation and the evolution of behavior. American Naturalist, 160, S143–S159.

    Article  PubMed  Google Scholar 

  • Bolker, B. M., Brooks, M. E., Clark, C. J., Geange, S. W., Poulsen, J. R., Stevens, M. H. H., Simone, S., & White, J. (2009). Generalized linear mixed models: A practical guide for ecology and evolution. Trends in Ecology and Evolution, 24(3), 127–135.

    Article  PubMed  Google Scholar 

  • Bradley, B. J., & Lawler, R. R. (2011). Linking genotypes, phenotypes, and fitness in wild primate populations. Evolutionary Anthropology, 20(3), 104–119.

    Article  PubMed  Google Scholar 

  • Brent, L. J. N., Heilbronner, S. R., Horvath, J. E., Gonzalez-Martinez, J., Ruiz-Lambides, A., Robinson, A. G., Skene, J. H. P., & Platt, M. L. (2013a). Genetic origins of social networks in rhesus macaques. Scientific Reports, 3, 1042.

    Article  PubMed Central  PubMed  Google Scholar 

  • Brent, L. J. N., MacLarnon, A., Platt, M. L., & Semple, S. (2013b). Seasonal changes in the structure of rhesus macaque social networks. Behavioral Ecology and Sociobiology, 67, 349–359.

    Article  PubMed  Google Scholar 

  • Brommer, J. E. (2011). Whither P ST ? the approximation of Q ST by P ST in evolutionary and conservation biology. Journal of Evolutionary Biology, 24, 1160–1168.

    Article  CAS  PubMed  Google Scholar 

  • Brommer, J. E., Kontiainen, P., & Pietiäinen, H. (2012). Selection on plasticity of seasonal life-history traits using random regression mixed model analysis. Ecology and Evolution, 2, 695–704.

    Article  PubMed  Google Scholar 

  • Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference: A practical information-theoretic approach (2nd ed.). New York: Springer.

    Google Scholar 

  • Campbell, C. J., Fuentes, A., MacKinnon, K. C., Bearder, S., & Stumpf, R. (Eds.). (2011). Primates in perspective. New York: Oxford University Press.

    Google Scholar 

  • Carrasco, J. L. (2010). A generalized concordance correlation coefficient based on the variance components generalized linear mixed models for overdispersed count data. Biometrics, 66, 897–904.

    Article  PubMed  Google Scholar 

  • Charmantier, A., & Garant, D. (2005). Environmental quality and evolutionary potential: Lessons from wild populations. Proceedings of the Royal Society of London B: Biological Sciences, 272, 1415–1425.

    Article  Google Scholar 

  • Cheverud, J. M., & Dittus, W. P. J. (1992). Primate population studies at Polonnaruwa II. Heritability of body measurements in a natural population of toque macaques. American Journal of Primatology, 27, 145–156.

    Article  Google Scholar 

  • Cheverud, J. M., & Moore, A. J. (1994). Quantitative genetics and the role of the environment provided by relatives in behavioral evolution. In C. R. B. Boake (Ed.), Quantitative genetic studies of behavioral evolution (pp. 67–100). Chicago: University of Chicago Press.

    Google Scholar 

  • Cheverud, J. M., & Wolf, J. B. (2009). The genetics and evolutionary consequences of maternal effects. In D. Maestripieri & J. M. Mateo (Eds.), Maternal effects in mammals (pp. 11–37). Chicago: University of Chicago Press.

    Chapter  Google Scholar 

  • Clutton-Brock, T., & Janson, C. (2012). Primate socioecology at the crossroads: Past, present, and future. Evolutionary Anthropology, 21, 136–150.

    Article  PubMed  Google Scholar 

  • Dingemanse, N. J., & Dochtermann, N. A. (2013). Quantifying individual variation in behaviour: Mixed-effect modelling approaches. Journal of Animal Ecology, 82, 39–54.

    Article  PubMed  Google Scholar 

  • Dingemanse, N. J., Kazem, A. J. N., Réale, D., & Wright, J. (2010). Behavioural reaction norms: Animal personality meets individual plasticity. Trends in Ecology and Evolution, 25, 81–89.

    Article  PubMed  Google Scholar 

  • Dingemanse, N. J., & Réale, D. (2005). Natural selection and animal personality. Behaviour, 142, 1165–1190.

    Article  Google Scholar 

  • Elston, D. A., Moss, R., Boulinier, T., Arrowsmith, C., & Lambin, X. (2001). Analysis of aggregation, a worked example: Numbers of ticks on red grouse chicks. Parasitology, 122, 563–569.

    Article  CAS  PubMed  Google Scholar 

  • Foulley, J. L., Gianola, D., & Im, S. (1987). Genetic evaluation of traits distributed as poisson-binomial with reference to reproductive characters. Theoretical and Applied Genetics, 73, 870–877.

    Article  CAS  PubMed  Google Scholar 

  • Fox, J. (2003). Effect displays in R for generalised linear models. Journal of Statistical Software, 8(15), 1–27.

    Google Scholar 

  • Fox, J. (2008). Applied regression analysis and generalized linear models (2nd ed.). Thousand Oaks, CA: SAGE.

    Google Scholar 

  • Fox, J., & Hong, J. (2009). Effect displays in R for multinomial and proportional-odds logit models: Extensions to the effects package. Journal of Statistical Software, 32(1), 1–24.Available at: http://www.jstatsoft.org/v32/i01/

  • Freckleton, R. P. (2009). The seven deadly sins of comparative analysis. Journal of Evolutionary Biology, 22(7), 1367–1375.

    Article  CAS  PubMed  Google Scholar 

  • Frentiu, F. D., Clegg, S. M., Chittock, J., Burke, T., Blows, M. W., & Owens, I. P. F. (2008). Pedigree-free animal models: The relatedness matrix reloaded. Proceedings of the Royal Society of London B: Biological Sciences, 275, 639–647.

    Article  Google Scholar 

  • Gelman, A., & Shirley, K. (2011). Inference from simulations and monitoring convergence. InS. Brooks, Gelman A, Jones GL, Meng X (eds) Handbook of Markov Chain Monte Carlo, CRC Press, London, chap 6, pp 163–174

  • Geyer, C. J. (2011). Introduction to Markov chain Monte Carlo. In S. Brooks, A. Gelman, G. L. Jones, & X. Meng (Eds.), Handbook of Markov Chain Monte Carlo (pp. 3–48). London: CRC Press.

    Google Scholar 

  • Grafen, A. (1984). Natural selection, kin selection and group selection. In J. R. Krebs & N. B. Davies (Eds.), Behavioural ecology: An evolutionary approach (2nd ed., pp. 62–84). New York: Blackwell.

    Google Scholar 

  • Hadfield, J. D. (2010). MCMC methods for multi-response generalized linear mixed models: The MCMCglmm R package. Journal of Statistical Software, 33(2), 1–22.

    Google Scholar 

  • Hadfield, J. D., & Nakagawa, S. (2010). General quantitative genetic methods for comparative biology: Phylogenies, taxonomies and multi-trait models for continuous and categorical characters. Journal of Evolutionary Biology, 23(3), 494–508.

    Article  CAS  PubMed  Google Scholar 

  • Hadfield, J. D., Nutall, A., Osorio, D., & Owens, I. P. (2007). Testing the phenotypic gambit: Phenotypic, genetic and environmental correlations of colour. Journal of Evolutionary Biology, 20, 549–557.

    Article  CAS  PubMed  Google Scholar 

  • Hilbe, J. M. (2011). Negative binomial regression (2nd ed.). New York: Cambridge University Press.

    Book  Google Scholar 

  • Housworth, E. A., Martins, E. P., & Lynch, M. (2004). The phylogenetic mixed model. American Naturalist, 163(1), 84–96.

    Article  PubMed  Google Scholar 

  • Jones, C. B. (2005). Behavioral flexibility in primates: Causes and consequences. New York: Springer.

    Book  Google Scholar 

  • Klingenberg, C. P. (1996). Multivariate allometry. In L. F. Marcus, M. Corti, A. Loy, G. J. P. Naylor, & D. E. Slice (Eds.), Advances in morphometrics (pp. 23–49). New York: Plenum Press.

    Chapter  Google Scholar 

  • Korsgaard, I. R., Andersen, A. H., & Jensen, J. (2002). Prediction error variance and expected response to selection, when selection is based on the best predictor—for Gaussian and threshold characters, traits following a Poisson mixed model and survival traits. Genetics, Selection, Evolution, 34, 307–333.

    Article  PubMed  Google Scholar 

  • Kruschke, J. (2011). Doing Bayesian data analysis: A tutorial introduction with R and BUGS. Burlington, MA: Academic Press.

    Google Scholar 

  • Kruuk, L. E. B. (2004). Estimating genetic parameters in natural populations using the ‘animal model. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 359(1446), 873–890.

    Article  PubMed  Google Scholar 

  • Kruuk, L. E. B., Slate, J., & Wilson, A. J. (2008). New answers for old questions: The evolutionary quantitative genetics of wild animal populations. Ecology, 39, 525–548.

    Google Scholar 

  • Lande, R. (1982). A quantitative genetic theory of life history evolution. Ecology, 63(3), 607–615.

    Article  Google Scholar 

  • Lawler, R. R. (2006). Sifaka positional behavior: Ontogenetic and quantitative genetic approaches. American Journal of Physical Anthropology, 131, 261–271.

    Article  PubMed  Google Scholar 

  • Leigh, S. R. (2001). Evolution of human growth. Evolutionary Anthropology, 10, 223–236.

    Article  Google Scholar 

  • Loeys, T., Moerkerke, B., De Smet, O., & Buysse, A. (2012). The analysis of zero-inflated count data: Beyond zero-inflated Poisson regression. British Journal of Mathematical and Statistical Psychology, 65, 163–180.

    Article  PubMed  Google Scholar 

  • Lynch, M., & Walsh, B. (1998). Genetics and analysis of quantitative traits. Sunderland, MA: Sinauer Associates.

    Google Scholar 

  • Maestripieri, D. (2009). Maternal influences on offspring growth, reproduction, and behavior in primates. In D. Maestripieri & J. M. Mateo (Eds.), Maternal effects in mammals (pp. 256–291). Chicago: University of Chicago Press.

    Chapter  Google Scholar 

  • Martin, J. G. A., Nussey, D. H., Wilson, A. J., & Réale, D. (2011). Measuring individual differences in reaction norms in field and experimental studies: A power analysis of random regression models. Methods in Ecology and Evolution, 2, 362–374.

    Article  Google Scholar 

  • McCulloch, C. E., & Searle, S. R. (2001). Generalized, linear, and mixed models. New York: John Wiley & Sons.

    Google Scholar 

  • Meyer, K. (2005). Random regression analyses using B-splines to model growth of Australian Angus cattle. Genetics, Selection, Evolution, 37, 473–500.

    Article  PubMed  Google Scholar 

  • Moore, A. J., Haynes, K. F., Preziosi, R. F., & Moore, P. J. (2002). The evolution of interacting phenotypes: Genetics and evolution of social dominance. American Naturalist, 160, S186–S197.

    Article  PubMed  Google Scholar 

  • Morrissey, M. B., & Wilson, A. J. (2010). pedantics: An r package for pedigree-based genetic simulation and pedigree manipulation, characterization and viewing. Molecular Ecology Resources, 10, 711–719.

    Article  PubMed  Google Scholar 

  • Nakagawa, S., & Schielzeth, H. (2010). Repeatability for Gaussian and non-Gaussian data: A practical guide for biologists. Biological Reviews of the Cambridge Philosophical Society, 85, 935–956.

    PubMed  Google Scholar 

  • Nee, S., Colegrave, N., West, S. A., & Grafen, A. (2005). The illusion of invariant quantities in life histories. Science, 309, 1236–1239.

    Article  CAS  PubMed  Google Scholar 

  • O’Hara, R. B., Cano, J. M., Ovaskainen, O., Teplitsky, C., & Ahlo, J. S. (2008). Bayesian approaches in evolutionary quantitative genetics. Journal of Evolutionary Biology, 21, 949–957.

    Article  PubMed  Google Scholar 

  • Olesen, I., Perez-Enciso, M., Gianola, D., & Thomas, D. L. (1994). A comparison of normal and nonnormal mixed models for number of lambs born in Norwegian sheep. Journal of Animal Science, 72, 1166–1173.

    CAS  PubMed  Google Scholar 

  • Pemberton, J. M. (2008). Wild pedigrees: The way forward. Proceedings of the Royal Society of London B: Biological Sciences, 275, 613–621.

    Article  CAS  Google Scholar 

  • Peters, R. H. (1991). A critique for ecology. New York: Cambridge University Press.

    Google Scholar 

  • Plomin, R., DeFries, J. C., McClearn, G. E., & McGuffin, P. (2009). Behavioral genetics (5th ed.). New York: Worth.

    Google Scholar 

  • Price, T., & Schluter, D. (1991). On the low heritability of life history traits. Evolution, 45, 853–861.

    Article  Google Scholar 

  • Quinn, J. L., Charmantier, A., Garant, D., & Sheldon, B. C. (2006). Data depth, data completeness, and their influence on quantitative genetic estimation in two contrasting bird populations. Journal of Evolutionary Biology, 19, 994–1002.

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team. (2012). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available at: http://www.R-project.org

  • Rawlins, R. G., & Kessler, M. J. (Eds.). (1986). The Cayo Santiago macaques: History, behavior, and biology. Albany: SUNY Press.

    Google Scholar 

  • Roff, D. A. (1994). Optimality modeling and quantitative genetics: A comparison of the two approaches. In C. R. B. Boake (Ed.), Quantitative genetic studies of behavioral evolution (pp. 49–66). Chicago: University of Chicago Press.

    Google Scholar 

  • Roff, D. A. (1997). Evolutionary quantitative genetics. New York: Chapman and Hall.

    Book  Google Scholar 

  • Schielzeth, H. (2010). Simple means to improve the interpretability of regression coefficients. Methods in Ecology and Evolution, 1, 103–113.

    Article  Google Scholar 

  • Schlichting, C. D., & Pigliucci, M. (1998). Phenotypic evolution: A reaction norm perspective. Sunderland, MA: Sinauer Associates.

    Google Scholar 

  • Silk, J. B. (1984). Measurement of the relative importance of individual selection and kin selection among females of the genus Macaca. Evolution, 38(3), 553–559.

    Article  Google Scholar 

  • Silk, J. B. (2002). Using the “f”-word in primatology. Behaviour, 139, 421–446.

    Article  Google Scholar 

  • Sillanpää, M. J. (2011). On statistical methods for estimating heritability in wild populations. Molecular Ecology, 20(7), 1324–1332.

    Article  PubMed  Google Scholar 

  • Sorensen, D., & Gianola, D. (2002). Likelihood, Bayesian, and MCMC methods in quantitative genetics. New York: Springer.

    Google Scholar 

  • Spencer, H. G. (2009). Effects of genomic imprinting on quantitative traits. Genetica, 136, 285–293.

    Article  PubMed  Google Scholar 

  • Spiegelhalter, D. J., Best, N. G., Carlin, B. P., & Van Der Linde, A. (2002). Bayesian measures of model complexity and fit. Journal of the Royal Statistical Society B: Statistical Methodology, 64, 583–639.

    Article  Google Scholar 

  • Stirling, D. G., Reale, D., & Roff, D. A. (2002). Selection, structure and the heritability of behaviour. Journal of Evolutionary Biology, 15, 277–289.

    Article  Google Scholar 

  • Tung, J., Alberts, S. C., & Wray, G. A. (2010). Evolutionary genetics in wild primates: Combining genetic approaches with field studies of natural populations. Trends in Genetics, 26, 353–362.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • van Oers, K., & Sinn, D. L. (2011). Toward a basis for the phenotypic gambit: Advances in the evolutionary genetics of animal personality. In M. Inoue-Murayama, S. Kawamura, & A. Weiss (Eds.), From genes to animal behavior (pp. 165–183). New York: Springer.

    Chapter  Google Scholar 

  • Visscher, P. M., Hill, W. G., & Wray, N. R. (2008). Heritability in the genomics era—concepts and misconceptions. Nature Reviews Genetics, 9, 255–266.

    Article  CAS  PubMed  Google Scholar 

  • Visscher, P. M., McEvoy, B., & Yang, J. (2010). From Galton to GWAS: Quantitative genetics of human height. Genetical Research, 92, 371–379.

    Article  Google Scholar 

  • Vitzthum, V. J. (2003). A number no greater than the sum of its parts: The use and abuse of heritability. Human Biology, 75, 539–558.

    Article  PubMed  Google Scholar 

  • Wainer, H. (1974). The suspended rootogram and other visual displays: An empirical validation. American Statistician, 28, 143–145.

    Google Scholar 

  • Weiss, A., King, J. E., & Enns, R. M. (2002). Subjective well-being is heritable and genetically correlated with dominance in chimpanzees (Pan troglodytes). Journal of Personality and Social Psychology, 83(5), 1141–1149.

    Article  PubMed  Google Scholar 

  • Williamson, D. E., Coleman, K., Bacanu, S., Devlin, B. J., Rogers, J., Ryan, N. D., & Cameron, J. L. (2003). Heritability of fearful-anxious endophenotypes in infant rhesus macaques: A preliminary report. Biological Psychiatry, 53, 284–291.

    Article  PubMed  Google Scholar 

  • Wilson, A. J. (2008). Why h 2 does not always equal V A /V P ? Journal of Evolutionary Biology, 21(3), 647–650.

    Article  CAS  PubMed  Google Scholar 

  • Wilson, A. J., Reale, D., Clements, M. N., Morrissey, M. M., Postma, E., Walling, C. A., Kruuk, L. E. B., & Nussey, D. H. (2010). An ecologist’s guide to the animal model. Journal of Animal Ecology, 79, 13–26.

    Article  PubMed  Google Scholar 

  • Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. A., & Smith, G. M. (2009). Mixed effects models and extensions in ecology with R. New York:Springer.

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Acknowledgments

We thank the Caribbean Primate Research Center (CPRC) for the permission to undertake research on Cayo Santiago, along with Bonn Aure and Jacqueline Buhl, who assisted in data collection, and Elizabeth Maldonado, Angelina Ruiz-Lambides, and Janis Gonzalez-Martinez, who provided access to the CPRC pedigree database. L. J. N. Brent also thanks Michael Platt for mentorship during the collection of these data. L. J. N. Brent was funded by fellowships awarded by the Duke Center for Interdisciplinary Decision Sciences. Additional funds were provided by NIMH grants no. R01-MH096875 and R01-MH089484. The CPRC is supported by a grant no. 8-P40 OD012217-25 from the National Center for Research Resources (NCRR) and the Office of Research Infrastructure Programs (ORIP) of the National Institutes of Health. G. E. Blomquist is supported by the University of Missouri Department of Anthropology and Research Council. G. E. Blomquist also thanks L. J. N. Brent and Noah Snyder-Mackler for the invitation to participate in the International Primatological Society symposium leading to this special issue.

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Blomquist, G.E., Brent, L.J.N. Applying Quantitative Genetic Methods to Primate Social Behavior. Int J Primatol 35, 108–128 (2014). https://doi.org/10.1007/s10764-013-9709-5

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