Abstract
The analysis of phenotypic covariances among genetically related individuals is the basis for estimations of genetic and phenotypic effects on phenotypes. Beyond heritability, there are several other estimates that can be made with behavior genetic models of interest to primatologists. Some of these estimates are feasible with primate samples because they take advantage of the types of relatives available to compare in primate species and because most behaviors are expressed orders of magnitude more often and in a greater variety of contexts than morphological or life-history traits. The hypotheses that can be tested with these estimates are contrasted with hypotheses that will be difficult to achieve in primates because of sample size limitations. Feasible comparisons include the proportion of variance from interaction effects, the variation of genetic effects across environments, and the genetics of growth and development. Simulation shows that uncertainty of genetic parameters can be reduced by sampling each individual more than once. Because sample sizes are likely to remain relatively small in most primate behavior genetics, expressing uncertainty in parameter estimates is needed to move our inferences forward.
Similar content being viewed by others
References
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.
Bell, A. M., Hankison, S. J., & Laskowski, K. L. (2009). The repeatability of behaviour: A meta-analysis. Animal Behaviour, 77(4), 771–783.
Bijma, P. (2010). Estimating indirect genetic effects: Precision of estimates and optimum designs. Genetics, 186(3), 1013–1028.
Brent, L. J. N., Heilbronner, S. R., Horvath, J. E., Gonzalez-Martinez, J., Ruiz-Lambides, A., Robinson, A. G., et al. (2013). Genetic origins of social networks in rhesus macaques. Scientific Reports, 3. doi:10.1038/srep01042.
Briley, D. A., & Tucker-Drob, E. M. (2013). Explaining the increasing veritability of cognitive ability across development: A meta-analysis of longitudinal twin and adoption studies. Psychological Science. doi:10.1177/0956797613478618.
Bush, W. S., & Moore, J. H. (2012). Genome-wide association studies. PLoS Computational Biology, 8(12), e1002822. doi:10.1371/journal.pcbi.1002822.
Cavigelli, S. A., & Pereira, M. E. (2000). Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta). Hormones and Behavior, 37(3), 246–255.
Charney, E. (2012). Behavior genetics and postgenomics. Behavioral and Brain Sciences, 35(05), 331–358.
Cheverud, J. M., Rutledge, J. J., & Atchley, W. R. (1983). Quantitative genetics of development: Genetic correlations among age-specific trait values and the evolution of ontogeny. Evolution, 37(5), 895–905.
Cockerham, C. C. (1954). An extension of the concept of partitioning hereditary variance for analysis of covariances among relatives when epistasis is present. Genetics, 39(6), 859.
Cumming, G. (2008). Replication and p intervals: p values predict the future only vaguely, but confidence intervals do much better. Perspectives on Psychological Science, 3(4), 286–300.
de Moor, M. H., Costa, P., Terracciano, A., Krueger, R., De Geus, E., Toshiko, T., et al. (2010). Meta-analysis of genome-wide association studies for personality. Molecular Psychiatry, 17(3), 337–349.
Dohm, M. (2002). Repeatability estimates do not always set an upper limit to heritability. Functional Ecology, 16(2), 273–280.
Eaves, L. J. (1988). Dominance alone is not enough. Behavior Genetics, 18(1), 27–33.
Eaves, L. J., Last, K. A., Young, P. A., & Martin, N. G. (1978). Model-fitting approaches to the analysis of human behaviour. Heredity, 41(3), 249–320.
Ebstein, R. (2006). The molecular genetic architecture of human personality: Beyond self-report questionnaires. Molecular Psychiatry, 11(5), 427–445.
Edwards, A. C., Rollmann, S. M., Morgan, T. J., & Mackay, T. F. (2006). Quantitative genomics of aggressive behavior in Drosophila melanogaster. PLoS Genetics, 2(9), e154.
Efron, B., & Tibshirani, R. J. (1994). An introduction to the bootstrap. New York: Chapman & Hall.
Fairbanks, L. A., Newman, T. K., Bailey, J. N., Jorgensen, M. J., Breidenthal, S. E., Ophoff, R. A., et al. (2004). Genetic contributions to social impulsivity and aggressiveness in vervet monkeys. Biological Psychiatry, 55(6), 642–647.
Falconer, D. S., & Mackay, T. F. C. (1996). Introduction to quantitative genetics. Harlow, UK: Pearson.
Fisher, R. A. (1918). XV.—The correlation between relatives on the supposition of Mendelian inheritance. Earth and Environmental Science Transactions of the Royal Society of Edinburgh, 52(02), 399–433.
Gelman, A. (2005). Analysis of variance—why it is more important than ever. The Annals of Statistics, 33(1), 1–53.
Gelman, A., & Shalizi, C. R. (2013). Philosophy and the practice of Bayesian statistics. British Journal of Mathematical and Statistical Psychology, 66, 8–38.
Gianola, D., & de los Campos, G. (2009). Inferring genetic values for quantitative traits non-parametrically. Genetical Research, 90(06), 525–540.
Goldberg, A. D., Allis, C. D., & Bernstein, E. (2007). Epigenetics: A landscape takes shape. Cell, 128(4), 635.
Gordon, T. P., & Bernstein, I. S. (1973). Seasonal variation in sexual behavior of all male Rhesus troops. American Journal of Physical Anthropology, 38(2), 221–225.
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.
Hill, R., Barrett, L., Gaynor, D., Weingrill, T., Dixon, P., Payne, H., et al. (2003). Day length, latitude and behavioural (in) flexibility in baboons (Papio cynocephalus ursinus). Behavioral Ecology and Sociobiology, 53(5), 278–286.
Hill, W. G., Goddard, M. E., & Visscher, P. M. (2008). Data and theory point to mainly additive genetic variance for complex traits. PLoS Genetics, 4(2), e1000008.
Hopkins, W. D., Adams, M. J., & Weiss, A. (2013). Genetic and environmental contributions to the expression of handedness in chimpanzees (Pan troglodytes). Genes, Brain and Behavior, 12, 446–452.
Hur, Y. M. (2007). Evidence for nonadditive genetic effects on Eysenck Personality Scales in South Korean twins. Twin Research and Human Genetics, 10(02), 373–378.
Inoue-Murayama, M. (2009). Genetic polymorphism as a background of animal behavior. Animal Science Journal, 80(2), 113–120.
Johnson, W., Turkheimer, E., Gottesman, I. I., & Bouchard, T. J., Jr. (2009). Beyond heritability twin studies in behavioral research. Current Directions in Psychological Science, 18(4), 217–220.
Kandler, C. (2012). Nature and nurture in personality development: The case of neuroticism and extraversion. Current Directions in Psychological Science, 21(5), 290–296.
Kappeler, P. M., & van Schaik, C. P. (2002). Evolution of primate social systems. International Journal of Primatology, 23(4), 707–740.
Keller, M. C., Coventry, W. M., Heath, A. C., & Martin, N. G. (2005). Widespread evidence for non-additive genetic variation in Cloninger’s and Eysenck’s personality dimensions using a twin plus sibling design. Behavior Genetics, 35, 707–721.
Kerr, M. K., & Churchill, G. A. (2001). Statistical design and the analysis of gene expression microarray data. Genetics Research, 77(02), 123–128.
King, J. E., Weiss, A., & Sisco, M. S. (2008). Aping humans: Age and sex effects in chimpanzee (Pan troglodytes) and human (Homo sapiens) personality. Journal of Comparative Psychology, 122, 418–427.
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.
Kruuk, L. E. B., & Hadfield, J. D. (2007). How to separate genetic and environmental causes of similarity between relatives. Journal of Evolutionary Biology, 20, 1890–1903.
Lande, R. (1979). Quantitative genetic analysis of multivariate evolution, applied to brain: Body size allometry. Evolution, 33(1), 402–416.
Lawler, R. R., & Blomquist, G. E. (2010). Multivariate selection theory in primatology: An introduction to the concepts and literature. Open Anthropology Journal, 3, 206–229.
Lykken, D. T., Bouchard, T., Jr., McGue, M., & Tellegen, A. (1992). Emergenesis: Genetic traits that may not run in familes. American Psychologist, 47, 1565–1577.
Lynch, M., & Walsh, B. (1998). Genetics and analysis of quantitative traits. Sunderland, MA: Sinauer.
Maas, C. J., & Hox, J. J. (2005). Sufficient sample sizes for multilevel modeling. Methodology, 1(3), 86–92.
Majolo, B., & Koyama, N. (2006). Seasonal effects on reconciliation in Macaca fuscata yakui. International Journal of Primatology, 27(5), 1383–1397.
Majolo, B., Ventura, R., & Koyama, N. F. (2005). Sex, rank and age differences in the Japanese macaque (Macaca fuscata yakui) participation in inter-group encounters. Ethology, 111(5), 455–468.
Maruhashi, T. (1981). Activity patterns of a troop of Japanese monkeys (Macaca fuscata yakui) on Yakushima Island, Japan. Primates, 22(1), 1–14.
Mendoza, S. P., Lowe, E. L., Resko, J. A., & Levine, S. (1978). Seasonal variations in gonadal hormones and social behavior in squirrel monkeys. Physiology & Behavior, 20(5), 515–522.
Merilä, J., & Sheldon, B. C. (1999). Genetic architecture of fitness and nonfitness traits: empirical patterns and development of ideas. Heredity, 83(2), 103–109.
Meuwissen, T., Hayes, B., & Goddard, M. (2013). Accelerating improvement of livestock with genomic selection. Annual Review of Animal Biosciences, 1(1), 221–237.
Moore, A. J., Brodie III, E. D., & Wolf, J. B. (1997). Interacting phenotypes and the evolutionary process: I. Direct and indirect genetic effects of social interactions. Evolution, 51(5), 1352–1362.
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(4), 711–719.
Morrissey, M. B., Wilson, A. J., Pemberton, J. M., & Ferguson, M. M. (2007). A framework for power and sensitivity analyses for quantitative genetic studies of natural populations, and case studies in Soay sheep (Ovis aries). Journal of Evolutionary Biology, 20(6), 2309–2321.
Nakagawa, S., & Schielzeth, H. (2010). Repeatability for Gaussian and non-Gaussian data: A practical guide for biologists. Biological Reviews, 85(4), 935–956.
Nussey, D., Wilson, A., & Brommer, J. (2007). The evolutionary ecology of individual phenotypic plasticity in wild populations. Journal of Evolutionary Biology, 20(3), 831–844.
Ostner, J., Kappeler, P., & Heistermann, M. (2002). Seasonal variation and social correlates of androgen excretion in male redfronted lemurs (Eulemur fulvus rufus). Behavioral Ecology and Sociobiology, 52(6), 485–495.
Phillips, P. C., & Arnold, S. J. (1999). Hierarchical comparison of genetic variance-covariance matrices. I. Using the Flury hierarchy. Evolution, 53(5), 1506–1515.
Poissant, J., Réale, D., Martin, J. G. A., Festa-Bianchet, M., & Coltman, D. W. (2013). A quantitative trait locus analysis of personality in wild bighorn sheep. Ecology and Evolution, 3(3), 474–481.
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(3), 994–1002.
Rice, S. H. (2004). Evolutionary theory: Mathematical and conceptual foundations. Sunderland, MA: Sinauer Associates.
Robinson, M. R., & Beckerman, A. P. (2013). Quantifying multivariate plasticity: Genetic variation in resource acquisition drives plasticity in resource allocation to components of life history. Ecology Letters, 16, 281–290.
Ross, S. (2009). North American regional chimpanzee studbook (Pan troglodytes). Chicago: Linocln Park Zoo.
Shrout, P. E., & Fleiss, J. L. (1979). Intraclass correlations: Uses in assessing rater reliability. Psychological Bulletin, 86, 420–428.
Slate, J. (2013). From Beavis to beak colour: A simulation study to examine how much QTL mapping can reveal about the genetic architecture of quantitative traits. Evolution, 67(5), 1251–1262.
Sokal, R., & Rohlf, F. (1995). Biometry (3rd ed.). New York: W. H. Freeman.
Strier, K. B., Ziegler, T. E., & Wittwer, D. J. (1999). Seasonal and social correlates of fecal testosterone and cortisol levels in wild male muriquis (Brachyteles arachnoides). Hormones and Behavior, 35(2), 125–134.
Uher, J. (2011). Individual behavioral phenotypes: An integrative meta-theoretical framework. Why “behavioral syndromes” are not analogs of “personality”. Developmental Psychobiology, 53(6), 521–548.
Uher, J., Addessi, E., & Visalberghi, E. (2013). Contextualised behavioural measurements of personality differences obtained in behavioural tests and social observations in adult capuchin monkeys (Cebus apella). Journal of Research in Personality, 47(4), 427–444.
van Oers, K., Drent, P. J., de Jong, G., & van Noordwijk, A. J. (2004). Additive and nonadditive genetic variation in avian personality traits. Heredity, 93(5), 496–503.
Ventura, R., Majolo, B., Schino, G., & Hardie, S. (2005). Differential effects of ambient temperature and humidity on allogrooming, self–grooming, and scratching in wild Japanese macaques. American Journal of Physical Anthropology, 126(4), 453–457.
Weiss, A., Bates, T. C., & Luciano, M. (2008). Happiness is a personal(ity) thing – The genetics of personality and well-being in a representative sample. Psychological Science, 19, 205–210.
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, 1141–1149.
Weiss, A., King, J. E., & Figueredo, A. J. (2000). The heritability of personality factors in chimpanzees (Pan troglodytes). Behavior Genetics, 30, 213–221.
Wilson, A. J., Réale, D., Clements, M. N., Morrissey, M. M., Postma, E., Walling, C. A., et al. (2009). An ecologist's guide to the animal model. Journal of Animal Ecology, 79(1), 13–26.
Wilson, R. S. (1978). Synchronies in mental development: An epigenetic perspective. Science, 202(4371), 939–948.
Wolak, M. E. (2012). nadiv : An R package to create relatedness matrices for estimating non-additive genetic variances in animal models. Methods in Ecology and Evolution, 3(5), 792–796.
Acknowledgments
I thank Matt Robinson and two anonymous reviewers for their comments on this manuscript. I am indebted to Alex Weiss, Ana Maria Fernández, Jarrod Hadfield, Lauren Brent, Loeske Kruuk, Luis Apiolaza, Jocelyn Poissant, Elisabeth Bolund, Anna Santure, and Isabel Winney for their high-yielding discussions that prompted me to write this all down. I also thank Antje Engelhardt for inviting me to speak on these topics.
Author information
Authors and Affiliations
Corresponding author
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 123 kb)
Rights and permissions
About this article
Cite this article
Adams, M.J. Feasibility and Uncertainty in Behavior Genetics for the Nonhuman Primate. Int J Primatol 35, 156–168 (2014). https://doi.org/10.1007/s10764-013-9722-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10764-013-9722-8