Shared spatial effects on quantitative genetic parameters: Accounting for spatial autocorrelation and home range overlap reduces estimates of heritability in wild red deer

Evolution

Volumn 66, Issue 8, 2012, Pages 2411-2426

  Stopher, Katie V ^a   Walling, Craig A ^a   Morris, Alison ^a   Guinness, Fiona E ^b   Clutton Brock, Tim H ^b   Pemberton, Josephine M ^a   Nussey, Daniel H ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

"animal model"; Additive genetic variance; Maternal effects; Microevolution; Resource heterogeneity

Indexed keywords

DEER; DISPERSAL; ECOLOGICAL MODELING; ENVIRONMENTAL EFFECT; ESTIMATION METHOD; GENETIC VARIATION; HERITABILITY; HETEROGENEITY; HOME RANGE; MATERNAL EFFECT; PHENOTYPE; QUANTITATIVE ANALYSIS; SPATIAL ANALYSIS; WILD POPULATION;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BIOLOGICAL MODEL; BIRTH WEIGHT; DEER; ENVIRONMENT; FEMALE; GENETIC VARIABILITY; GENETICS; PHYSIOLOGY; REPRODUCTION; SEASON; SPATIAL ANALYSIS; UNITED KINGDOM;

ANIMALS; BIRTH WEIGHT; DEER; ENVIRONMENT; FEMALE; GENETIC VARIATION; HOMING BEHAVIOR; MODELS, BIOLOGICAL; REPRODUCTION; SCOTLAND; SEASONS; SPATIAL ANALYSIS;

ANIMALIA; CERVUS ELAPHUS; VERTEBRATA;

EID: 84864300430     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2012.01620.x     Document Type: Article

References (77)

1. Albon, S. D., H. J. Staines, F. E. Guinness, and T. H. Clutton-Brock. 1992. Density-dependent changes in the spacing behaviour of female kin in red deer. J. Anim. Ecol. 61:131-137.
2. Bhattacharyya, A. 1943. On a measure of divergence between two statistical populations defined by their probability distributions. Bull. Calcutta Math. Soc. 35:99-109.
3. Borger, L., N. Franconi, G. De Michele, A. Gantz, F. Meschi, A. Manica, S. Lovari, and T. Coulson. 2006. Effects of sampling regime on the mean and variance of home range size estimates. J. Anim. Ecol. 75:1393-1405.
4. Burgueno, J. C. A., J. Crossa, M. Banziger, A. R. Gilmour, and B. R. Cullis. 2000. User's guide for spatial analysis of field variety trials using asreml. CIMMYT, Mexico.
5. Calenge, C. 2006. The package "Adehabitat" For the r software: a tool for the analysis of space and habitat use by animals. Ecol. Modell. 197:516-519.
6. Charmantier, A., L. E. B. Kruuk, J. Blondel, and M. M. Lambrechts. 2004. Testing for microevolution in body size in three blue tit populations. J. Evol. Biol. 17:732-743.
7. Charmantier, A., M. Bruro, O. Giminez, and H. Weimerskirch. 2011. Heritability of short-scale natal dispersal in a large-scale foraging bird, the wandering albatross. J. Evol. Biol. 24:1487-1496.
8. Cliff, A. O., and J. K. Ord. 1981. Spatial processes: models and applications. Pion, London.
9. Clutton-Brock, T. H., F. E. Guinness, and S. D. Albon. 1982. Red deer: behaviour and ecology of two sexes. Univ. of Chicago Press, Chicago, IL.
10. Costa e Silva, J., G. W. Dutkowski, and A. R. Gilmour. 2001. Analysis of early tree height in forest genetic trials is enhanced by including a spatially correlated residual. Can. J. For. Res. 31:1887-1893.
11. Coulson, T., F. Guinness, J. Pemberton, and T. Clutton-Brock. 2004. The demographic consequences of releasing a population of red deer from culling. Ecology 85:411-422.
12. Coulson, T. N., S. D. Albon, F. E. Guinness, J. P. Pemberton, and T. H. Clutton-Brock. 1997. Population sub-stucture, local density and calf winter survival in red deer (Cervus elaphus). Ecology 78:852-863.
13. Coulson, T. N., L. E. B. Kruuk, G. Tavecchia, J. M. Pemberton, and T. H. Clutton-Brock. 2003. Estimating selection on neonatal traits in red deer using elasticity path analysis. Evolution 57:2879-2892.
14. Croft, D. P., J. Krause, and R. James. 2004. Social networks in the guppy (Poecilia reticulata). Proc. R. Soc. Lond. Ser. B Biol. Sci. 271:S516-S519.
15. Croft, D. P., R. James, P. O. R. Thomas, C. Hathaway, D. Mawdsley, K. N. Laland, and J. Krause. 2006. Social structure and co-operative interactions in a wild population of guppies (Poecilia reticulata). Behav. Ecol. Sociobiol. 59:644-650.
16. Cullis, B. R., and A. C. Gleeson. 1989. Efficiency of neighbor analysis for replicated variety trials in australia. J. Agric. Sci. 113:233-239.
17. Cullis, B. R., and A. C. Gleeson. 1991. Spatial-analysis of field experiments-an extension to 2 dimensions. Biometrics 47:1449-1460.
18. Danchin, E., A. Charmantier, F. A. Champagne, A. Mesoudi, B. Pujol, and S. Blanchet. 2011. Beyond DNA: integrating inclusive inheritance into an extended theory of evolution. Nat. Rev. Genet. 12:475-486.
19. Doligez, B., L. Gustafsson, and T. Part. 2009. 'Heritability' of dispersal propensity in a patchy population. Proc. R. Soc. Lond. Ser. B Biol. Sci. 276:2829-2836.
20. Dutkowski, G. W., J. C. E. Silva, A. R. Gilmour, and G. A. Lopez. 2002. Spatial analysis methods for forest genetic trials. Can. J. For. Res. 32:2201-2214.
21. Ellegren, H., and B. C. Sheldon. 2008. Genetic basis of fitness differences in natural populations. Nature 452:169-175.
22. Falconer, D. S., and T. F. C. Mackay. 1996. Introduction to quantitative genetics. 4th ed. Prentice Hall, London.
23. Fieberg, J., and C. O. Kochanny. 2005. Quantifying home-range overlap: the importance of the utilization distribution.J. Wildl. Manage. 69:1346-1359.
24. Fortin, M. D., and M. R. T. Dale. 2005. Spatial analysis: a guide for ecologists. Cambridge Univ. Press, Cambridge, U.K.
25. Fortin, M. J., and M. R. T. Dale. 2009. Spatial autocorrelation in ecological studies: a legacy of solutions and myths. Geogr. Anal. 41:392-397.
26. Frere, C. H., M. Krutzen, J. Mann, R. C. Connor, L. Bejder, and W. B. Sherwin. 2010. Social and genetic interactions drive fitness variation in a free-living dolphin population. Proc. Natl. Acad. Sci. USA 107:19949-19954.
27. Gilmore, A. R., B. J. Gogel, B. R. Cullis, and R. Thompson. 2009. Asreml user guide release 3.0. VSN International Ltd, Hemel Hempsted.
28. Gilmour, A. R., B. R. Cullis, and A. P. Verbyla. 1997. Accounting for natural extraneous variation in the analysis of field experiments. J. Agric. Biol. Environ. Stat. 2:269-273.
29. Guinness, F. E., T. H. Clutton-Brock, and S. D. Albon. 1978. Factors affecting calf mortality in red deer (Cervus elaphus). J. Anim. Ecol. 47:817-832.
30. Hadfield, J. D., D. S. Richardson, and T. Burke. 2006. Towards unbiased parentage assignment: combining genetic, behavioural and spatial data in a bayesian framework. Mol. Ecol. 15:3715-3730.
31. Haining, R. 2004. Spatial data analysis: theory and practice. Cambridge Univ. Press, New York.
32. Henderson, C. R. 1953. Estimation of variance and covariance components. Biometrics 9:226-252.
33. Henderson, C. R. 1976. Simple method for computing inverse of a numerator relationship matrix used in prediction of breeding values. Biometrics 32:69-83.
34. Houle, D. 1992. Comparing evolvability and variability of quantitative traits. Genetics 130:195-204.
35. Kissling, W. D., and G. Carl. 2008. Spatial autocorrelation and the selection of simultaneous autoregressive models. Global Ecol. Biogeogr. 17:59-71.
36. Kruuk, L. E. B. 2004. Estimating genetic parameters in natural populations using the 'animal model'. Philos. Trans. R. Soc. London, Ser. B Biol. Sci. 359:873-890.
37. Kruuk, L. E. B., and J. D. Hadfield. 2007. How to separate genetic and environmental causes of similarity between relatives. J. Evol. Biol. 20:1890-1903.
38. Kruuk, L. E. B., T. H. Clutton-Brock, J. Slate, J. M. Pemberton, S. Brotherstone, and F. E. Guinness. 2000. Heritability of fitness in a wild mammal population. Proc. Natl. Acad. USA 97:698-703.
39. Kruuk, L. E. B., J. Merila, and B. C. Sheldon. 2001. Phenotypic selection on a heritable trait revisited. Am. Nat. 158:557-571.
40. Kruuk, L. E. B., J. Slate, and A. J. Wilson. 2008. New answers for old questions: the evolutionary quantitative genetics of wild animal populations. Annu. Rev. Ecol. Evol. Syst. 39:525-548.
41. Lande, R. 1982. A quantitative genetic theory of life-history evolution. Ecology 63:607-615.
42. Legendre, P. 1993. Spatial autocorrelation-trouble or new paradigm. Ecology 74:1659-1673.
43. Lynch, M., and B. Walsh. 1998. Genetics and analysis of quantitative traits. Sinauer, Sunderland.
44. MacColl, A. D. C., and B. J. Hatchwell. 2003. Heritability of parental effort in a passerine bird. Evolution 57:2191-2195.
45. Magnussen, S. 1993. Bias in genetic variance estimates due to spatial autocorrelation. Theor. Appl. Genet. 86:349-355.
46. McLoughlin, P. D., M. S. Boyce, T. Coulson, and T. Clutton-Brock. 2006. Lifetime reproductive success and density-dependent, multi-variable resource selection. Proc. R. Soc. Lond. Ser. B Biol. Sci. 273:1449-1454.
47. McLoughlin, P. D., T. Coulson, and T. Clutton-Brock. 2008. Cross-generational effects of habitat and density on life history in red deer. Ecology 89:3317-3326.
48. McNab, B. K. 1963. Bioenergetics and determination of home range size. Am. Nat. 97:133-140.
49. Merila, J., and B. C. Sheldon. 2000. Lifetime reproductive success and heritability in nature. Am. Nat. 155:301-310.
50. Moyes, K. 2007. Demographic consequences of individual variation. Ph.D. thesis, University of Kent, Canterbury, U.K.
51. Moyes, K., D. H. Nussey, M. N. Clements, F. E. Guinness, A. Morris, S. Morris, J. M. Pemberton, L. E. B. Kruuk, and T. H. Clutton-Brock. 2011. Advancing breeding phenology in response to environmental change in a wild red deer population. Glob. Change Biol. 17:2455-2469.
52. Nussey, D. H., T. H. Clutton-Brock, S. D. Albon, J. Pemberton, and L. E. B. Kruuk. 2005a. Constraints on plastic responses to climate variation in red deer. Biol. Lett. 1:457-460.
53. Nussey, D. H., T. H. Clutton-Brock, D. A. Elston, S. D. Albon, and L. E. B. Kruuk. 2005b. Phenotypic plasticity in a maternal trait in red deer. J. Anim. Ecol. 74:387-396.
54. Nussey, D. H., D. W. Coltman, T. Coulson, L. E. B. Kruuk, A. Donald, S. J. Morris, T. H. Clutton-Brock, and J. Pemberton. 2005c. Rapidly declining fine-scale spatial structure in female red deer. Mol. Ecol. 14:3395-3405.
55. Nussey, D. H., L. E. B. Kruuk, A. Morris, M. N. Clements, J. M. Pemberton, and T. H. Clutton-Brock. 2009. Inter- and intra-sexual variation in ageing patterns across reproductive traits in a wild red deer population. Am. Nat. 174:342-357.
56. Palucci, V., L. R. Schaeffer, F. Miglior, and V. Osborne. 2007. Non-additive genetic effects for fertility traits in canadian holstein cattle. Genet. Selection Evol. 39:181-193.
57. Postma, E., and A. Charmantier 2007. What 'animal models' can and cannot tell ornithologists about the genetics of wild populations. J. Ornithology 148:633-642.
58. R Development Core Team. 2008. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, Available at URL (accessed February 1, 2011).
59. Rhodes, M., G. W. Wardell-Johnson, M. P. Rhodes, and B. Raymond. 2006. Applying network analysis to the conservation of habitat trees in urban environments: a case study from Brisbane, Australia. Conserv. Biol. 20:861-870.
60. Rodriguez-Munoz, R., A. Bretman, J. Slate, C. A. Walling, and T. Tregenza. 2010. Natural and sexual selection in a wild insect population. Science 328:1269-1272.
61. Silk, J. B., S. C. Alberts, and J. Altmann. 2003. Social bonds of female baboons enhance infant survival. Science 302:1231-1234.
62. Silk, J. B., J. C. Beehner, T. J. Bergman, C. Crockford, A. L. Engh, L. R. Moscovice, R. M. Wittig, R. M. Seyfarth, and D. L. Cheney. 2010. Strong and consistent social bonds enhance the longevity of female baboons. Curr. Biol. 20:1359-1361.
63. Smith, S. P., and A. Maki-Tanila. 1990. Genotypic covariance matrices and their inverses for models allowing dominance and inbreeding. Genet. Select. Evol. 22:65-91.
64. Stopher, K. V., J. M. Pemberton, T. H. Clutton-Brock, and T. Coulson. 2008. Individual differences, density dependence and offspring birth traits in a population of red deer. Proc. R. Soc. Lond. Ser. B Biol. Sci. 275:2137-2145.
65. Stopher, K. V., D. H. Nussey, T. H. Clutton-Brock, F. E. Guinness, A. Morris, and J. M. Pemberton. 2011. The red deer rut revisited: female excursions but no evidence females move to mate with preferred males. Behav. Ecol. 22:808-818.
66. Teplitsky, C., N. G. Mouawad, J. Balbontin, F. De Lope, and A. P. Møller. 2011. Quantitative genetics of migration syndromes: a study of two barn swallow populations. J. Evol. Biol. 24:2025-2039.
67. Tufto, J., R. Andersen, and J. Linnell. 1996. Habitat use and ecological correlates of home range size in a small cervid: the roe deer. J. Anim. Ecol. 65:715-724.
68. van der Jeugd, H. P., and R. McCleery. 2002. Effects of spatial autocorrelation, natal philopatry and phenotypic plasticity on the heritability of laying date. J. Evol. Biol. 15:380-387.
69. Walling, C. A., J. M. Pemberton, J. D. Hadfield, and L. E. B. Kruuk. 2010. Comparing parentage inference software: re-analysis of a red deer pedigree. Mol. Ecol. 19:1914-1928.
70. Walsh, B., and M. Lynch. 2009. Evolution and selection of quantitative traits. Available at.
71. Wang, J., and A. W. Santure. 2009. Parentage and sibship inference from multilocus genotype data under polygamy. Genetics 181:1579-1594.
72. Waser, P. M., and W. T. Jones. 1989. Heritability of dispersal in banner-tailed kangaroo rats, dipodomys-spectabilis. Anim. Behav. 37:987-991.
73. Wey, T., D. T. Blumstein, W. Shen, and F. Jordan. 2008. Social network analysis of animal behaviour: a promising tool for the study of sociality. Anim. Behav. 75:333-344.
74. Whitehead, H. 2008. Analysing animal societies: quantitative methods for vertebrate social analysis. Chicago Univ. Press, Chicago, IL.
75. Wilson, A. J., D. W. Coltman, J. M. Pemberton, A. D. J. Overall, K. A. Byrne, and L. E. B. Kruuk. 2005. Maternal genetic effects set the potential for evolution in a free-living vertebrate population. J. Evol. Biol. 18:405-414.
76. Worton, B. J. 1987. A review of models of home range for animal movement. Ecol. Modell. 38:277-298.
77. Worton, B. J. 1989. Kernel methods for estimating the utilization distribution in home-range studies. Ecology. 70:164-168.