Abstract
Heritabilities of traits closely related to fitness (e.g. life-history traits) tend to be lower than those of morphological traits in natural populations. It is unclear, however, whether this pattern reflects relatively low additive-genetic variation, relatively high residual variation (i.e. non-additive and environmental effects) or both. A standard, half-sib breeding design was used to estimate narrow-sense heritabilities and coefficients of additive-genetic variation (CVA) for a life-history trait (total fecundity), a morphological trait (wing length) and a behavioural trait (allocation of eggs among available resources) in two outbred populations of the seed beetle Callosobruchus maculatus. Heritabilities of fecundity and wing length were high in both populations whereas the heritability of egg-laying behaviour was low but non-zero. In contrast, estimates of ‘evolvability’, which depend on CVA, were highest for fecundity, intermediate for egg-laying behaviour and lowest for wing length. These results resemble those from a recent survey of Drosophila studies and suggest that the typically low heritabilities of behavioural or life-history traits are better explained by high residual variation than by low additive-genetic variation. Phenotypic and genetic correlations were generally not significant except for a positive relationship between wing length and fecundity. No evidence was obtained of a trade-off or underlying functional relationship between the number of eggs laid and the pattern of egg dispersion among available resources.
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References
Arnold, S J. 1992. Constraints on phenotypic evolution. Am Nat, 140 (Suppl.), 85–107.
Barton, N H, and Turelli, M. 1989. Evolutionary quantitative genetics: how little do we know? Ann Rev Genet, 23, 337–370.
Becker, W A. 1984. Manual of Quantitative Genetics, 4th edn. Academic Enterprises, Pullman, WA.
Charlesworth, B. 1984. The evolutionary genetics of life histories. In: Shorrocks, B. (ed.), Evolutionary Ecology, Blackwell Scientific, Oxford, pp. 117–133.
Charlesworth, B. 1990. Optimization models, quantitative genetics, and mutation. Evolution, 44, 520–538.
Cowley, D E, and Atchley, W R. 1992. Comparison of quantitative genetic parameters. Evolution, 46, 1965–1967.
Credland, P F, Dick, K M, and Wright, A W. 1986. Relationships between larval density, adult size and egg production in the cowpea seed beetle, Callosobruchus maculatus. Ecol Entomol, 11, 41–50.
Credland, P F, and Wright, A W. 1990. Oviposition deterrents of Callosobruchus maculatus (Coleoptera: Bruchidae). Physiol Entomol, 15, 285–298.
Falconer, D S. 1989. Introduction to Quantitative Genetics, 3rd edn. Wiley, New York.
Fisher, R A. 1958. The Genetical Theory of Natural Selection, 2nd edn. Dover Publications, New York.
Fox, C W. 1993. A quantitative analysis of oviposition preference and larval performance on two hosts in the bruchid beetle, Callosobruchus maculatus. Evolution, 47, 166–175.
Gustafsson, L. 1986. Lifetime reproductive success and heritability: empirical support for Fisher's fundamental theorem. Am Nat, 128, 761–764.
Hagstrum, D W. 1985. Preharvest infestation of cowpeas by the cowpea weevil (Coleoptera: Bruchidae) and population trends during storage in Florida. J Econ Entomol, 78, 358–361.
Houle, D. 1991. Genetic covariance of fitness correlates: what genetic correlations are made of and why it matters. Evolution, 45, 630–648.
Houle, D. 1992. Comparing evolvability and variability of quantitative traits. Genetics, 130, 195–204.
Huignard, J, Leroi, B, Alzouma, I, and Germain, J F. 1985. Oviposition and development of Bruchidius atrolineatus (Pic) and Callosobruchus maculatus (F.) (Coleoptera: Bruchidae) in Vigna unguiculata (Walp) cultures in Niger. Insect Sci Appl, 6, 691–699.
Lande, R. 1982. A quantitative genetic theory of life history evolution. Ecology, 63, 607–615.
Messina, F J. 1989. Genetic basis of variable oviposition behavior in Callosobruchus maculatus (Coleoptera: Bruchidae). Ann Entomol Soc Am, 82, 792–796.
Messina, F J. 1990. Alternative life-histories in Callosobruchus maculatus: environmental and genetic bases. In: Fujii, K., Gatehouse, A. M. R., Johnson, C. D., Mitchell, R. and Yoshida, T. (eds), Bruchids and Legumes: Economics, Ecology and Coevolution, Kluwer Academic, The Netherlands, pp. 303–315.
Messina, F J. 1991. Life-history variation in a seed beetle: adult egg-laying vs. larval competitive ability. Oecologia, 85, 447–455.
Messina, F J, Gardner, S L, and Morse, G E. 1991. Host discrimination by egg-laying seed beetles: causes of population differences. Anim Behav, 41, 773–780.
Messina, F J, and Mitchell, R. 1989. Intraspecific variation in the egg-spacing behaviour of the seed beetle Callosobruchus maculatus. J Insect Behav, 2, 727–741.
Messina, F J, and Renwick, J A A. 1985. Ability of ovipositing seed beetles to discriminate between seeds with differing egg loads. Ecol Entomol, 10, 225–230.
Mitchell, R. 1975. The evolution of oviposition tactics in the bean weevil, Callosobruchus maculatus (F.). Ecology, 56, 696–702.
Mitchell, R. 1983. Effects of host-plant variability on the fitness of sedentary herbivorous insects. In: Denno, R. F. and McClure, M. S. (eds), Variable Plants and Herbivores in Natural and Managed Systems, Academic Press, New York, pp. 343–370.
Mitchell, R. 1990. Behavioral ecology of Callosobruchus maculatus. In: Fujii, K., Gatehouse, A. M. R., Johnson, C. D., Mitchell, R. and Yoshida, T. (eds), Bruchids and Legumes: Economics, Ecology and Coevolution, Kluwer Academic, The Netherlands, pp. 317–330.
Moller, H, Smith, R H, and Sibly, R M. 1989. Evolutionary demography of a bruchid beetle. I. Quantitative genetical analysis of the female life history. Funct Ecol, 3, 673–681.
Mousseau, T A, and Roff, D A. 1987. Natural selection and the heritability of fitness components. Heredity, 59, 181–197.
Price, T, and Schlurer, D. 1991. On the low heritability of life-history traits. Evolution, 45, 853–861.
Roff, D A, and Mousseau, T A. 1987. Quantitative genetics and fitness: lessons from Drosophila. Heredity, 58, 103–118.
SAS Institute Inc. 1988. SAS/STAT User's Guide. SAS Inst. Inc., Cary, NC.
Service, P M, and Rose, M R. 1985. Genetic covariation among life-history components: the effect of novel environments. Evolution, 39, 943–945.
Shaw, R G. 1992. Comparison of quantitative genetic parameters: reply to Cowley and Atchley. Evolution, 46, 1967–1969.
Sibly, R M, Smith, R H, and Møller, H. 1991. Evolutionary demography of a bruchid beetle. IV. Genetic trade-off, stabilizing selection and a model of optimal body size. Funct Ecol, 5, 594–601.
Smith, R H. 1991. Genetic and phenotypic aspects of life-history evolution in animals. Adv Ecol Res, 21, 63–120.
Sokal, R R, and Rohlf, F J. 1981. Biometry, 2nd edn. W. H. Freeman, San Francisco.
Stearns, S, De Jong, G, and Newman, B. 1991. The effects of phenotypic plasticity on genetic correlations. Trends Ecol Evol, 6, 122–126.
Tanaka, Y. 1991. Individual variation of scent avoiding oviposition behavior in adzuki bean weevil Callosobruchus chinensis. J Ethol, 9, 31–33.
Taper, M L. 1990. Experimental character displacement in the adzuki bean weevil, Callosobruchus chinensis. In: Fujii, K., Gatehouse, A. M. R., Johnson, C. D., Mitchell, R. and Yoshida, T. (eds), Bruchids and Legumes: Economics, Ecology and Coevolution, Kluwer Academic, The Netherlands, pp. 289–301.
Tucić, N, Milośević, M, Gliksman, I, Milanović, D, and Aleksić, I. 1991. The effects of larval density on genetic variation and covariation among life-history traits in the bean weevil (Acanthoscelides obtectus Say). Funct Ecol, 5, 525–534.
Utida, S. 1972. Density dependent polymorphism in the adult of Callosobruchus maculatus (Coleoptera, Bruchidae). J Stored Prod Res, 8, 111–126.
Wasserman, S S. 1986. Behavioral analysis of male-induced interstrain differences in realized fecundity in Callosobruchus maculatus. In: Huettel, M. D. (ed.), Evolutionary Genetics of Invertebrate Behavior, Plenum, New York, pp. 145–152.
Wasserman, S S, and Futuyma, D J. 1981. Evolution of host plant utilization in laboratory populations of the southern cowpea weevil, Callosobruchus maculatus Fabricius (Coleoptera: Bruchidae). Evolution, 35, 605–617.
Willis, J H, Coynes, J A, and Kirkpatrick, M. 1991. Can one predict the evolution of quantitative characters without genetics? Evolution, 45, 441–444.
Wilson, K, and Hill, L. 1989. Factors affecting egg maturation in the bean weevil Callosobruchus maculatus. Physiol Entomol, 14, 115–126.
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Messina, F. Heritability and ‘evolvability’ of fitness components in Callosobruchus maculatus. Heredity 71, 623–629 (1993). https://doi.org/10.1038/hdy.1993.187
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DOI: https://doi.org/10.1038/hdy.1993.187
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