EXPRESSION OF ADDITIVE GENETIC VARIANCES AND COVARIANCES FOR WILD RADISH FLORAL TRAITS: COMPARISON BETWEEN FIELD AND GREENHOUSE ENVIRONMENTS
Jeffrey K. Conner
W. K. Kellogg Biological Station and Department of Plant Biology, Michigan State University, Hickory Corners, Michigan 49060
E-mail: [email protected]
Search for more papers by this authorRachael Franks
W. K. Kellogg Biological Station and Department of Plant Biology, Michigan State University, Hickory Corners, Michigan 49060
Search for more papers by this authorChristy Stewart
W. K. Kellogg Biological Station and Department of Plant Biology, Michigan State University, Hickory Corners, Michigan 49060
Search for more papers by this authorJeffrey K. Conner
W. K. Kellogg Biological Station and Department of Plant Biology, Michigan State University, Hickory Corners, Michigan 49060
E-mail: [email protected]
Search for more papers by this authorRachael Franks
W. K. Kellogg Biological Station and Department of Plant Biology, Michigan State University, Hickory Corners, Michigan 49060
Search for more papers by this authorChristy Stewart
W. K. Kellogg Biological Station and Department of Plant Biology, Michigan State University, Hickory Corners, Michigan 49060
Search for more papers by this authorAbstract
Abstract Measurements of the genetic variation and covariation underlying quantitative traits are crucial to our understanding of current evolutionary change and the mechanisms causing this evolution. This fact has spurred a large number of studies estimating heritabilities and genetic correlations in a variety of organisms. Most of these studies have been done in laboratory or greenhouse settings, but it is not well known how accurately these measurements estimate genetic variance and covariance expressed in the field. We conducted a quantitative genetic half-sibling analysis on six floral traits in wild radish. Plants were grown from seed in the field and were exposed to natural environmental variation throughout their lives, including herbivory and intra- and interspecific competition. The estimates of heritabilities and the additive genetic variance-covariance matrix (G) obtained from this analysis were then compared to previous greenhouse estimates of the same floral traits from the same natural population. Heritabilities were much lower in the field for all traits, and this was due to both large increases in environmental variance and decreases in additive genetic variance. Additive genetic covariance expressed was also much lower in the field. These differences resulted in highly significant differences in the G matrix between the greenhouse and field environments using two complementary testing methods. Although the G matrices shared some principal components in common, they were not simply proportional to each other. Therefore, the greenhouse results did not accurately depict how the floral traits would respond to natural selection in the field.
Literature Cited
- Arnold, S. J., and M. J. Wade 1984a. On the measurement of natural and sexual selection: applications. Evolution. 38: 720–734.
- 1984b. On the measurement of natural and sexual selection: theory. Evolution. 38: 709–719.
- Bennington, C. C., and J. B. McGraw 1996. Environment-dependence of quantitative genetic parameters in Impatiens pallida. Evolution. 50: 1083–1097.
- Blum, A. 1988. Plant breeding for stress environments. CRC Press, Boca Raton , FL .
- Bryant, E. H., and L. M. Meffert 1998. Quantitative genetic estimates of morphometric variation in wild-caught and laboratory-reared houseflies. Evolution. 52: 626–630.
- Campbell, D. R. 1996. Evolution of floral traits in a hermaphroditic plant: field measurements of heritabilities and genetic correlations. Evolution. 50: 1442–1453.
- Campbell, D. R., N. M. Waser, M. V. Price, E. A. Lynch, and R. J. Mitchell 1991. Components of phenotypic selection: Pollen export and flower corolla width in Ipomopsis aggregata. Evolution. 45: 1458–1467.
- Ceccarelli, S. 1994. Specific adaptation and breeding for marginal conditions. Euphytica. 77: 205–219.
- Conner, J. K. 1997. Floral evolution in wild radish: the roles of pollinators, natural selection, and genetic correlations among traits. Int. J. Plant Sci.. 158: S108–S120.
- Conner, J. K., and S. Rush 1996. Effects of flower size and number on pollinator visitation to wild radish, Raphanus raphanistrum. Oecologia. 105: 509–516.
- Conner, J. K., and S. Via 1993. Patterns of phenotypic and genetic correlations among morphological and life-history traits in wild radish, Raphanus raphanistrum. Evolution. 47: 704–711.
- Conner, J. K., R. Davis, and S. Rush 1995. The effect of wild radish floral morphology on pollination efficiency by four taxa of pollinators. Oecologia. 104: 234–245.
- Conner, J. K., S. Rush, and P. Jennetten 1996. Measurements of natural selection on floral traits in wild radish (Raphanus raphanistrum). I. Selection through lifetime female fitness. Evolution. 50: 1127–1136.
- Coyne, J. A., and E. Beecham 1987. Heritability of two morphological characters within and among natural populations of Dro-sophila melanogaster. Genetics. 117: 727–737.
- Cresswell, J. E. 2000. Manipulation of female architecture in flowers reveals a narrow optimum for pollen deposition. Ecology. 81: 3244–3249.
- Dean, A. M. 1995. A molecular investigation of genotype by environment interactions. Genetics. 139: 19–33.
- Falconer, D. S., and T. F. C. Mackay 1996. Introduction to quantitative genetics. Longman, Harlow , U.K .
- Flury, B. D. 1988. Common principal components and related multivariate models. Wiley, New York .
- Galen, C. 1989. Measuring pollinator-mediated selection on morphometric traits: bumblebees and the alpine sky pilot, Polemonium viscosum. Evolution. 43: 882–890.
- 1996. Rates of floral evolution: adaptation to bumblebee pollination in an alpine wildflower, Polemonium viscosum. Evolution. 50: 120–125.
- Harder, L. D., and S. C. H. Barrett 1993. Pollen removal from tristylous Pontederia cordata: effects of anther position and pollinator specialization. Ecology. 74: 1059–1072.
- Hoffmann, A. A., and J. Merila″ 1999. Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol. Evol.. 14: 96–101.
- Holloway, G. J., S. R. Povey, and R. M. Sibly 1990. The effect of new environment on adapted genetic architecture. Heredity. 64: 323–330.
- Houle, D. 1992. Comparing evolvability and variability of quantitative traits. Genetics. 130: 195–204.
- Houle, D., J. Mezey, and P. Galpern 2002. Interpretation of the results of common principal components analysis. Evolution. 56: 433–440.
- Jain, K. K. 2001. Biochips for gene spotting. Science. 294: 621–625.
- Karoly, K., and J. K. Conner 2000. Heritable variation in a family-diagnostic trait. Evolution. 54: 1433–1438.
- Kingsolver, J. G., H. E. Hoekstra, J. M. Hoekstra, D. Berrigan, S. N. Vignieri, C. E. Hill, A. Hoang, P. Gibert, and P. Beerli 2001. The strength of phenotypic selection in natural populations. Am. Nat.. 157: 245–261.
- Lande, R. 1979. Quantitative genetic analysis of multivariate evolution, applied to brain:body size allometry. Evolution. 33: 402–416.
- Lande, R., and S. J. Arnold 1983. The measurement of selection on correlated characters. Evolution. 37: 1210–1226.
- Littell, R. C., G. A. Milliken, W. W. Stroup, and R. D. Wolfinger 1996. SAS system for mixed models. SAS Institute, Cary , NC .
- Lynch, M. 1999. Estimating genetic correlations in natural populations. Genet. Res. Camb.. 74: 255–264.
- Lynch, M., and B. Walsh 1998. Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland , MA .
-
Mazer, S. J.
1987. The quantitative genetics of life history and fitness components in Raphanus raphanistrum L. (Brassicaceae): ecological and evolutionary consequences of seed-weight variation.
Am. Nat.. 130: 891–914.
10.1086/284754 Google Scholar
- Mazer, S. J., and C. T. Schick 1991. Constancy of population parameters for life-history and floral traits in Raphanus sativus L. II. Effects of planting density on phenotype and heritability estimates. Evolution. 45: 1888–1907.
- Mazer, S. J., and L. M. Wolfe 1992. Planting density influences the expression of genetic variation in seed mass in wild radish (Raphanus sativus L., Brassicaceae). Am. J. Bot.. 79: 1185–1193.
- Mitchell-Olds, T. 1986. Quantitative genetics of survival and growth in Impatiens capensis. Evolution. 40: 107–116.
- Montalvo, A. M., and R. G. Shaw 1994. Quantitative genetics of sequential life-history and juvenile traits in the partially selfing perennial, Aquilegia caerulea. Evolution. 48: 828–841.
- Morgan, M. T., and J. K. Conner 2001. Using genetic markers to directly estimate male selection gradients. Evolution. 55: 272–281.
- Mousseau, T. A., and D. A. Roff 1987. Natural selection and the heritability of fitness components. Heredity. 59: 181–197.
- Murcia, C. 1990. Effect of floral morphology and temperature on pollen receipt and removal in Ipomoea trichocarpa. Ecology. 71: 1098–1109.
- Palmer, A. R. 2000. Quasireplication and the contract of error: Lessons from sex ratios, heritabilities and fluctuating asymmetry. Annu. Rev. Ecol. Syst.. 31: 441–480.
- Panetsos, C. A., and H. G. Baker 1967. The origin of variation in “wild” Raphanus sativus (Cruciferae) in California. Genetics. 38: 243–274.
- Phillips, P. C., and S. J. Arnold 1999. Hierarchical comparison of genetic variance-covariance matrices. I. Using the Flury hierarchy. Evolution. 53: 1506–1515.
- Reale, D., and D. A. Roff 2001. Estimating genetic correlations in natural populations in the absence of pedigree information: Accuracy and precision of the Lynch Method. Evolution. 55: 1249–1255.
- Riska, B., T. Prout, and M. Turelli 1989. Laboratory estimates of heritabilities and genetic correlations in nature. Genetics. 123: 865–871.
- Ritland, K. 1996. A marker-based method for inferences about quantitative inheritance in natural populations. Evolution. 50: 1062–1073.
-
Roach, D. A., and
R. D. Wulff
1987. Maternal effects in plants.
Annu. Rev. Ecol. Syst.. 18: 209–235.
10.1146/annurev.es.18.110187.001233 Google Scholar
-
Roff, D. A.
1997. Evolutionary quantitative genetics. Chapman and Hall,
New York
.
10.1111/j.0014-3820.2004.tb01726.x Google Scholar
- SAS Institute. 1999. SAS/STAT user's guide. Ver 8. SAS Institute, Cary , NC .
- Scheiner, S. 1993. Genetics and evolution of phenotypic plasticity. Annu. Rev. Ecol. Syst.. 24: 35–68.
- Schlichting, C. D. 1986. The evolution of phenotypic plasticity in plants. Annu. Rev. Ecol. Syst.. 17: 667–693.
- Schoen, D. J., G. Bell, and M. J. Lechowicz 1994. The ecology and genetics of fitness in forest plants. IV. Quantitative genetics of fitness components in Impatiens pallida (Balsaminaceae). Am. J. Bot.. 81: 232–239.
- Service, P. M., and M. R. Rose 1985. Genetic covariation among life-history components: The effect of novel environments. Evolution. 39: 943–945.
- Shaw, R. G. 1986. Response to density in a wild population of the perennial herb Salvia lyrata: variation among families. Evolution. 40: 492–505.
- 1991. The comparison of quantitative genetic parameters between populations. Evolution. 45: 143–151.
- Shaw, R. G., G. A. J. Platenkamp, F. H. Shaw, and R. H. Podolsky 1995. Quantitative genetics of response to competitors in Nemophila menziesiia field experiment. Genetics. 139: 397–406.
- Simons, A. M., and D. A. Roff 1994. The effect of environmental variability on the heritabilities of traits of a field cricket. Evolution. 48: 1637–1649.
- Snow, A. A. 1990. Effects of pollen-load size and number of donors on sporophyte fitness in wild radish (Raphanus raphanistrum). Am. Nat.. 136: 742–758.
- Stanton, M. L., A. A. Snow, and S. N. Handel 1986. Floral evolution: attractiveness to pollinators increases male fitness. Science. 232: 1625–1627.
- Steppan, S. J., P. C. Phillips, and D. Houle 2002. Comparative quantitative genetics: evolution of the G matrix. Trends Ecol. Evol.. 17: 320–327.
- Stratton, D. 1998. Reaction norm functions and QTL-environment interactions for flowering time in Arabidopsis thaliana. Heredity. 81: 144–155.
- Thiede, D. A. 1998. Maternal inheritance and its effect on adaptive evolution: a quantitative genetic analysis of maternal effects in a natural plant population. Evolution. 52: 998–1015.
- Weigensberg, I., and D. A. Roff 1996. Natural heritabilities: Can they be reliably estimated in the laboratory Evolution 50: 2149–2157.
- Williams, J. L., and J. K. Conner 2001. Sources of phenotypic variation in floral traits in wild radish, Raphanus raphanistrum (Brassicaceae). Am. J. Bot.. 88: 1577–1581.
- Wolfe, L. M., and S. C. H. Barrett 1989. Patterns of pollen removal and deposition in tristylous Pontederia cordata L. (Pontederi-aceae). Biol. J. Linn. Soc.. 36: 317–329.
- Wu, R. 1998. The detection of plasticity genes in heterogeneous environments. Evolution. 52: 967–977.
- Young, H. J., and M. L. Stanton 1990. Influences of floral variation on pollen removal and seed production in wild radish. Ecology. 71: 536–547.