SELECTION AND INBREEDING DEPRESSION: EFFECTS OF INBREEDING RATE AND INBREEDING ENVIRONMENT
William R. Swindell
Department of Biological Sciences, Bowling Green State University, Bowling Green, Ohio 43403
E-mail: [email protected]
Search for more papers by this authorJuan L. Bouzat
Department of Biological Sciences, Bowling Green State University, Bowling Green, Ohio 43403
E-mail: [email protected]
Search for more papers by this authorWilliam R. Swindell
Department of Biological Sciences, Bowling Green State University, Bowling Green, Ohio 43403
E-mail: [email protected]
Search for more papers by this authorJuan L. Bouzat
Department of Biological Sciences, Bowling Green State University, Bowling Green, Ohio 43403
E-mail: [email protected]
Search for more papers by this authorAbstract
Abstract The magnitude of inbreeding depression in small populations may depend on the effectiveness with which natural selection purges deleterious recessive alleles from populations during inbreeding. The effectiveness of this purging process, however, may be influenced by the rate of inbreeding and the environment in which inbreeding occurs. Although some experimental studies have examined these factors individually, no study has examined their joint effect or potential interaction. In the present study, therefore, we performed an experiment in which 180 lineages of Drosophila melanogaster were inbred at slow and fast inbreeding rates within each of three inbreeding environments (benign, high temperature, and competitive). The fitness of all lineages was then measured in a common benign environment. Although slow inbreeding reduced inbreeding depression in lineages inbred under high temperature stress, a similar reduction was not observed with respect to the benign or competitive treatments. Overall, therefore, the effect of inbreeding rate was nonsignificant. The inbreeding environment, in contrast, had a larger and more consistent effect on inbreeding depression. Under both slow and fast rates of inbreeding, inbreeding depression was significantly reduced in lineages inbred in the presence of a competitor D. melanogaster strain. A similar reduction of inbreeding depression occurred in lineages inbred under high temperature stress at a slow inbreeding rate. Overall, our findings show that inbreeding depression is reduced when inbreeding takes place in a stressful environment, possibly due to more effective purging under such conditions.
Literature Cited
- Armbruster, P., and D. G. Rogers. 2004. Does pollen competition reduce the cost of inbreeding Am. J. Bot. 91: 1939–1943.
- Armbruster, W. S., and D. H. Reed. 2005. Inbreeding depression in benign and stressful environments. Heredity 95: 235–242.
- Barlow, R. 1981. Experimental evidence for interactions between heterosis and environment in animals. Anim. Breeding Abstr. 49: 715–737.
- Bijlsma, R., J. Bundgaard, and W. F. Van Putten. 1999. Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. J. Evol. Biol. 12: 1125–1137.
- Bijlsma, R., J. Bundgaard, and A. C. Boerema. 2000. Does inbreeding affect the extinction risk of small populations? Predictions from Drosophila. J. Evol. Biol. 13: 502–514.
- Bochdanovits, Z., and G. De Jong. 2003. Temperature dependent larval resource allocation shaping adult body size in Drosophila melanogaster. J. Evol. Biol. 16: 1159–1167.
- Bubliy, O. A., V. Loeschcke, A. G. Imasheva. 2000. Effect of stressful and nonstressful growth temperatures on variation of sternopleural bristle number in Drosophila melanogaster. Evolution 54: 1444–1449.
- Charlesworth, B., and D. Charlesworth. 1999. The genetic basis of inbreeding depression. Genet. Res. Camb. 74: 329–340.
- Charlesworth, D., and B. Charlesworth. 1987. Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18: 237–268.
- Charlesworth, D., M. T. Morgan, and B. Charlesworth. 1990. Inbreeding depression, genetic load, and the evolution of outcrossing rates in a multilocus system with no linkage. Evolution 44: 1469–1489.
- Chen, X. 1993. Comparison of inbreeding and outbreeding in hermaphroditic Arianta arbustorum (L.) (land snail). Heredity 71: 456–461.
- Coyne, J. A., and E. Beecham. 1987. Heritability of two morphological characters within and among natural populations of Drosophila melanogaster. Genetics 117: 727–737.
- Crnokrak, P., and D. A. Roff. 1999. Inbreeding depression in the wild. Heredity 83: 260–270.
- Crow, J. F., and N. E. Morton. 1955. Measurement of gene frequency drift in small populations. Evolution 9: 202–214.
- David, J. R., C. Bocquet, and M. Louis-Scheemaeker. 1977. Genetic latitudinal adaptation of Drosophila melanogaster: new discriminative biometrical traits between European and equatorial African populations. Genet. Res. 30: 247–255.
- Day, S. B., E. H. Bryant, and L. M. Meffert. 2003. The influence of variable rates of inbreeding on fitness, environmental responsiveness, and evolutionary potential. Evolution 57: 1314–1324.
- del Castillo, R. 1998. Fitness consequences of maternal and nonmaternal components of inbreeding in the gynodioecious Phacelia dubia. Evolution 52: 44–60.
- Duarte, L. C., C. Bouteiller, P. Fontanillas, E. Petit, and N. Perrin. 2003. Inbreeding in the greater white-toothed shrew, Crocidura russula. Evolution 57: 638–645.
- Dudash, M. R. 1990. Relative fitness of selfed and outcrossed progeny in a self-compatible, protandrous species, Sabatia angularis L. (Gentianaceae): a comparison in three environments. Evolution 44: 1129–1139.
- Eckert, C. G., and S. C. H. Barrett. 1994. Inbreeding depression in partially self-fertilizing Decodon verticillatus (Lythraceae): population-genetic and experimental analyses. Evolution 48: 952–964.
- Edmands, S., and J. K. Deimler. 2004. Local adaptation, intrinsic coadaptation and the effects of environmental stress on interpopulation hybrids in the copepod Tigriopus californicus. J. Exp. Mar. Biol. Ecol. 303: 183–196.
- Ehiobu, N. G., M. E. Goddard, and J. F. Taylor. 1989. Effect of rate of inbreeding on inbreeding depression in Drosophila melanogaster. Theor. Appl. Genet. 77: 123–127.
- Falconer, D. S., and T. F. C. Mackay. 1996. Introduction to quantitative genetics. 4th ed. Longman, Harlow , U.K.
- Fernandez, A., M. Angel Toro, and C. Lopez-Fanjul. 1995. The effect of inbreeding on the redistribution of genetic variance of fecundity and viability in Tribolium castaneum. Heredity 75: 376–381.
- Fowler, K., and M. C. Whitlock. 1999. The variance in inbreeding depression and the recovery of fitness in bottlenecked populations. Proc. R. Soc. Lond. B. 266: 2061–2066.
- Frankham, R. 1995a. Inbreeding and extinction: a threshold effect. Conserv. Biol. 9: 792–799.
- Frankham, R.. 1995b. Effective population-size adult-population size ratios in wildlife: a review. Genet. Res. 66: 95–107.
- Frankham, R.. 2005. Stress and adaptation in conservation genetics. J. Evol. Biol. 18: 750–755.
- Frankham, R., L. P. Jones, and J. S. F. Barker. 1968. The effects of population size and selection intensity in selection for a quantitative character in Drosophila. I. Short-term response to selection. Genet. Res. Camb. 12: 237–248.
-
Frankham, R.,
J. D. Ballou, and
D. A. Briscoe. 2002. Introduction to conservation genetics. Cambridge Univ. Press,
Cambridge
,
U.K.
10.1046/j.1365-294X.2003.01702.x Google Scholar
- Fu, Y., G. Namkoong, and J. E. Carlson. 1998. Comparison of breeding strategies for purging inbreeding depression via simulation. Conserv. Biol. 12: 856–864.
- Gilchrist, A. S., and L. Partridge. 1999. A comparison of the genetic basis of wing size divergence in three parallel body size clines of Drosophila melanogaster. Genetics 153: 1775–1787.
- Glémin, S. 2003. How are deleterious mutations purged? Drift versus nonrandom mating. Evolution 57: 2678–2687.
- Goldstein, D. B., and A. G. Clark. 1995. Microsatellite variation in North American populations of Drosophila melanogaster. Nucleic Acid Res. 23: 3882–3886.
- Gram, W. K., and V. L. Sork. 2001. Association between environmental and genetic heterogeneity in forest tree populations. Ecology 82: 2012–2021.
- Haag, C. R., O. Sakwinska, and D. Ebert. 2003. Test of synergistic interaction between infection and inbreeding in Daphnia magna. Evolution 57: 777–783.
- Hayes, C. N., J. A. Winsor, and A. G. Stephenson. 2005. Environmental variation influences the magnitude of inbreeding depression in Cucurbita pepo ssp. texana (Cucurbitaceae). J. Evol. Biol. 18: 147–155.
- Henry, P. Y., R. Pradel, and P. Jarne. 2003. Environment-dependent inbreeding depression in a hermaphroditic freshwater snail. J. Evol. Biol. 16: 1211–1222.
- Hedrick, P. W. 1994. Purging inbreeding depression and the probability of extinction: full-sib mating. Heredity 73: 364–372.
- Hedrick, P. W.. 2000. Genetics of populations. 2nd ed. Jones and Bartlett, Sudbury , MA .
- Hoffmann, A. A., and P. A. Parsons. 1991. Evolutionary genetics and environmental stress. Oxford Univ. Press, Oxford , U.K.
- Husband, B. C., and S. C. H. Barrett. 1992. Effective population size and genetic drift in tristylous Eichhornia paniculata (Pontederiaceae). Evolution 46: 1875–1890.
- Husband, B. C., and D. W. Schemske. 1996. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50: 54–70.
- Jiménez, J. A., K. A. Hughes, G. Alaks, L. Graham, and R. C. Lacy. 1994. An experimental study of inbreeding depression in a natural habitat. Science 266: 271–273.
- Johnston, M. O. 1992. Effects of cross and self-fertilization on progeny fitness in Lobelia cardinalis and L. siphilitica. Evolution 46: 688–702.
- Jungen, H., and D. L. Hartl. 1979. Average fitness of populations of Drosophila melanogaster as estimated using compound-autosome strains. Evolution 33: 359–370.
- Kalinowski, S. T., P. W. Hedrick, and P. S. Miller. 1999. No inbreeding depression observed in Mexican and red wolf captive breeding programs. Conserv. Biol. 13: 1371–1377.
- Keller, L. F., and D. M. Waller. 2002. Inbreeding effects in wild populations. Trends Ecol. Evol. 17: 230–241.
- Keller, L. F., P. R. Grant, B. R. Grant, and K. Petren. 2002. Environmental conditions affect the magnitude of inbreeding depression in survival of Darwin's finches. Evolution 56: 1229–1239.
- Kondrashov, A. S., and D. Houle. 1994. Genotype-environment interactions and the estimation of the genomic mutation rate in Drosophila melanogaster. Proc. R. Soc. Lond. B 258: 221–227.
- Kristensen, T. N., J. Dahlgaard, and V. Loeschcke. 2003. Effects of inbreeding and environmental stress on fitness using Drosophila buzzatii as a model system. Conserv. Genet. 4: 453–465.
- Lande, R., and D. W. Schemske. 1985. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39: 24–40.
- Latter, B. D. H., J. C. Mulley, D. Reid, and L. Pascoe. 1995. Reduced genetic load revealed by slow inbreeding in Drosophila melanogaster. Genetics 139: 287–297.
- Lesbarreres, D., S. R. Primmer, A. Laurila, and J. Merilä. 2005. Environmental and population dependency of genetic variability-fitness correlations in Rana temporaria. Mol. Ecol. 14: 311–323.
- Lynch, M. 1988. Design and analysis of experiments on random drift and inbreeding depression. Genetics 120: 791–807.
- Lynch, M., and B. Walsh. 1998. Genetics and analysis of quantitative traits. Sinauer, Sunderland , MA .
- Mackay, T. F. C. 1980. Genetic variance, fitness, and homeostasis in varying environments: an experimental check of the theory. Evolution 34: 1219–1222.
- Meagher, S., D. J. Penn, and W. K. Potts. 2000. Male-male competition magnifies inbreeding depression in wild house mice. Proc. Natl. Acad. Sci. USA 97: 3324–3329.
- Miller, P. S. 1994. Is inbreeding depression more severe in a stressful environment Zoo Biol. 13: 195–208.
- Miller, P. S., and H. W. Hedrick. 2001. Purging of inbreeding depression and fitness decline in bottlenecked populations of Drosophila melanogaster. J. Evol. Biol. 14: 595–601.
- Nevo, E. 1978. Genetic variation in natural populations: patterns and theory. Theor. Popul. Biol. 13: 121–177.
- Pederson, D. G. 1968. Environmental stress, heterozygote advantage, and genotype-environment interaction in Arabidopsis. Heredity 23: 127–138.
- Pray, L. A., and C. J. Goodnight. 1995. Genetic variation in inbreeding depression in the red flour beetle Tribolium castaneum. Evolution 49: 176–188.
- Pray, L. A., C. J. Goodnight, L. Stevens, J. M. Schwartz, and G. Y. Yan. 1996. The effect of population size on effective population size: an empirical study in the red flour beetle Tribolium castaneum. Genet. Res. 68: 151–155.
- Pusey, A., and M. Wolf. 1996. Inbreeding avoidance in animals. Trends Ecol. Evol. 11: 201–206.
- Radwan, J. 2003. Inbreeding depression in fecundity and inbred line extinction in the bulb mite, Rhizoglyphus robini Heredity 90: 371–376.
- Ralls, K. P., P. H. Harvey, and A. M. Lyles. 1986. Inbreeding in natural populations of birds and mammals. Pp. 35–56 in M. E. Soulè, ed. Conservation biology. Sinauer Associates, Sunderland , MA .
- Reed, D. H. 2005. Relationship between population size and fitness. Conserv. Biol. 19: 560–568.
- Reed, D. H., and E. H. Bryant. 2001. Genetic load, fitness, and their relationship to purging in experimental populations of the housefly. Conserv. Genet. 2: 57–61.
- Reed, D. H., D. A. Briscoe, R. Frankham. 2002. Inbreeding and extinction: the effect of environmental stress and lineage. Conserv. Genet. 3: 301–307.
- Reed, D. H., E. H. Lowe, D. A. Briscoe, and R. Frankham. 2003a. Inbreeding and extinction: effects of inbreeding rate. Conserv. Genet. 4: 405–410.
- Reed, D. H., E. H. Lowe, D. A. Briscoe, and R. Frankham. 2003b. Fitness and adaptation in a novel environment: effect of inbreeding, prior environment, and lineage. Evolution 57: 1822–1828.
- Rich, S. S., and A. E. Bell. 1980. Genotype-environment interaction effects in long-term selected populations of Tribolium. J. Hered. 71: 319–322.
- Rowe, G., and T. J. Beebee. 2005. Intraspecific competition disadvantages inbred natterjack toad (Bufo calamita) genotypes over outbred ones in a shared pond environment. J. Anim. Ecol. 74: 71–76.
- Ruban, P. S., E. P. Cunningham, and P. M. Sharp. 1988. Heterosis × nutrition interaction in Drosophila melanogaster. Theor. Appl. Genet. 76: 136–142.
-
Sambrook, J.,
E. F. Fritsch, and
T. Maniatis. 1989. Molecular cloning: a laboratory manual. 2nd ed.
Cold Spring Harbor Laboratory Press,
Cold Spring Harbor
,
NY
.
10.1111/j.1095-8312.1996.tb01434.x Google Scholar
- Schlotterer, C., C. Vogl, and D. Tautz. 1997. Polymorphism and locus-specific effects on polymorphism at microsatellite loci in natural populations of Drosophila melanogaster populations. Genetics 146: 309–320.
- Schneller, J. J., and R. Holderegger. 1996. Genetic variation in small, isolated fern populations. J. Veg. Sci. 7: 113–120.
-
Sokal, R. R., and
F. J. Rohlf. 1995. Biometry. W. H. Freeman,
New York
.
10.1577/1548-8659(1986)115<149:LOPDOR>2.0.CO;2 Google Scholar
- Spielman, D., B. W. Brook, and R. Frankham. 2004. Most species are not driven to extinction before genetic factors impact them. Proc. Natl. Acad. Sci. 101: 15261–15264.
- Thornhill, N. 1993. The natural history of inbreeding and outbreeding: theoretical and empirical perspectives. Univ. of Chicago Press, Chicago .
- Visscher, P. M., D. Smith, S. J. G. Hall, and J. L. Williams. 2001. A viable herd of genetically uniform cattle. Nature 409: 303.
- Wade, M. J. 1980. Effective population size: the effects of sex, genotype, and density on the mean and variance of offspring numbers in the flour beetle, Tribolium castaneum. Genet. Res. 36: 1–10.
- Walter, H. S. 1990. Small viable population: the red-tailed hawk of Socorro Island. Conserv. Biol. 4: 441–443.
- Wang, J. 2000. Effects of population structures and selection strategies on the purging of inbreeding depression due to deleterious mutations. Genet. Res. Camb. 76: 75–86.
- Wang, J. W., G., Hill, D., Charlesworth, and B. Charlesworth. 1999. Dynamics of inbreeding depression due to deleterious mutations in small populations: mutation parameters and inbreeding rate. Genet. Res. Camb. 74: 168–178.
- Weber, K. E. 1990. Increased selection response in larger populations. I. Selection for wing-tip height in Drosophila melanogaster at three population sizes. Genetics 125: 579–584.
- Weber, K. E.. 1996. Large genetic change at small fitness cost in large populations of Drosophila melanogaster selected for wind tunnel flight: rethinking fitness surfaces. Genetics 144: 205–213.
- Willis, J. H. 1999. The role of genes of large effect on inbreeding depression in Mimulus guttatus. Evolution 53: 1678–1691.
- Windig, J. J., R. F. Veerkamp, and S. Nylin. 2004. Quantitative genetic variation in an island population of the speckled wood butterfly (Pararge aegeria). Heredity 93: 450–454.
- Wokac, R. M. 2003. On the importance of inbreeding at Tauernschecken goats. Arch. Tierzucht. 46: 455–469.
- Wool, D., and E. Sverdlov. 1976. Sib-mating populations in an unpredictable environment: effects on components of fitness. Evolution 30: 119–129.
- Wu, H. X., A. C. Matheson, and A. Abarquez. 2002. Inbreeding in Pinus radiate. IV. The effect of inbreeding on wood density. Ann. For. Sci. 59: 557–562.
- Wright, S., and W. E. Kerr. 1954. Experimental studies of the distribution of gene frequencies in very small populations of Drosophila melanogaster. II. Bar. Evolution 8: 225–240.
- Young, T. P. 1994. Natural die-offs of large mammals: implications for conservation. Conserv. Biol. 8: 410–418.