HOW CLOSELY CORRELATED ARE MOLECULAR AND QUANTITATIVE MEASURES OF GENETIC VARIATION? A META-ANALYSIS
David H. Reed
Key Centre for Biodiversity and Bioresources, Department of Biological Sciences, Macquarie University, New South Wales 2109, Australia. E-mail: [email protected]
Search for more papers by this authorRichard Frankham
Key Centre for Biodiversity and Bioresources, Department of Biological Sciences, Macquarie University, New South Wales 2109, Australia. E-mail: [email protected]
Search for more papers by this authorDavid H. Reed
Key Centre for Biodiversity and Bioresources, Department of Biological Sciences, Macquarie University, New South Wales 2109, Australia. E-mail: [email protected]
Search for more papers by this authorRichard Frankham
Key Centre for Biodiversity and Bioresources, Department of Biological Sciences, Macquarie University, New South Wales 2109, Australia. E-mail: [email protected]
Search for more papers by this authorAbstract
Abstract.— The ability of populations to undergo adaptive evolution depends on the presence of quantitative genetic variation for ecologically important traits. Although molecular measures are widely used as surrogates for quantitative genetic variation, there is controversy about the strength of the relationship between the two. To resolve this issue, we carried out a meta-analysis based on 71 datasets. The mean correlation between molecular and quantitative measures of genetic variation was weak (r = 0.217). Furthermore, there was no significant relationship between the two measures for life-history traits (r =−0.11) or for the quantitative measure generally considered as the best indicator of adaptive potential, heritability (r =−0.08). Consequently, molecular measures of genetic diversity have only a very limited ability to predict quantitative genetic variability. When information about a population's short-term evolutionary potential or estimates of local adaptation and population divergence are required, quantitative genetic variation should be measured directly.
Literature Cited
- Allegrucci, G., D. Cesaroni, and V. Sbordoni. 1987. Adaptation and speciation of Dolichopoda cave crickets (Orthoptera, Rhaphi-dophoridae): geographic variation of morphometric indices and allozyme frequencies. Biol. J. Linn. Soc. 31: 151–160.
- Allendorf, F. W., and R. F. Leary. 1986. Heterozygosity and fitness in natural populations of animals. Pp. 57–76 in M. E. Soulé, ed. Conservation biology: the science of scarcity and diversity. Sinauer, Sunderland , MA .
- Allendorf, F. W., D. Bayles, D. L. Bottom, K. P. Currens, C. A. Frissell, D. Hankin, J. A. Lichatowich, W. Nehlsen, P. C. Trotter, and T. H. Williams. 1997. Prioritizing Pacific salmon stocks for conservation. Conserv. Biol. 11: 140–152.
- Aquadro, C. F., and C. W. Kilpatrick. 1981. Morphological and biochemical variation and differentiation in insular and mainland deer mice. Pp. 215–229 in M. H. Smith and J. Joule, eds. Mammalian population genetics. Univ. of Georgia Press, Athens , GA .
- Armbruster, P., W. E. Bradshaw, and C. M. Holzapfel. 1998. Effects of postglacial range expansion on allozyme and quantitative genetic variation of the pitcher-plant mosquito, Wyeomyia smithii. Evolution 52: 1697–1704.
- Arnqvist, G., and D. Wooster. 1995. Meta-analysis: synthesizing research findings in ecology and evolution. Trends Ecol. Evol. 10: 236–240.
- Ashley, M. V., and C. Wills. 1989. Mitochondrial-DNA and allozyme divergence patterns are correlated among island deer mice. Evolution 43: 646–650.
- Avise, J. C., and G. C. Johns. 1999. Proposal for a standardized temporal scheme of biological classification for extant species. Proc. Natl. Acad. Sci. USA 96: 7358–7363.
- Ballou, J., and R. C. Lacy. 1995. Identifying genetically important individuals for management of genetic diversity in pedigreed populations. Pp. 76–111 in J. Ballou, M. Gilpin, and T. Foose, eds. Population management for survival and recovery: analytical methods and strategies in small population conservation. Columbia Univ. Press, New York .
- Beacham, T. D., and R. E. Withler. 1985. Heterozygosity and morphological variability of pink salmon (Oncorhynchus gorbuscha) from southern British Columbia and Puget Sound. Can. J. Genet. Cytol. 27: 571–579.
- Berwaerts, K., H. Van Dyck, S. Van Dongen, and E. Matthysen. 1998. Morphological and genetic variation in the speckled wood butterfly (Pararge aegeria L.) among differently fragmented landscapes. Neth. J. Zool. 48: 241–253.
- Briscoe, D. A., J. M. Malpica, A. Robertson, G. J. Smith, R. Frankham, R. G. Banks, and J. S. F. Barker. 1992. Rapid loss of genetic variation in large captive populations of Drosophila flies: implications for the genetic management of captive populations. Conserv. Biol. 6: 416–425.
- Britten, H. B. 1996. Meta-analyses of the association between multilocus heterozygosity and fitness. Evolution 50: 2158–2164.
- Bryant, E. H. 1984. A comparison of electrophoretic and morphometric variability in the face fly, Musca autumnalis. Evolution 38: 455–458.
- Bryant, E. H., S. A. McCommas, and L. M. Combs. 1986. The effect of an experimental bottleneck upon quantitative genetic variation in the housefly. Genetics 114: 1191–1211.
- Bryant, E. H., V. L. Backus, M. E. Clark, and D. H. Reed. 1999. Experimental tests of captive breeding for endangered species. Conserv. Biol. 13: 1487–1496.
- Bush, G. L., S. M. Case, A. C. Wilson, and J. L. Patton. 1977. Rapid speciation and chromosomal evolution in mammals. Proc. Natl. Acad. Sci. 74: 3942–3946.
- Butlin, R. K., and T. Tregenza. 1998. Levels of genetic polymorphism: marker loci versus quantitative traits. Phil. Trans. R. Soc. Lond. B 353: 187–198.
- Chakraborty, R. 1981. The distribution of the number of heterozygous loci in an individual in natural populations. Genetics 98: 466–477.
- Cherry, L. M., S. M. Case, and A. C. Wilson. 1978. Frog perspective on the morphological difference between humans and chimpanzees. Science 200: 209–211.
- Cheverud, J., E. Routman, C. Jaquish, S. Tardif, G. Peterson, N. Belfiore, and L. Forman. 1994. Quantitative and molecular genetic variation in captive cotton-top tamarins (Saguinus oedipus). Conserv. Biol. 8: 95–104.
- Cheverud, J. M., T. T. Vaughn, L. S. Pletscher, K. King-Ellison, J. Bailiff, E. Adams, C. Erickson, and A. Bonislawski. 1999. Epistasis and the evolution of additive genetic variance in populations that pass through a bottleneck. Evolution 53: 1009–1018.
- Colli, G. R., A. K. Peres Jr., and H. J. Da Cunha. 1998. A new species of Tupinambis (Squamata: Teiidae) from central Brazil, with an analysis of morphological and genetic variation in the genus. Herpetologica 54: 477–492.
- Coyne, J. A., and H. A. Orr. 1989. Patterns of speciation in Drosophila. Evolution 43: 362–381.
- Coyne, J. A., and H. A. Orr. 1997. “Patterns of speciation in Drosophila” revisited. Evolution 51: 295–303.
- Crandall, K. A., O. R. P. Bininda-Emonds, G. M. Mace, and R. K. Wayne. 2000. Considering evolutionary processes in conservation biology. Trends Ecol. Evol. 15: 290–295.
- Crnokrak, P., and D. A. Roff. 1995. Dominance variance: associations with selection and fitness. Heredity 75: 530–540.
- Dennison, M. D., and A. J. Baker. 1991. Morphometric variability in continental and Atlantic island populations of chaffinches (Fringilla coelebs). Evolution 45: 29–39.
- Falconer, D. S. 1989. Introduction to quantitative genetics. 3rd ed. Longman Scientific and Technical, New York .
- Felsenstein, J. 1986. Population differences in quantitative characters and gene frequencies: a comment on papers by Lewontin and Rogers. Am. Nat. 127: 731–732.
- Frankham, R. 1995. Conservation genetics. Annu. Rev. Genet. 29: 305–327.
- Franklin, I. R. 1980. Evolutionary change in small populations. Pp. 135–150 in M. E. Soulé and B. A. Wilcox, eds. Conservation biology: an evolutionary-ecological perspective. Sinauer, Sunderland , MA .
- Futuyma, D. J. 1998. Evolutionary biology. 3rd ed. Sinauer, Sunderland , MA .
- Griffith, B., J. M. Scott, J. W. Carpenter, and C. Reed. 1989. Trans-location as a species conservation tool: status and strategy. Science 245: 477–480.
- Gurevitch, J., L. L. Morrow, A. Wallace, and J. S. Walsh. 1992. A meta-analysis of competition in field experiments. Am. Nat. 140: 539–572.
-
Haig, S. M., and
J. C. Avise. 1996. Avian conservation genetics. Pp.
160–189
in
J. C. Avise and
J. L. Hamrick, eds.
Conservation genetics: case histories from nature. Chapman and Hall,
New York
.
10.1007/978-1-4757-2504-9_6 Google Scholar
- Hard, J. H. 1995. A quantitative genetic perspective on the conservation of intraspecific diversity. Am. Fish. Soc. Symp. 17: 304–326.
- Hedrick, P. W. 1999. Highly variable loci and their interpretation in evolution and conservation. Evolution 53: 313–318.
- Hedrick, P. W., and O. Savolainen. 1996. Molecular and adaptive variation: a perspective for endangered species. Pp. 92–102 in J. Maschinski, D. H. Hammond, and L. Holter, eds. Southwestern rare and endangered plants: proceedings of the second conference. U.S. Dept. of Agriculture, Forest Service, Rocky Mt. Forest and Range Experiment Station, Fort Collins , CO .
- Houle, D. 1989. Allozyme associated heterosis in Drosophila melanogaster. Genetics 123: 789–801.
- Houle, D., B. Morikawa, and M. Lynch. 1996. Comparing mutational variabilities. Genetics 143: 1467–1483.
- Hunter, J. E., and F. L. Schmidt. 1990. Methods of meta-analysis: correcting errors and bias in research findings. Sage, Newbury Park , CA .
- Jain, S. K., L. Wu, and K. R. Vaidya. 1980. Levels of morphological and allozyme variation in Indian amaranths: a striking contrast. J. Hered. 71: 283–285.
- Karhu, A., P. Hurme, M. Karjalainen, P. Karvonen, K. Kärkkäinen, and O. Savolainen. 1996. Do molecular markers reflect patterns of differentiation in adaptive traits of conifers Theor. Appl. Genet. 93: 215–221.
- King, M. C., and A. C. Wilson. 1975. Evolution at two levels in humans and chimpanzees. Science 188: 107–116.
- Knapp, E. E., and K. J. Rice. 1998. Comparison of isozymes and quantitative traits for evaluating patterns of genetic variation in purple needlegrass (Nasella pulchra). Conserv. Biol. 12: 1031–1041.
- 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. Sci. USA 97: 698–703.
- Lande, R. 1982. A quantitative genetic theory of life history evolution. Ecology 63: 607–615.
-
Lande, R., and
G. R. Barrowclough. 1987. Effective population size, genetic variation, and their use in population management. Pp.
87–123
in
M. E. Soulé, ed.
Viable populations in conservation. Sinauer Associates,
Sunderland
,
MA
.
10.1017/CBO9780511623400.007 Google Scholar
- Lerner, I. M. 1954. Genetic homeostasis. Oliver and Boyd, Edinburgh .
- Lewontin, R. C. 1984. Detecting population differences in quantitative characters as opposed to gene frequencies. Am. Nat. 123: 115–124.
-
Light, R. J., and
D. B. Pillemer. 1984. Summing up: the science of reviewing research. Harvard Univ. Press,
Cambridge
,
MA
.
10.4159/9780674040243 Google Scholar
- Lónn, M., and H. C. Prentice. 1990. Mosaic variation in Swedish Petrorhagia prolifera (Caryophyllaceae): the partitioning of morphometric and electrophoretic diversity. Biol. J. Linn. Soc. 41: 353–373.
- Lopez-Fanjul, C., and W. G. Hill. 1973. Genetic differences between populations of Drosophila melanogaster for a quantitative trait. II. Wild and laboratory populations. Genet. Res. 22: 69–78.
- Lopez-Fanjul, C., and A. Villaverde. 1989. Inbreeding increases genetic variation for viability in Drosophila melanogaster. Evolution 43: 1800–1804.
- Lynch, M. 1996. A quantitative-genetic perspective on conservation issues. Pp. 471–501 in J. C. Avise and J. L. Hamrick, eds. Conservation genetics: case histories from nature. Chapman and Hall, New York .
- Lynch, M. 1999. Estimating genetic correlations in natural populations. Genet. Res. 74: 255–264.
- Lynch, M., M. Pfrender, K. Spitze, N. Lehman, J. Hicks, D. Allen, L. Latta, M. Ottene, F. Bogue, and J. Colbourne. 1999. The quantitative and molecular genetic architecture of a subdivided species. Evolution 53: 100–110.
- Mammuris, Z., A. P. Apostolidis, A. Triantafyllidis, P. S. Economidis, and C. Triantaphyllidis. 1998. Relationship between morphological and genetic variation in red mullet (Mullus bar-batus) populations from Greek seas. Folia Zool. 47: 295–303.
- Mather, K. 1973. Genetical structure of populations. Chapman and Hall, London .
- McClenaghan, L. R., Jr., and M. S. Gaines. 1981. Genic and morphological variability in central and marginal populations of Sigmodon hipsidus. Pp. 202–213 in M. H. Smith and J. Joule, eds. Mammalian population genetics. Univ. of Georgia Press, Athens , GA .
- Merilä, J. 1997. Quantitative trait and allozyme divergence in the greenfinch (Carduelis chloris, Aves: Fringillidae). Biol. J. Linn. Soc. 61: 243–266.
- Merilä, J., and B. C. Sheldon. 2000. Lifetime reproductive success and heritability in nature. Am. Nat. 155: 301–310.
- Moran, P., and I. Kornfield. 1993. Retention of ancestral polymorphism in the mbuna species flock (Teleostei: Cichlidae). Mol. Biol. Evol. 10: 1015–1029.
-
Nei, M.
1987. Molecular evolutionary genetics. Columbia Univ. Press,
New York
.
10.1111/j.1365-294X.2006.02908.x Google Scholar
-
Nevo, E.,
D. Zohary,
A. H. D. Brown, and
M. Haber. 1979. Genetic diversity and environmental associations of wild barley, Hordeum spontaneum, in Israel.
Evolution
33: 815–833.
10.1111/j.1558-5646.1979.tb04737.x Google Scholar
- O'Brien, S. J., M. E. Roelke, L. Marker, A. Newman, C. A. Winkler, D. Meltzer, L. Colly, J. F. Evermann, M. Bush, and D. E. Wildt. 1985. Genetic basis for species vulnerability in the cheetah. Science 227: 1428–1434.
- Oosterhout, C. van 1998. Captive metapopulations of the butterfly Bicyclus anynana. Ph.D. diss., University of Leiden, Leiden, the Netherlands.
- Oostermeijer, J. G. B., M. W. van Eijck, N. C. van Leeuwen, and J. C. M. den Nijs. 1995. Analysis of relationship between allozyme heterozygosity and fitness in the rare Gentiana pneumonthe L. J. Evol. Biol. 8: 739–759.
- Ouborg, N. J., and R. Van Treuren. 1995. Variation in fitness-related characters among small and large populations of Salvia pratensis. J. Ecol. 83: 369–380.
- Patterson, C., D. M. Williams, and C. J. Humphries. 1993. Congruence between molecular and morphological phylogenies. Annu. Rev. Ecol. Syst. 24: 153–188.
- Patton, J. L., S. Y. Yang, and P. Myers. 1975. Genetic and morphological divergence among introduced rat populations (Rattus rattus) of the Galapagos archipelago, Ecuador. Syst. Zool. 24: 296–310.
- Prentice, H. C. 1992. The structure of morphometric and allozyme variation in relict populations of Gypsophila fastigiata (Caryophyllaceae) in Sweden. Biol. J. Linn. Soc. 47: 197–216.
- Price, S. C., K. M. Shumaker, A. L. Kahler, R. W. Allard, and J. E. Hill. 1984. Estimates of population differentiation obtained from enzyme polymorphisms and quantitative characters. J. Hered. 75: 141–142.
- Rabbani, M. A., Y. Murakami, Y. Kuginuki, and K. Takayanagi. 1998. Genetic variation in radish (Raphanus sativus L.) germplasm from Pakistan using morphological traits and RAPDs. Genet. Res. Crop Evol. 45: 307–316.
- Reed, D. H. 1998. Population size, selection, and mutation-accumulation. Ph.D. diss., University of Houston, Houston, TX.
- Ritland, K. 1996. A marker-based method for inferences about quantitative inheritance in natural populations. Evolution 50: 1062–1073.
- Rogers, A. R. 1986. Population differences in quantitative characters as opposed to gene frequencies. Am. Nat. 127: 729–730.
- Rundle, H. D., L. Nagel, J. W. Boughman, and D. Schluter. 2000. Natural selection and parallel speciation in sympatric sticklebacks. Science 287: 306–307.
- Ryman, N., U. Lagercrantz, L. Andersson, R. Chakraborty, and R. Rosenberg. 1984. Lack of correspondence between genetic and morphologic variability patterns in Atlantic herring (Clupea harengus). Heredity 53: 687–704.
- Saccheri, I. J., P. M. Brakefield, and R. A. Nichols. 1996. Severe inbreeding depression and rapid fitness rebound in the butterfly Bicyclus anynana (Satyridae). Evolution 50: 2000–2013.
- Saccheri, I. J., I. J. Wilson, R. A. Nichols, M. W. Bruford, and P. M. Brakefield. 1999. Inbreeding of bottlenecked butterfly populations: estimation using the likelihood of changes in marker allele frequencies. Genetics 151: 1053–1063.
- Schnell, G. D., and R. K. Selander. 1981. Environmental and morphological correlates of genetic variation in mammals. Pp. 60–99 in M. H. Smith and J. Joule, eds. Mammalian population genetics. Univ. of Georgia Press, Athens .
- Schnell, G. D., T. L. Best, and M. L. Kennedy. 1978. Interspecific morphologic variation in kangaroo rats (Dipodomys): degree of concordance with genic variation. Syst. Zool. 27: 34–48.
- Schwaegerle, K. E., K. Garbutt, and F. A. Bazzaz. 1986. Differentiation among nine populations of Phlox. I. Electrophoretic and quantitative variation. Evolution 40: 506–517.
- Simonsen, V. 1976. Electrophoretic studies on the blood proteins of domestic dogs and other Canidae. Hereditas 82: 7–18.
- Slatkin, M. 1987. Gene flow and the geographic structure of natural populations. Science 236: 787–792.
-
Sokal, R. R., and
F. J. Rohlf. 1995. Biometry. 3rd ed.
W. H. Freeman,
San Fransisco
,
CA
.
10.1577/1548-8659(1986)115<149:LOPDOR>2.0.CO;2 Google Scholar
- Soulé, M. E., and S. Y. Yang. 1973. Genetic variation in the side-blotched lizards on islands in the Gulf of California. Evolution 27: 593–600.
- Soulé, M. E., and G. P. Zegers. 1996. Phenetics of natural populations. V. Genetic correlates of phenotypic variation in the pocket gopher (Thomomys bottae) in California. J. Hered. 87: 341–350.
-
Soulé, M. E.,
S. Y. Yang,
M. G. Weiler, and
G. C. Gorman. 1973. Island lizards: the genetic-phenetic variation correlation.
Nature
242: 190–192.
10.1038/242191a0 Google Scholar
- Spitze, K. 1993. Population structure in Daphnia obtusa: quantitative genetic and allozyme variation. Genetics 135: 367–374.
- Strauss, R. E. 1989. Associations between genetic heterozygosity and morphological variability in freshwater sculpins, genus Cottus (Teleostei: Cottidae). Biochem. Syst. Ecol. 17: 333–340.
- Strauss, R. E. 1991. Correlations between heterozygosity and phenotypic variability in Cottus (Teleostei: Cottidae) character components. Evolution 45: 1950–1956.
- Wade, M. J., S. M. Shuster, and L. Stevens. 1996. Inbreeding: its effect on response to selection for pupal weight and the heritable variance in fitness in the flour beetle, Tribolium castaneum. Evolution 50: 723–733.
- Waldmann, P., and S. Andersson. 1998. Comparison of quantitative genetic variation and allozyme diversity within and between populations of Scabiosa canescens and S. columbaria. Heredity 81: 79–86.
- Wayne, R. K., S. B. George, D. Gilbert, P. W. Collins, S. D. Kovach, D. Girman, and N. Lehman. 1991. A morphological and genetic study of the island fox, Urocyon littoralis. Evolution 45: 1849–1868.
- Yezerinac, S. M., S. C. Lougheed, and P. Handford. 1992. Morphological variability and enzyme heterozygosity: individual and population level correlations. Evolution 46: 1959–1964.
- Zink, R. M., M. F. Smith, and J. L. Patton. 1985. Associations between heterozygosity and morphological variance. J. Hered. 76: 415–420.