The maintenance of genetic variability by mutation in a polygenic character with linked loci

Lande, Russell

doi:10.1017/s0016672300016037

Cited by 736 publications

(282 citation statements)

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“…The ectotherm and endotherm data are from this study and are based upon the median by trait data set. The Drosophila data are derived from Roff and Mousseau (1987) and is based upon the median by study data set There are many factors which may be responsible for the maintenance of genetic variance of fitness characters, The rate of origin of variation by mutation alone may be sufficient to maintain substantial additive genetic variance within natural populations (Lande, 1976;Turelli, 1984). Heterozygote advantage (Falconer, 1981), frequency dependent selection (Bulmer, 1980), variable selection in heterogeneous environments (Ewing, 1979), diversifying selection (Thoday, 1972), and migration (Felsenstein, 1976) have been proposed as possible mechanisms for the sustenance of genetic variation.…”

Section: Discussionmentioning

confidence: 99%

“…However, these data are rather few and derived primarily from domestic animals, which may be partly inbred. Extension to wild, outbred organisms may be erroneous.It is possible that some significant amount of additive genetic variance can be maintained within natural populations, even for characters tightly connected to fitness; possible mechanisms include mutation (Lande, 1976; Turelli, 1984), heterozygote advantage (Falconer, 1981), frequency dependence (Bulmer, 1980), fluctuating environments (Ewing, 1979) and migration (Felsenstein, 1976). In addition, zero additive genetic variance in fitness is consistent with positive heritability estimates of fitness components when there exists negative genetic correlations between components (Rose and Charlesworth, 1981).…”

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confidence: 99%

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Natural selection and the heritability of fitness components

1987

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The hypothesis that traits closely associated with fitness will generally possess lower heritabilities than traits more loosely connected with fitness is tested using 1120 narrow sense heritability estimates for wild, outbred animal populations, collected from the published record. Our results indicate that life history traits generally possess lower heritabilities than morphological traits, and that the means, medians, and cumulative frequency distributions of behavioural and physiological traits are intermediate between life history and morphological traits. These findings are consistent with popular interpretations of Fisher's (1930Fisher's ( , 1958 Fundamental Theorem of Natural Selection, and Falconer (1960, 1981), but also indicate that high heritabilities are maintained within natural populations even for traits believed to he under strong selection. It is also found that the heritability of morphological traits is significantly lower for ectotherms than it is for endotherms which may in part be a result of the strong correlation between life history and body size for many ectotherms. INTRODUCTIONThe fundamental theorem of natural selection states: "The rate of increase in fitness of any organism at any time is equal to its genetic variance in fitness at that time" (Fisher, 1930). Fisher's theorem is axiomatic to much of current evolutionary research. It has been variously interpreted but is generally construed to imply that traits that have been closely and consistently associated with fitness will exhibit low additive genetic variances as a result of natural selection (e.g., Hegmann and Dingle, 1982; Lynch and Sulzbach, 1984; Riddel et cii., 1981). However, the validity of the fundamental theorem is dependent upon many assumptions that may not usually be met by natural populations (e.g., population equilibrium, weak selection, constancy of genotypic fitnesses over time, and independence of genotypic frequencies) (Charlesworth, 1987). The maintenance of low additive genetic variance has also been inferred to imply low heritability (in the narrow sense); "On the whole, characters with the lowest heritabilities are those most closely connected with fitness, while characters with the highest heritabilities are those that might be judged on biological grounds to be the least important as determinants of natural selection." (Falconer, 1960(Falconer, , 1981.) The most extensive compilation of data in support of this view is that presented in table 10.1 of Falconer (1981). However, these data are rather few and derived primarily from domestic animals, which may be partly inbred. Extension to wild, outbred organisms may be erroneous.It is possible that some significant amount of additive genetic variance can be maintained within natural populations, even for characters tightly connected to fitness; possible mechanisms include mutation (Lande, 1976; Turelli, 1984), heterozygote advantage (Falconer, 1981), frequency dependence (Bulmer, 1980), fluctuating environments (Ewing, 1979) and migration (Felsenstein, 197...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Natural selection and the heritability of fitness components

1987

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“…Two perspectives on the evolutionary stability of the G matrix provide contrasting views on treating G as a constant over evolutionary time, a proposition first suggested by Lande (1975Lande ( , 1979Lande ( , 1980a. According to one perspective, G may fluctuate erratically through time, reflecting change in underlying gene frequencies (Turelli 1988;Shaw et al 1995;Roff 2000) or in genes of major effect (Agrawal et al 2001).…”

Section: Methodological Considerationsmentioning

confidence: 99%

MIPoD: A Hypothesis‐Testing Framework for Microevolutionary Inference from Patterns of Divergence

Hohenlohe¹,

Arnold²

2008

The American Naturalist

119

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Despite the many triumphs of comparative biology during the past few decades, the field has remained strangely divorced from evolutionary genetics. In particular, comparative methods have failed to incorporate multivariate process models of microevolution that include genetic constraint in the form of the G matrix. Here we explore the insights that might be gained by such an analysis. A neutral model of evolution by genetic drift that depends on effective population size and the G matrix predicts a probability distribution for divergence of population trait means on a phylogeny. Use of a maximum likelihood (ML) framework then allows us to compare independent direct estimates of G with the ML estimates based on the observed pattern of trait divergence among taxa. We assess the departure from neutrality, and thus the role of different types of selection and other forces, in a stepwise hypothesis-testing procedure based on parameters for the size, shape, and orientation of G. We illustrate our approach with a test case of data on vertebral number evolution in garter snakes. KeywordsG matrix; genetic line of least resistance; maximum likelihood; selective line of least resistance; Thamnophis; vertebral number A large literature on the comparative analysis of evolving traits has blossomed during the past 25 years (Felsenstein 1985;Harvey and Pagel 1991;Lynch 1991;Martins and Garland 1991;Martins 1994Martins , 2000Rohlf 2001;Steppan 2004;Carvalho et al. 2005). Interest in tracing trait evolution on independently estimated phylogenies has been responsible for putting a new face on comparative biology. New methodologies have allowed investigators to assay statistical associations between trait values and putative selective pressures (e.g., Darst et al. 2005;Ord and Martins 2006;Strmberg 2006) and to test alternative models of evolutionary process (Hansen 1997;Butler and King 2004). Despite success on these and other fronts, the new comparative biology has been strangely divorced from evolutionary genetics. Process models have been adopted from evolutionary genetics to provide the substructure for statistical inference (Martins and Hansen 1997), but estimates of genetic parameters usually play no role in comparative biology. The divorce between comparative biology and evolutionary genetics is especially vivid in the case of continuously distributed phenotypic traits. For these kinds of traits, which are often polygenic, quantitative genetic models promise deep understanding of

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“…In particular, mutationselection models 12 and the neutral theory of evolution 13 indicate that the strength of stabilizing selection is an important determinant of standing levels of variation. All else being equal, weaker stabilizing selection is expected to maintain higher levels of variation than stronger stabilizing selection.…”

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Regulatory evolution across the protein interaction network

2004

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Protein-protein interactions may impose constraints on both structural and regulatory evolution. Here we show that protein-protein interactions are negatively associated with evolutionary variation in gene expression. Moreover, interacting proteins have similar levels of variation in expression, and their expression levels are positively correlated across strains. Our results suggest that interacting proteins undergo similar evolutionary dynamics, and that their expression levels are evolutionarily coupled. These patterns hold for organisms as diverse as budding yeast and fruit flies.Recent studies on variation in gene expression in natural populations indicate that a number of factors influence regulatory evolution, including membership in a particular functional class or biological process 1 and the pattern of sex-biased expression 2,3 . Protein-protein interactions may also be relevant to regulatory evolution if they mean that the interacting partners of a given protein impose stricter stoichiometric requirements. For proteins that participate in complexes, such requirements may result in increased selection pressure to maintain evolutionarily stable expression levels and might be manifested in a negative association between evolutionary variation in gene expression and the number of protein interactions.We analyzed variation in expression of 5,978 yeast (Saccharomyces cerevisiae) genes among four natural isolates grown under identical laboratory conditions 4 , of 4,439 fly (Drosophila melanogaster) genes in adult males from eight wild-type strains of geographically diverse origin 2 and of a similar number of genes assayed in both sexes of two species of Drosophila 3 . We matched these data to protein-protein interactions that could be assigned with high confidence (confidence score 4 0.55): 8,728 in yeast 5 and 3,964 in flies 6 . Choosing interactions with more stringent selection criteria produced similar results (Supplementary Note online).The breadth of variation of expression for a given gene in both flies and yeast (gene expression polymorphism) was negatively correlated with the number of protein-protein interactions found for the product of that gene (yeast: r ¼ -0.11, P o 0.0001, n ¼ 3,536; flies: r ¼ -0.15, P ¼ 0.022, n ¼ 225; Fig. 1). Gene expression divergence between two Drosophila species was also negatively associated with the number of protein-protein interactions (males: r ¼ -0.18, P ¼ 0.012, n ¼ 205; females: r ¼ -0.19, P ¼ 0.007, n ¼ 205). Furthermore, the connectivity of a protein was an excellent predictor of the mean variation in expression in classes of genes with a similar number of interactions ( Supplementary Fig. 1 online). Taken together, these results suggest that protein interactions might be a constraint that reduces evolutionary variation in gene expression both within and between species.Among yeast proteins, the rate of accumulation of replacement substitutions decreases as the number of protein-protein interactions increases 7,8 . The importance of this conclusion has been d...

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The maintenance of genetic variability by mutation in a polygenic character with linked loci

Cited by 736 publications

References 29 publications

Natural selection and the heritability of fitness components

Natural selection and the heritability of fitness components

MIPoD: A Hypothesis‐Testing Framework for Microevolutionary Inference from Patterns of Divergence

Regulatory evolution across the protein interaction network

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