Modularity and the Cost of Complexity

Welch, John J.; Waxman, David J.

doi:10.1111/j.0014-3820.2003.tb00581.x

Cited by 172 publications

(177 citation statements)

References 49 publications

(43 reference statements)

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“…Theoretical models suggest that pleiotropic effects can affect the adaptive process, usually reducing the rate of evolution (11,44). The number of branches produced is one of the strongest predictors of A. thaliana's fitness, as shown here and in previous laboratory-and field-based studies (41,45,46).…”

Section: Discussionsupporting

confidence: 71%

Antagonistic pleiotropic effects reduce the potential adaptive value of the FRIGIDA locus

Scarcelli

Cheverud

Schaal

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

113

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Although the occurrence of epistasis and pleiotropy is widely accepted at the molecular level, its effect on the adaptive value of fitness-related genes is rarely investigated in plants. Knowledge of these features of a gene is critical to understand the molecular basis of adaptive evolution. Here we investigate the importance of pleiotropy and epistasis in determining the adaptive value of a candidate gene using the gene FRI (FRIGIDA), which is thought to be the major gene controlling flowering time variation in Arabidopsis thaliana. The effect of FRI on flowering time was analyzed in an outbred population created by randomly mating 19 natural accessions of A. thaliana. This unique population allows the estimation of FRI effects independent of any linkage association with other loci due to demographic processes or to coadapted genes. It also allows for the estimation of pleiotropic effects of FRI on fitness and inflorescence architecture. We found that FRI explains less variation in flowering time than previously observed among natural accessions, and interacts epistatically with the FLC locus. Although early flowering plants produce more fruits under spring conditions, and nonfunctional alleles of FRI were associated with early flowering, variation at FRI was not associated with fitness. We show that nonfunctional FRI alleles have negative pleiotropic effects on fitness by reducing the numbers of nodes and branches on the inflorescence. We propose that these antagonistic pleiotropic effects reduce the adaptive value of FRI, and helps explain the maintenance of alternative life history strategies across natural populations of A. thaliana.Arabidopsis thaliana ͉ FLC ͉ flowering time ͉ pleiotropy ͉ gene-by-environment interaction D espite decades of research, we still know surprisingly little about the molecular basis of adaptation (but see refs. 1 and 2). To understand the genetic basis of adaptive evolution it is necessary to combine knowledge of the molecular basis of fitness-related traits with information about how selection acts on the available genetic variation (1). A number of candidate genes underlying adaptive traits have been identified in studies by using QTL analysis or forward genetic approaches (3-5). The role of candidate genes on past adaptive evolution is then often investigated by looking at rates and patterns of nucleotide substitution for evidence of past selection. Although a number of studies have shown that the rate of synonymous-to-nonsynonymous substitution in candidate genes is compatible with natural selection (6-8), demographic dynamics also can cause departure from the neutral expectation (9, 10). Thus, direct evidence for selection at the molecular level is ultimately needed, and such data are still very limited.Determining the adaptive value of candidate genes is further complicated by the fact that the relationship between genotype and fitness is complex and results from the combination and/or interaction of multiple traits and genes. Consequently, understanding the relationship b...

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Section: Discussionsupporting

confidence: 71%

Antagonistic pleiotropic effects reduce the potential adaptive value of the FRIGIDA locus

Scarcelli

Cheverud

Schaal

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

113

View full text Add to dashboard Cite

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“…In addition, one can just as easily point to a long list of pathologies that can arise from an overly rapid proliferation of a new phenotype, and such scenarios have motivated a completely alternative, and equally speculative, view, that selection can favor mechanisms that suppress evolvability (103). Furthermore, theoretical studies have shown that the kinds of complexities that are often focused on by those enamored with evolvability (e.g., increased dimensionality and modularity) can actually inhibit the rate of adaptive evolution (104)(105)(106). Although the arguments are technical, they are no more abstract that the verbal reasoning of the evolvability school.…”

Section: Evolvabilitymentioning

confidence: 99%

The frailty of adaptive hypotheses for the origins of organismal complexity

Lynch

2007

Proc. Natl. Acad. Sci. U.S.A.

698

568

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The vast majority of biologists engaged in evolutionary studies interpret virtually every aspect of biodiversity in adaptive terms. This narrow view of evolution has become untenable in light of recent observations from genomic sequencing and populationgenetic theory. Numerous aspects of genomic architecture, gene structure, and developmental pathways are difficult to explain without invoking the nonadaptive forces of genetic drift and mutation. In addition, emergent biological features such as complexity, modularity, and evolvability, all of which are current targets of considerable speculation, may be nothing more than indirect by-products of processes operating at lower levels of organization. These issues are examined in the context of the view that the origins of many aspects of biological diversity, from gene-structural embellishments to novelties at the phenotypic level, have roots in nonadaptive processes, with the populationgenetic environment imposing strong directionality on the paths that are open to evolutionary exploitation.adaptation ͉ genome evolution ͉ evolvability ͉ modularity ͉ population genetics

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“…1b). Naively, this model predicts a reduction in evolvability per trait with increasing complexity, if pleiotropy is taken as a proxy for complexity (Orr 2000;Welch and Waxman 2003).…”

Section: Modeling Pleiotropymentioning

confidence: 99%

Genotype-Phenotype Maps Maximizing Evolvability: Modularity Revisited

Pavličev

Hansen

2011

Evol Biol

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The mechanisms translating genetic to phenotypic variation determine the distribution of heritable phenotypic variance available to selection. Pleiotropy is an aspect of this structure that limits independent variation of characters. Modularization of pleiotropy has been suggested to promote evolvability by restricting genetic covariance among unrelated characters and reducing constraints due to correlated response. However, modularity may also reduce total genetic variation of characters. We study the properties of genotype-phenotype maps that maximize average conditional evolvability, measured as the amount of unconstrained genetic variation in random directions of phenotypic space. In general, maximal evolvability occurs by maximizing genetic variance and minimizing genetic covariance. This does not necessarily require modularity, only patterns of pleiotropy that cancel on average. The detailed structure of the most evolvable genotype-phenotype maps depends on the distribution of molecular variance. When molecular variance is determined by mutation-selection equilibrium either highly pleiotropic or highly modular genotype-phenotype maps can be optimal, depending on the mutation rate and the relative strengths of stabilizing selection on the characters.

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Modularity and the Cost of Complexity

Cited by 172 publications

References 49 publications

Antagonistic pleiotropic effects reduce the potential adaptive value of the FRIGIDA locus

Antagonistic pleiotropic effects reduce the potential adaptive value of the FRIGIDA locus

The frailty of adaptive hypotheses for the origins of organismal complexity

Genotype-Phenotype Maps Maximizing Evolvability: Modularity Revisited

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