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Interaction-based evolution: how natural selection and nonrandom mutation work together.

Livnat A - Biol. Direct (2013)

Bottom Line: How can selection operate effectively on genetic interactions?This allows selection on a fleeting combination of interacting alleles at different loci to have a hereditary effect according to the combination's fitness.Ford Doolittle.

View Article: PubMed Central - HTML - PubMed

ABSTRACT

Background: The modern evolutionary synthesis leaves unresolved some of the most fundamental, long-standing questions in evolutionary biology: What is the role of sex in evolution? How does complex adaptation evolve? How can selection operate effectively on genetic interactions? More recently, the molecular biology and genomics revolutions have raised a host of critical new questions, through empirical findings that the modern synthesis fails to explain: for example, the discovery of de novo genes; the immense constructive role of transposable elements in evolution; genetic variance and biochemical activity that go far beyond what traditional natural selection can maintain; perplexing cases of molecular parallelism; and more.

Presentation of the hypothesis: Here I address these questions from a unified perspective, by means of a new mechanistic view of evolution that offers a novel connection between selection on the phenotype and genetic evolutionary change (while relying, like the traditional theory, on natural selection as the only source of feedback on the fit between an organism and its environment). I hypothesize that the mutation that is of relevance for the evolution of complex adaptation-while not Lamarckian, or "directed" to increase fitness-is not random, but is instead the outcome of a complex and continually evolving biological process that combines information from multiple loci into one. This allows selection on a fleeting combination of interacting alleles at different loci to have a hereditary effect according to the combination's fitness.

Testing and implications of the hypothesis: This proposed mechanism addresses the problem of how beneficial genetic interactions can evolve under selection, and also offers an intuitive explanation for the role of sex in evolution, which focuses on sex as the generator of genetic combinations. Importantly, it also implies that genetic variation that has appeared neutral through the lens of traditional theory can actually experience selection on interactions and thus has a much greater adaptive potential than previously considered. Empirical evidence for the proposed mechanism from both molecular evolution and evolution at the organismal level is discussed, and multiple predictions are offered by which it may be tested.

Reviewers: This article was reviewed by Nigel Goldenfeld (nominated by Eugene V. Koonin), Jürgen Brosius and W. Ford Doolittle.

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Mutation as a biological process. a) Mutation as a biological processmeans that genes interact in the determination of mutation. In the schematicfigure, information from three different loci (A, B and C) comes together,through cis-acting elements and trans-acting factors, to affect theprobability and nature of a genetic change in one of these loci (B). Inputsinto this mutational process are shown by the annotated arrows. The downwardarrow represents the writing of mutation, for example by components of theso-called “error-repair” machinery, here not restoring butchanging the genetic state from what it was previously. In reality, manymore pieces of information than depicted here for simplicity may beinvolved. b) After meiosis, the changed locus (B*) carries in it aninformation-signature from the combination that participated in thegeneration of the change, and thus allows the combination as a whole to havea lasting effect, even though its components are no longer all present.
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Figure 1: Mutation as a biological process. a) Mutation as a biological processmeans that genes interact in the determination of mutation. In the schematicfigure, information from three different loci (A, B and C) comes together,through cis-acting elements and trans-acting factors, to affect theprobability and nature of a genetic change in one of these loci (B). Inputsinto this mutational process are shown by the annotated arrows. The downwardarrow represents the writing of mutation, for example by components of theso-called “error-repair” machinery, here not restoring butchanging the genetic state from what it was previously. In reality, manymore pieces of information than depicted here for simplicity may beinvolved. b) After meiosis, the changed locus (B*) carries in it aninformation-signature from the combination that participated in thegeneration of the change, and thus allows the combination as a whole to havea lasting effect, even though its components are no longer all present.

Mentions: Given that genes interact in the determination of genetic change, and keeping theassumption that their alleles interact, this means that the mutation that drivesevolution is a process that combines information from alleles at multiple loci andwrites the result of the combination operation into one locus—the locus beingchanged by mutation (Figure 1a). (Also if multiple loci arechanged at once, information is combined from multiple loci to enact these multiplechanges.) By combining information from alleles at multiple loci into one locus,this operation creates from the combination of alleles a piece of information thatis not broken by the sexual shuffling of the genes, and is therefore heritable(Figure 1b). (It creates an allele, and this is an elementaryunit for the shuffling; the shuffling breaks only combinations of alleles). Thismeans that combinations of alleles at different loci do have an effect that laststhrough the shuffling: they transmit information to future generations through themutations that are derived from them.


Interaction-based evolution: how natural selection and nonrandom mutation work together.

Livnat A - Biol. Direct (2013)

Mutation as a biological process. a) Mutation as a biological processmeans that genes interact in the determination of mutation. In the schematicfigure, information from three different loci (A, B and C) comes together,through cis-acting elements and trans-acting factors, to affect theprobability and nature of a genetic change in one of these loci (B). Inputsinto this mutational process are shown by the annotated arrows. The downwardarrow represents the writing of mutation, for example by components of theso-called “error-repair” machinery, here not restoring butchanging the genetic state from what it was previously. In reality, manymore pieces of information than depicted here for simplicity may beinvolved. b) After meiosis, the changed locus (B*) carries in it aninformation-signature from the combination that participated in thegeneration of the change, and thus allows the combination as a whole to havea lasting effect, even though its components are no longer all present.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4231362&req=5

Figure 1: Mutation as a biological process. a) Mutation as a biological processmeans that genes interact in the determination of mutation. In the schematicfigure, information from three different loci (A, B and C) comes together,through cis-acting elements and trans-acting factors, to affect theprobability and nature of a genetic change in one of these loci (B). Inputsinto this mutational process are shown by the annotated arrows. The downwardarrow represents the writing of mutation, for example by components of theso-called “error-repair” machinery, here not restoring butchanging the genetic state from what it was previously. In reality, manymore pieces of information than depicted here for simplicity may beinvolved. b) After meiosis, the changed locus (B*) carries in it aninformation-signature from the combination that participated in thegeneration of the change, and thus allows the combination as a whole to havea lasting effect, even though its components are no longer all present.
Mentions: Given that genes interact in the determination of genetic change, and keeping theassumption that their alleles interact, this means that the mutation that drivesevolution is a process that combines information from alleles at multiple loci andwrites the result of the combination operation into one locus—the locus beingchanged by mutation (Figure 1a). (Also if multiple loci arechanged at once, information is combined from multiple loci to enact these multiplechanges.) By combining information from alleles at multiple loci into one locus,this operation creates from the combination of alleles a piece of information thatis not broken by the sexual shuffling of the genes, and is therefore heritable(Figure 1b). (It creates an allele, and this is an elementaryunit for the shuffling; the shuffling breaks only combinations of alleles). Thismeans that combinations of alleles at different loci do have an effect that laststhrough the shuffling: they transmit information to future generations through themutations that are derived from them.

Bottom Line: How can selection operate effectively on genetic interactions?This allows selection on a fleeting combination of interacting alleles at different loci to have a hereditary effect according to the combination's fitness.Ford Doolittle.

View Article: PubMed Central - HTML - PubMed

ABSTRACT

Background: The modern evolutionary synthesis leaves unresolved some of the most fundamental, long-standing questions in evolutionary biology: What is the role of sex in evolution? How does complex adaptation evolve? How can selection operate effectively on genetic interactions? More recently, the molecular biology and genomics revolutions have raised a host of critical new questions, through empirical findings that the modern synthesis fails to explain: for example, the discovery of de novo genes; the immense constructive role of transposable elements in evolution; genetic variance and biochemical activity that go far beyond what traditional natural selection can maintain; perplexing cases of molecular parallelism; and more.

Presentation of the hypothesis: Here I address these questions from a unified perspective, by means of a new mechanistic view of evolution that offers a novel connection between selection on the phenotype and genetic evolutionary change (while relying, like the traditional theory, on natural selection as the only source of feedback on the fit between an organism and its environment). I hypothesize that the mutation that is of relevance for the evolution of complex adaptation-while not Lamarckian, or "directed" to increase fitness-is not random, but is instead the outcome of a complex and continually evolving biological process that combines information from multiple loci into one. This allows selection on a fleeting combination of interacting alleles at different loci to have a hereditary effect according to the combination's fitness.

Testing and implications of the hypothesis: This proposed mechanism addresses the problem of how beneficial genetic interactions can evolve under selection, and also offers an intuitive explanation for the role of sex in evolution, which focuses on sex as the generator of genetic combinations. Importantly, it also implies that genetic variation that has appeared neutral through the lens of traditional theory can actually experience selection on interactions and thus has a much greater adaptive potential than previously considered. Empirical evidence for the proposed mechanism from both molecular evolution and evolution at the organismal level is discussed, and multiple predictions are offered by which it may be tested.

Reviewers: This article was reviewed by Nigel Goldenfeld (nominated by Eugene V. Koonin), Jürgen Brosius and W. Ford Doolittle.

Show MeSH