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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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Related in: MedlinePlus

A schematic diagram showing the evolution of signals in thePoldi  gene, modified from Heinen etal. [11], with permission from Elsevier. The visualpresentation follows closely that of Heinen et al. [11]. Exons and introns are not drawn to scale. Observed genesare shown in blue, and a possible history, consistent with thenonfunctional-ancestor consensus view in the literature, is shown inred. Checks and crosses represent presence and absence of signals,respectively. According to a parsimony-based interpretation of thedata, a possibility arises that signals have been added on thetimescale of millions of years. Note that the total number ofsignals is monotonically increasing with decreasing phylogeneticdistance to Mus musculus (as the clade including M.cypriacus, M. macedonicus, and M.spicilegus can be rotated around its base).
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Figure 3: A schematic diagram showing the evolution of signals in thePoldi gene, modified from Heinen etal. [11], with permission from Elsevier. The visualpresentation follows closely that of Heinen et al. [11]. Exons and introns are not drawn to scale. Observed genesare shown in blue, and a possible history, consistent with thenonfunctional-ancestor consensus view in the literature, is shown inred. Checks and crosses represent presence and absence of signals,respectively. According to a parsimony-based interpretation of thedata, a possibility arises that signals have been added on thetimescale of millions of years. Note that the total number ofsignals is monotonically increasing with decreasing phylogeneticdistance to Mus musculus (as the clade including M.cypriacus, M. macedonicus, and M.spicilegus can be rotated around its base).

Mentions: Armed with this new theoretical framework, we can take a closer look at thede novo gene data. Consider, for example, the case of thePoldi gene analyzed by Heinen et al. [11]. In the house mouse (Mus musculus) and closely relatedspecies, this gene is transcribed in postmeiotic cells of the testis andshows evidence of functionality (reduced sperm motility and testis weight inknockout mice). In Figure 3, the signals forPoldi transcription and splicing are shown for mammalianspecies of increasing distance from Mus musculus. Notice how inhumans (the most distant species from Mus musculus in the sample),only 2 out of 6 signals are present. In Rattus norvegicus, 4 out of6 signals are present. In the basal Mus species Mus caroliand Mus famulus, as well as in Mus spicilegus, 5 out of 6signals are present. And in the remaining, focal species of Mus,all 6 signals are present. By parsimony, it is assumed that the gene wasmissing at least one signal at the root of this phylogeny, and thattherefore at least one if not more signals were added in time. Looking atthis phylogenetic tree without preconceptions, we see the possibility of aslow and tentative construction of a gene over the long-term and thereforein multiple lineages, where in the Mus genus it reaches the pointof transcription first.


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

Livnat A - Biol. Direct (2013)

A schematic diagram showing the evolution of signals in thePoldi  gene, modified from Heinen etal. [11], with permission from Elsevier. The visualpresentation follows closely that of Heinen et al. [11]. Exons and introns are not drawn to scale. Observed genesare shown in blue, and a possible history, consistent with thenonfunctional-ancestor consensus view in the literature, is shown inred. Checks and crosses represent presence and absence of signals,respectively. According to a parsimony-based interpretation of thedata, a possibility arises that signals have been added on thetimescale of millions of years. Note that the total number ofsignals is monotonically increasing with decreasing phylogeneticdistance to Mus musculus (as the clade including M.cypriacus, M. macedonicus, and M.spicilegus can be rotated around its base).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: A schematic diagram showing the evolution of signals in thePoldi gene, modified from Heinen etal. [11], with permission from Elsevier. The visualpresentation follows closely that of Heinen et al. [11]. Exons and introns are not drawn to scale. Observed genesare shown in blue, and a possible history, consistent with thenonfunctional-ancestor consensus view in the literature, is shown inred. Checks and crosses represent presence and absence of signals,respectively. According to a parsimony-based interpretation of thedata, a possibility arises that signals have been added on thetimescale of millions of years. Note that the total number ofsignals is monotonically increasing with decreasing phylogeneticdistance to Mus musculus (as the clade including M.cypriacus, M. macedonicus, and M.spicilegus can be rotated around its base).
Mentions: Armed with this new theoretical framework, we can take a closer look at thede novo gene data. Consider, for example, the case of thePoldi gene analyzed by Heinen et al. [11]. In the house mouse (Mus musculus) and closely relatedspecies, this gene is transcribed in postmeiotic cells of the testis andshows evidence of functionality (reduced sperm motility and testis weight inknockout mice). In Figure 3, the signals forPoldi transcription and splicing are shown for mammalianspecies of increasing distance from Mus musculus. Notice how inhumans (the most distant species from Mus musculus in the sample),only 2 out of 6 signals are present. In Rattus norvegicus, 4 out of6 signals are present. In the basal Mus species Mus caroliand Mus famulus, as well as in Mus spicilegus, 5 out of 6signals are present. And in the remaining, focal species of Mus,all 6 signals are present. By parsimony, it is assumed that the gene wasmissing at least one signal at the root of this phylogeny, and thattherefore at least one if not more signals were added in time. Looking atthis phylogenetic tree without preconceptions, we see the possibility of aslow and tentative construction of a gene over the long-term and thereforein multiple lineages, where in the Mus genus it reaches the pointof transcription first.

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
Related in: MedlinePlus