The role of robustness in phenotypic adaptation and innovation

Wagner, Andreas

doi:10.1098/rspb.2011.2293

Cited by 125 publications

(124 citation statements)

References 75 publications

(97 reference statements)

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“…Does innovation simplify system structure in some contexts and complexify it in others? Under what conditions does organism complexity [118] or system robustness [119] affect innovation? -Innovation instructs on associations between adaptation and fitness.…”

Section: (A) Searching For and Discovering Innovationmentioning

confidence: 99%

Innovation: an emerging focus from cells to societies

Hochberg

Marquet

Boyd

et al. 2017

Phil. Trans. R. Soc. B

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Innovations are generally unexpected, often spectacular changes in phenotypes and ecological functions. The contributions to this theme issue are the latest conceptual, theoretical and experimental developments, addressing how ecology, environment, ontogeny and evolution are central to understanding the complexity of the processes underlying innovations. Here, we set the stage by introducing and defining key terms relating to innovation and discuss their relevance to biological, cultural and technological change. Discovering how the generation and transmission of novel biological information, environmental interactions and selective evolutionary processes contribute to innovation as an ecosystem will shed light on how the dominant features across life come to be, generalize to social, cultural and technological evolution, and have applications in the health sciences and sustainability. This article is part of the theme issue ‘Process and pattern in innovations from cells to societies’.

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Section: (A) Searching For and Discovering Innovationmentioning

confidence: 99%

Innovation: an emerging focus from cells to societies

Hochberg

Marquet

Boyd

et al. 2017

Phil. Trans. R. Soc. B

Self Cite

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“…Support to the generation of neutral genotypic diversity after gene duplication comes from the classic belief that after duplication gene copies suffer relaxed selective constraints that allow one or both copies tolerating many-fold more mutations than otherwise, a fact with extensive experimental and theoretical support [2,86,87]. This phenomenon is more obvious when analyzing genomes populated with duplicates originated by whole-genome duplication, in which younger duplicates still preserve signatures of their larger tolerance to mutations than older duplicates [79,84,88,89].…”

Section: Evolution By Gene Duplication: Robustness To Mutational Insultsmentioning

confidence: 99%

“…Biological systems are inherently robust (resistant) to perturbations, maintaining the same phenotype in the face of external challenges and noise internal to the system [1,2]. Therefore, phenotypes are said to be robust if they resist perturbations.…”

Section: Introductionmentioning

confidence: 99%

Survival and innovation: The role of mutational robustness in evolution

Fares

2015

Biochimie

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a b s t r a c tBiological systems are resistant to perturbations caused by the environment and by the intrinsic noise of the system. Robustness to mutations is a particular aspect of robustness in which the phenotype is resistant to genotypic variation. Mutational robustness has been linked to the ability of the system to generate heritable genetic variation (a property known as evolvability). It is known that greater robustness leads to increased evolvability. Therefore, mechanisms that increase mutational robustness fuel evolvability. Two such mechanisms, molecular chaperones and gene duplication, have been credited with enormous importance in generating functional diversity through the increase of system's robustness to mutational insults. However, the way in which such mechanisms regulate robustness remains largely uncharacterized. In this review, I provide evidence in support of the role of molecular chaperones and gene duplication in innovation. Specifically, I present evidence that these mechanisms regulate robustness allowing unstable systems to survive long periods of time, and thus they provide opportunity for other mutations to compensate the destabilizing effects of functionally innovative mutations. The findings reported in this study set new questions with regards to the synergy between robustness mechanisms and how this synergy can alter the adaptive landscape of proteins. The ideas proposed in this article set the ground for future research in the understanding of the role of robustness in evolution.

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“…As development becomes more robust, less phenotypic variation is observed among individuals in a population (Scharloo 1991;de Visser et al 2003;Siegal and Leu 2014). This has implications not only for the relationship between genotype and phenotype, but also for evolution (Gibson and Wagner 2000;Gibson and Dworkin 2004;Wagner 2012). In one sense, robustness inhibits evolvability since it suppresses the phenotypic variation that selection acts upon.…”

mentioning

confidence: 99%

“…the same phenotype (Wagner 2012). Later, if canalization is impaired, the effects of the previously cryptic genetic variation are revealed as phenotypic variability.…”

mentioning

confidence: 99%

Differential Masking of Natural Genetic Variation by miR-9a in Drosophila

2015

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Genetic variation is prevalent among individuals of the same species and yet the potential effects of genetic variation on developmental outcomes are frequently suppressed. Understanding the mechanisms that are responsible for this suppression is an important goal. Previously, we found that the microRNA miR-9a mitigates the impact of natural genetic variants that promote the development of scutellar bristles in adult Drosophila. Here we find that miR-9a does not affect the impact of genetic variants that inhibit the development of scutellar bristles. We show this using both directional and stabilizing selection in the laboratory. This specificity of action suggests that miR-9a does not interact with all functional classes of developmental genetic variants affecting sensory organ development. We also investigate the impact of miR-9a on a fitness trait, which is adult viability. At elevated physiological temperatures, miR-9a contributes to viability through masking genetic variants that hinder adult viability. We conclude that miR-9a activity in different developmental networks contributes to suppression of natural variants from perturbing development. KEYWORDS Drosophila; miRNA; heritability; sensory organs; development O RGANISMS are subject to conditions of genetic variation, and yet their morphological development is often robust to such challenges. Hence, developmental outcomes are rendered uniform even in the face of variable conditions of existence. The relationship between this developmental robustness and phenotypic variation in natural populations has long been remarked upon, and Waddington (1942) coined the word canalization to describe the process. As development becomes more robust, less phenotypic variation is observed among individuals in a population (Scharloo 1991;de Visser et al. 2003;Siegal and Leu 2014). This has implications not only for the relationship between genotype and phenotype, but also for evolution (Gibson and Wagner 2000;Gibson and Dworkin 2004;Wagner 2012). In one sense, robustness inhibits evolvability since it suppresses the phenotypic variation that selection acts upon. However, when a phenotype is robust to the effects of mutations, then genetic variation can potentially accumulate in a neutral state. This might permit a broad set of connected genotypes to express the same phenotype (Wagner 2012). Later, if canalization is impaired, the effects of the previously cryptic genetic variation are revealed as phenotypic variability. These can be subject to selection, thus enhancing evolvability.Morphological variation is a consequence of variable development between individuals. Development, in turn, is the complex outcome of dynamic interactions between regulatory molecules. Developmental dynamics have been successfully simulated by biochemical reaction network models, which vary in size, topology, and circuit composition and depend upon the specific developmental process, tissue type, and species (Kitano 2004;Stathopoulos and Levine 2005;Wunderlich and DePace 2011). Studie...

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The role of robustness in phenotypic adaptation and innovation

Cited by 125 publications

References 75 publications

Innovation: an emerging focus from cells to societies

Innovation: an emerging focus from cells to societies

Survival and innovation: The role of mutational robustness in evolution

Differential Masking of Natural Genetic Variation by miR-9a in Drosophila

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