The Missing Response to Selection in the Wild

Pujol, Benoît; Blanchet, Simon; Charmantier, Anne; Danchin, Étienne; Facon, Benoît; Marrot, Pascal; Roux, Fabrice; Scotti, Ivan; Teplitsky, Céline; Thomson, Caroline; Winney, Isabel

doi:10.1016/j.tree.2018.02.007

Cited by 111 publications

(109 citation statements)

References 69 publications

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“…Today, the focus is slowly shifting towards the understanding of the mechanisms and evolutionary consequences of non-genetic inheritance, which remains one of the major challenges of modern biology (Bonduriansky, 2012;Kappeler & Meaney, 2012;Danchin, 2013;Grossniklaus et al, 2013;Klironomos, Berg & Collins, 2013;Heard & Martienssen, 2014;Bohacek & Mansuy, 2015;Kronholm & Collins, 2015;Sharma, 2015;Szyf, 2015;Klosin & Lehner, 2016;Wang et al, 2017;Pujol et al, 2018). In this context, a crucial question is 'whether there is a mechanism that could then fix these epigenetically driven phenotypic changes in the genetic sequence, thereby altering the course of evolution' (Szyf, 2014, p. 4).…”

Section: (B) To the Study Of Its Underlying Mechanismsmentioning

confidence: 99%

Epigenetically facilitated mutational assimilation: epigenetics as a hub within the inclusive evolutionary synthesis

et al. 2018

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After decades of debate about the existence of non‐genetic inheritance, the focus is now slowly shifting towards dissecting its underlying mechanisms. Here, we propose a new mechanism that, by integrating non‐genetic and genetic inheritance, may help build the long‐sought inclusive vision of evolution. After briefly reviewing the wealth of evidence documenting the existence and ubiquity of non‐genetic inheritance in a table, we review the categories of mechanisms of parent–offspring resemblance that underlie inheritance. We then review several lines of argument for the existence of interactions between non‐genetic and genetic components of inheritance, leading to a discussion of the contrasting timescales of action of non‐genetic and genetic inheritance. This raises the question of how the fidelity of the inheritance system can match the rate of environmental variation. This question is central to understanding the role of different inheritance systems in evolution. We then review and interpret evidence indicating the existence of shifts from inheritance systems with low to higher transmission fidelity. Based on results from different research fields we propose a conceptual hypothesis linking genetic and non‐genetic inheritance systems. According to this hypothesis, over the course of generations, shifts among information systems allow gradual matching between the rate of environmental change and the inheritance fidelity of the corresponding response. A striking conclusion from our review is that documented shifts between types of inherited non‐genetic information converge towards epigenetics (i.e. inclusively heritable molecular variation in gene expression without change in DNA sequence). We then interpret the well‐documented mutagenicity of epigenetic marks as potentially generating a final shift from epigenetic to genetic encoding. This sequence of shifts suggests the existence of a relay in inheritance systems from relatively labile ones to gradually more persistent modes of inheritance, a relay that could constitute a new mechanistic basis for the long‐proposed, but still poorly documented, hypothesis of genetic assimilation. A profound difference between the genocentric and the inclusive vision of heredity revealed by the genetic assimilation relay proposed here lies in the fact that a given form of inheritance can affect the rate of change of other inheritance systems. To explore the consequences of such inter‐connection among inheritance systems, we briefly review published theoretical models to build a model of genetic assimilation focusing on the shift in the engraving of environmentally induced phenotypic variation into the DNA sequence. According to this hypothesis, when environmental change remains stable over a sufficient number of generations, the relay among inheritance systems has the potential to generate a form of genetic assimilation. In this hypothesis, epigenetics appears as a hub by which non‐genetically inherited environmentally induced variation in traits can be...

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Section: (B) To the Study Of Its Underlying Mechanismsmentioning

confidence: 99%

Epigenetically facilitated mutational assimilation: epigenetics as a hub within the inclusive evolutionary synthesis

et al. 2018

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“…Their predictive power worked efficiently for the genetic improvement of complex traits in many animal and plant breeding programs. Yet when spatio-temporal ecological heterogeneity is involved, evolution in the wild remains largely unpredictable (Pemberton 2010;Pujol et al 2018).…”

Section: Impact Summarymentioning

confidence: 99%

“…Yet when spatio‐temporal ecological heterogeneity is involved, evolution in the wild remains largely unpredictable (Pemberton ; Pujol et al. ).…”

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confidence: 99%

On the importance of time scales when studying adaptive evolution

Perrier

Charmantier

2019

Evolution Letters

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Long‐term field studies coupled with quantitative genomics offer a powerful means to understand the genetic bases underlying quantitative traits and their evolutionary changes. However, analyzing and interpreting the time scales at which adaptive evolution occurs is challenging. First, while evolution is predictable in the short term, with strikingly rapid phenotypic changes in data series, it remains unpredictable in the long term. Second, while the temporal dynamics of some loci with large effects on phenotypic variation and fitness have been characterized, this task can be complicated in cases of highly polygenic trait architecture implicating numerous small effect size loci, or when statistical tests are sensitive to the heterogeneity of some key characteristics of the genome, like variation in recombination rate along the chromosomes. After introducing these aforementioned challenges, we discuss a recent investigation of the genomic architecture and spatio‐temporal variation in great tit bill length, which was related to the recent use of bird feeders. We discuss how this case study illustrates the importance of considering different temporal scales and evolutionary mechanisms both while analyzing trait temporal trends and when searching for and interpreting the signals of putative genomic footprints of selection. More generally this commentary discusses interesting challenges for unraveling the time scale at which adaptive traits evolve and their genomic bases.

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“…By exploring evolutionary potential in a fish species, our study complements a growing literature reviewed by Pujol et al (2018), most of which has been on birds and mammals, showing how mismatches between predicted and observed microevolution can result from a range of biological and statistical mechanisms. We used the Δβ test to infer that missing traits correlated with female body size were likely present, and thus that using the estimated phenotypic selection gradient in the univariate BE will likely lead to a biased microevolutionary prediction-that is that larger body size should evolve, when in fact no evolutionary trend was observed, nor was any predicted by the STS.…”

Section: Discussionmentioning

confidence: 96%

Evolutionary stasis of a heritable morphological trait in a wild fish population despite apparent directional selection

O’Sullivan

Aykanat

Johnston

et al. 2019

Ecology and Evolution

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Comparing observed versus theoretically expected evolutionary responses is important for our understanding of the evolutionary process, and for assessing how species may cope with anthropogenic change. Here, we document directional selection for larger female size in Atlantic salmon, using pedigree‐derived estimates of lifetime reproductive success as a fitness measure. We show the trait is heritable and, thus, capable of responding to selection. The Breeder's Equation, which predicts microevolution as the product of phenotypic selection and heritability, predicted evolution of larger size. This was at odds, however, with the observed lack of either phenotypic or genetic temporal trends in body size, a so‐called “paradox of stasis.” To investigate this paradox, we estimated the additive genetic covariance between trait and fitness, which provides a prediction of evolutionary change according to Robertson's secondary theorem of selection (STS) that is unbiased by missing variables. The STS prediction was consistent with the observed stasis. Decomposition of phenotypic selection gradients into genetic and environmental components revealed a potential upward bias, implying unmeasured factors that covary with trait and fitness. These results showcase the power of pedigreed, wild population studies—which have largely been limited to birds and mammals—to study evolutionary processes on contemporary timescales.

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The Missing Response to Selection in the Wild

Cited by 111 publications

References 69 publications

Epigenetically facilitated mutational assimilation: epigenetics as a hub within the inclusive evolutionary synthesis

Epigenetically facilitated mutational assimilation: epigenetics as a hub within the inclusive evolutionary synthesis

On the importance of time scales when studying adaptive evolution

Evolutionary stasis of a heritable morphological trait in a wild fish population despite apparent directional selection

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