Testing the neutral hypothesis of phenotypic evolution

Molecular Biology and Evolution

et al. 2020

Fisher’s fundamental theorem of natural selection predicts no additive variance of fitness in a natural population. Consistently, studies in a variety of wild populations show virtually no narrow-sense heritability (h2) for traits important to fitness. However, counterexamples are occasionally reported, calling for a deeper understanding on the evolution of additive variance. In this study, we propose adaptive divergence followed by population admixture as a source of the additive genetic variance of evolutionarily important traits. We experimentally tested the hypothesis by examining a panel of ∼1,000 yeast segregants produced by a hybrid of two yeast strains that experienced adaptive divergence. We measured >400 yeast cell morphological traits and found a strong positive correlation between h2 and evolutionary importance. Because adaptive divergence followed by population admixture could happen constantly, particularly in species with wide geographic distribution and strong migratory capacity (e.g., humans), the finding reconciles the observation of abundant additive variances in evolutionarily important traits with Fisher’s fundamental theorem of natural selection. Importantly, the revealed role of positive selection in promoting rather than depleting additive variance suggests a simple explanation for why additive genetic variance can be dominant in a population despite the ubiquitous between-gene epistasis observed in functional assays.

Section: Resultssupporting

confidence: 72%

Section: Resultsmentioning

confidence: 99%

The Origin of Additive Genetic Variance Driven by Positive Selection

Liu

Wang

Molecular Biology and Evolution

et al. 2020

“…Ho et al found faster evolution of more important morphological traits within and between species, supporting the adaptive hypothesis of phenotypic evolution (Ho, et al 2017). The adaptive divergence followed by population mixture may provide a clue to understand why additive variance of fitness traits are observed in some wild populations.…”

Section: Introductionmentioning

confidence: 76%

The source of additive genetic variance of evolutionarily important traits

Liu

Wang

et al. 2019

Preprint

Fisher's fundamental theorem of natural selection predicts no additive variance of fitness in a natural population. Consistently, observations in a variety of wild populations show virtually no narrow-sense heritability (h 2 ) for traits closely related to fitness.However, counterexamples are also reported, calling for a deeper understanding on the evolution of additive variance. In this study we propose adaptive divergence followed by population mixture as a source of additive variance of fitnessrelated traits. We experimentally tested the proposal by examining a panel of ~1,000 yeast segregants produced by a hybrid of two yeast strains subject to adaptive divergence. We measured over 400 yeast cell morphological traits and found a strong positive correlation between their h 2 and their relatedness to fitness. This pattern, being a counterexample of the prediction of Fisher's theorem, well supports our proposal. Because adaptive divergence followed by population mixture could happen constantly, particularly in some species including humans and domesticated animals or crops, the proposal provides a framework for reconciling the availability of abundant additive variances of important traits with Fisher's fundamental theorem of natural selection.

“…The number of mutations followed a Poisson distribution with the mean equal to , which is a random variable drawn from a gamma distribution with the shape parameter 0.5 and the scale parameter 400. We set 0.5 because such a distribution is similar to some empirically observed distributions for mutationally independent orthogonal traits such as yeast cell morphologies (Ho et al 2017) and fly wing morphologies (Houle and Fierst 2013). The phenotypic effect of a mutation on a trait followed a normal distribution with a mean of 0 and a standard deviation of 0.01.…”

Section: Mutational Inputmentioning

confidence: 96%

Fly wing evolution explained by a neutral model with mutational pleiotropy

Jiang

2020

Preprint

Self Cite

To what extent the speed of mutational production of phenotypic variation determines the rate of long-term phenotypic evolution is a central question in evolutionary biology. In a recent study, Houle et al. addressed this question by studying the mutational variation, microevolution, and macroevolution of locations of vein intersections on fly wings, reporting very slow phenotypic evolution relative to the rates of mutational input, high phylogenetic signals of these traits, and a strong, linear correlation between the mutational variance of a trait and its rate of evolution. Houle et al. examined multiple models of phenotypic evolution but found none consistent with all these observations. Here we demonstrate that the purported linear correlation between mutational variance and evolutionary divergence is an artifact. More importantly, patterns of fly wing evolution are explainable by a simple model in which the wing traits are neutral or neutral within a range of phenotypic values but their evolutionary rates are reduced because most mutations affecting these traits are purged owing to their pleiotropic effects on other traits that are under stabilizing selection. We conclude that the evolutionary patterns of fly wing morphologies are explainable under the existing theoretical framework of phenotypic evolution.