Can Population Genetics Adapt to Rapid Evolution?

doi:10.1016/j.tig.2016.04.005

Trends in Genetics

Volume 32, Issue 7, July 2016, Pages 408-418

https://doi.org/10.1016/j.tig.2016.04.005 Get rights and content

Trends

Studies of evolution in action show that phenotypic traits can often change dramatically over the course of just a few generations.

This differs markedly from the paradigm of slow molecular evolution commonly adopted in our population genetic models.

To assess whether our models are still appropriate, we need to better understand how rapid phenotypic evolution impacts the trajectories of genetic variation in a population.

New population genomic datasets will make it possible to directly observe how polymorphism frequencies change in a population over time, allowing us to test and refine our population genetic models.

Population genetics largely rests on a ‘standard model’ in which random genetic drift is the dominant force, selective sweeps occur infrequently, and deleterious mutations are purged from the population by purifying selection. Studies of phenotypic evolution in nature reveal a very different picture, with strong selection and rapid heritable trait changes being common. The time-rate scaling of phenotypic evolution suggests that selection on phenotypes is often fluctuating in direction, allowing phenotypes to respond rapidly to environmental fluctuations while remaining within relatively constant bounds over longer periods. Whether such rapid phenotypic evolution undermines the standard model will depend on how many genomic loci typically contribute to strongly selected traits and how phenotypic evolution impacts the dynamics of genetic variation in a population. Population-level sequencing will allow us to dissect the genetic basis of phenotypic evolution and study the evolutionary dynamics of genetic variation through direct measurement of polymorphism trajectories over time.

Section snippets

The Standard Model of Population Genetics

Charles Darwin thought of evolution as an innately slow process driven by small incremental changes that lead to noticeable differences between species only because they can accumulate over long periods of time. This view still runs deep in modern population genetics. We tend to assume that selective sweeps are rare in most natural populations and that most common genetic variation remains largely unaffected by such events. Catching a beneficial mutation on the fly should be extremely unlikely.

Examples of Rapid Phenotypic Evolution in Nature and Experiment

Studies of ‘evolution in action’ paint a markedly different picture from the paradigm of slow molecular evolution commonly adopted in our population genetic models. These studies show that phenotypic traits can often change dramatically over the course of just a few generations. Peter and Rosemary Grant's classic studies of rapid evolution in Darwin's finches 9, 10, 11 are well known by both scientists and non-scientists, but many other studies have now demonstrated rapid change in heritable

Examples of Rapid Molecular Evolution at Individual Loci

Important additional clues are provided by sequencing studies that increasingly allow us to dissect the genomic basis of phenotypic evolution. Such studies have revealed many examples of rapid phenotypic adaptation that were associated with extensive allele-frequency changes at individual genetic loci. One prominent example is the adaptation of marine sticklebacks to freshwater environments, which is driven by only a small set of genomic loci [37] yet has occurred repeatedly over just 50

Are Short-Term and Long-Term Evolutionary Rates Different?

If rapid phenotypic evolution is indeed common in nature and often associated with extensive frequency changes of molecular variants at many loci, why do we not observe higher levels of molecular divergence between extant species? A possible explanation is that selection may not always be as static as assumed by the standard model. If a considerable fraction of genetic variants has selection coefficients that vary in sign over space and time, being advantageous at some times and locations and

Population Genetics Might Be Underestimating the Role of Temporally Fluctuating Selection

While it is widely acknowledged that spatially varying selection can play an important role in the dynamics and maintenance of molecular variation [64], population genetics has remained rather skeptical regarding the significance of temporally fluctuating selection. This view traces back to theoretical arguments showing that, in standard models with non-overlapping generations, temporally fluctuating selection cannot maintain a polymorphism unless the heterozygote has higher geometric mean

Population Genetics Beyond the Standard Model

In the standard model we tend to assume that the selection coefficients of mutations remain constant over time and space. If instead selection coefficients often vary, evolutionary dynamics could be quite different. In this case, selection could play a much more important role among the processes that cause alleles to change in frequency over time. Classic selective sweeps, however, would remain rare, as alleles would usually not be driven all the way to fixation or loss. Instead, we should

Population Genetics Should Embrace Rapid Evolution

The appeal of modern population genetics stems in no small part from the elegance and simplicity of its underlying theoretical models. These models were largely devised in times when data were limited to measurements of molecular divergences between species and rough estimates of the genetic diversity within populations. Kimura's neutral theory of molecular evolution [97] provided a convincing explanation for the patterns in these data that did not require processes more complicated than random

Concluding Remarks

With genome sequencing becoming easier and cheaper, we have the opportunity to directly observe the essence of evolution: how allele frequencies change over time within a population, as in Figure 4B. With such data we can finally test the key assumptions of our population genetic models and study the processes that govern the patterns and dynamics of genetic variation in populations (see Outstanding Questions).

Key to achieving this goal will be extensive population sampling across time and

Acknowledgments

The authors thank Alan Bergland, Dmitri Petrov, and two anonymous reviewers for critically reading the manuscript and providing valuable feedback. They also thank Andrew Hendry for sharing the data compilation used in Figure 3. N.G.H. and S.P.E. were supported by NSF grant DEB-1256719. S.P.E. was also supported by NSF DEB-1353039.

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Trends in Genetics

ReviewCan Population Genetics Adapt to Rapid Evolution?

Trends

Section snippets

The Standard Model of Population Genetics

Examples of Rapid Phenotypic Evolution in Nature and Experiment

Examples of Rapid Molecular Evolution at Individual Loci

Are Short-Term and Long-Term Evolutionary Rates Different?

Population Genetics Might Be Underestimating the Role of Temporally Fluctuating Selection

Population Genetics Beyond the Standard Model

Population Genetics Should Embrace Rapid Evolution

Concluding Remarks

Acknowledgments

Trends Genet.

Trends Ecol. Evol.

Curr. Biol.

Trends Ecol. Evol.

Trends Genet.

The Causes of Molecular Evolution

The population genetics of adaptation: the distribution of factors fixed during adaptive evolution

Evolution

The genetic theory of adaptation: a brief history

Nat. Rev. Genet.

Detecting natural selection in genomic data

Annu. Rev. Genet.

Methods and models for unravelling human evolutionary history

Nat. Rev. Genet.

Assessing the evolutionary impact of amino acid mutations in the human genome

PLoS Genet.

Frequent adaptation and the McDonald–Kreitman test

Proc. Natl. Acad. Sci. U.S.A.

Genome-wide signals of positive selection in human evolution

Genome Res.

Unpredictable evolution in a 30-year study of Darwin's finches

Science

Evolution of character displacement in Darwin's finches

Science

Causes of lifetime fitness of Darwin's finches in a fluctuating environment

Proc. Natl. Acad. Sci. U.S.A.

Contemporary fisherian life-history evolution in small salmonid populations

Nature

Parallel evolution of Nicaraguan crater lake cichlid fishes via non-parallel routes

Nat. Commun.

Host race radiation in the soapberry bug: natural history with the history

Evolution

Genetic architecture of adaptive differentiation in evolving host races of the soapberry bug, Jadera haematoloma

Genetica

Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata)

Science

Selection analysis on the rapid evolution of a secondary sexual trait

Proc. Biol. Sci.

Over the falls? Rapid evolution of ecotypic differentiation in steelhead/rainbow trout (Oncorhynchus mykiss)

J. Hered.

Rapid evolution of a life history trait

Proc. Natl. Acad. Sci. U.S.A.

Relentless Evolution

Eco-Evolutionary Dynamics

Sustaining fisheries yields over evolutionary time scales

Science

Rapid evolution of a native species following invasion by a congener

Science

Reduction of adaptive genetic diversity radically alters eco-evolutionary community dynamics

Ecol. Lett.

The functional genomics of an eco-evolutionary feedback loop: linking gene expression, trait evolution, and community dynamics

Ecol. Lett.

Eco-evolutionary dynamics in response to selection on life-history

Ecol. Lett.

Experimentally induced host-shift changes life-history strategy in a seed beetle

J. Evol. Biol.

Rapid evolution and the convergence of ecological and evolutionary time

Ecol. Lett.

The peppered moth and industrial melanism: evolution of a natural selection case study

Heredity

Human predators outpace other agents of trait change in the wild

Proc. Natl. Acad. Sci. U.S.A.

Adaptation–not by sweeps alone

Nat. Rev. Genet.

The QTN program and the alleles that matter for evolution: all that's gold does not glitter

Evolution

Natural selection for grazer resistance to toxic cyanobacteria: evolution of phenotypic plasticity?

Review
Can Population Genetics Adapt to Rapid Evolution?