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GG12CH15-Lynch ARI 26 July 2011 11:14

The Repatterning ofEukaryotic Genomes byRandom Genetic DriftMichael Lynch,1 Louis-Marie Bobay,2

Francesco Catania,3 Jean-Francois Gout,1

and Mina Rho41Department of Biology and 4Department of Computer Science, Indiana University,Bloomington, Indiana 47408; email: milynch@indiana.edu2Microbial Evolutionary Genomics, Institut Pasteur, CNRS, URA2171, F-75724 Paris,France3Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN,United Kingdom

Annu. Rev. Genomics Hum. Genet. 2011.12:34766

First published online as a Review in Advance onJuly 13, 2011

The Annual Review of Genomics and Human Geneticsis online at genom.annualreviews.org

This articles doi:10.1146/annurev-genom-082410-101412

Copyright c 2011 by Annual Reviews.All rights reserved

1527-8204/11/0922-0347$20.00

Keywords

complexity, genome evolution, mutation, protein evolution,recombination

Abstract

Recent observations on rates of mutation, recombination, and randomgenetic drift highlight the dramatic ways in which fundamental evolu-tionary processes vary across the divide between unicellular microbesand multicellular eukaryotes. Moreover, population-genetic theory sug-gests that the range of variation in these parameters is sufficient to ex-plain the evolutionary diversification of many aspects of genome size andgene structure found among phylogenetic lineages. Most notably, largeeukaryotic organisms that experience elevated magnitudes of randomgenetic drift are susceptible to the passive accumulation of mutationallyhazardous DNA that would otherwise be eliminated by efficient selec-tion. Substantial evidence also suggests that variation in the population-genetic environment influences patterns of protein evolution, with theemergence of certain kinds of amino-acid substitutions and protein-protein complexes only being possible in populations with relativelysmall effective sizes. These observations imply that the ultimate ori-gins of many of the major genomic and proteomic disparities betweenprokaryotes and eukaryotes and among eukaryotic lineages have beenmolded as much by intrinsic variation in the genetic and cellular featuresof species as by external ecological forces.

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INTRODUCTION

It is generally acknowledged that the biologicalworld was entirely prokaryotic 3 billion yearsago, and that by 2.5 billion years ago, a keylineage had emerged that eventually gave riseto all of todays eukaryotes. Although prokary-otes are the evolutionary cradle of metabolicdiversity and still dominate the earth numeri-cally, the emergence of eukaryotes initiated anenormous radiation of morphological diversity.The factors responsible for this diversificationand the degree to which natural selection playeda role remain unclear.

Based on the attributes shared across theentire eukaryotic domain, we can be reason-ably certain that the ancestral eukaryotic cellharbored a complex genome and a complex in-ternal structure (47, 65, 83), and it is temptingto further assume that the emergence of inter-nal membrane-bound structures was a neces-sary precursor to the evolution of diverse ex-ternal morphologies (50). However, althoughcellular features comprise the physical substrateupon which natural selection operates, intrinsicprocesses operating at the population-geneticlevel dictate the types of paths that are open orclosed to evolutionary exploration within dif-ferent phylogenetic lineages. Here, we reviewthe evidence that alterations in the population-genetic environment played a central and pos-sibly definitive role in establishing the uniquetypes of evolutionary trajectories taken by vari-ous eukaryotic lineages at the genomic and pro-teomic levels.

As the subject material is broad, we willrestrict our attention to three fundamentalissues. First, we will examine the generalphylogenetic patterns of the three main non-adaptive features of the population-geneticenvironmentrandom genetic drift, recombi-nation, and mutationas the relative powersof these forces define the types of evolutionarychanges that are possible in various contexts.Second, we will review the broad set ofobservations on eukaryotic genome structurethat have emerged via the field of comparativegenomics. With considerably more data than

were available in the past, this overview willclearly establish the general boundaries of theoverall genome-architectural landscape withinwhich eukaryotic lineages have wandered overevolutionary time. Third, having establishedthe central role that random genetic drift andmutation have played in the diversification ofgenome structure, we will move to the next rungof the ladder in biological organization, thenature of the proteome, providing suggestivearguments that alterations in the nonadaptiveforces of evolution in the eukaryotic domainare of sufficient magnitude to influence theways in which protein evolution proceeds.New advances in population-genetic theory inthis area provide a potential resource for un-derstanding how complex cellular adaptationsmay have evolved in the ancestral eukaryote.

THE POPULATION-GENETICENVIRONMENT

Although natural selection plays an essentialrole in molding organismal diversity in waysthat ensure population survival, the stochasticnature of the processes of random genetic drift,recombination, and mutation makes it impossi-ble to precisely predict the genomic or pheno-typic responses that will be elicited by any spe-cific selective challenge. However, two thingsare clear. First, evolution follows the dictates ofDarwins descent with modificationnaturalselection operates on standing variation, withthe new variants that arise by mutation andrecombination being defined by the preexist-ing resources. Second, the ability of naturalselection to promote beneficial mutations anderadicate deleterious mutations depends onthe intensity of selection at the gene levelrelative to the power of random genetic drift.If the magnitude of drift exceeds the power ofselection, adaptations that would otherwise goforward cannot be actively promoted, whereasdegenerative mutations with sufficiently mildeffects will accumulate. Although the lattereffect can lead to extinction of a sufficientlysmall population (73, 74), it can also promotenovel paths of evolution as initially deleterious

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mutations that passively emerge at the DNAlevel are secondarily modified into new adap-tive forms. Here, we briefly review how themagnitudes of the three major features of thepopulation-genetic environment scale acrossthe tree of life.

Random Genetic Drift

Random sampling of the gene pool from gen-eration to generation is a ubiquitous sourceof evolutionary stochasticity. The magnitudeof drift is generally defined by the inverse ofthe effective number of gametes sampled pergeneration2Ne in a diploid species, where Neis the effective population size (15). AlthoughNe is generally expected to increase with theabsolute number of reproductive adults in aspecies (N), many additional factors influencepatterns of gene transmission across genera-tions. Most aspects of population structure,such as uneven sex ratios, variation in fam-ily size, nonrandom mating, and localized in-breeding, result in nonrandom representationof genomes across generations, guaranteeingthat Ne < Ni.e., that fluctuations of allelefrequencies across generations will be muchlarger than expected were gametes to be sam-pled equally from N parents.

However, of at least equal importance is thefact that the physical structure of the genomeensures that Ne will be further depressed be-low the expectation based on gamete sampling.This is because the fates of nucleotides at aspecific genomic site are determined by selec-tion operating not just on that site, but alsoon all linked sites under selection. As a con-sequence, the direct effects of some deleteriousmutations can be partially masked by fortuitouslinkage to beneficial mutations and also by thesimultaneous presence of competing deleteri-ous mutations in other individuals. In the ex-treme case of an obligately asexual species, Neis not much more than the number of individu-als in the highest fitness class of the population,as essentially all other individuals represent theliving dead who will leave no long-term de-scendants (29). Likewise, the ability of selection

to promote new adaptive mutations is reducedby linkage, as favorable (nonallelic) mutationsarising on homologous chromosomes cannot besimultaneously fixed unless recombination oc-curs between the two sites. These interferenceeffects from linkage are expected to increasewith