Human Population Genetics

302 Pages·2012·2.088 MB·English

by  John H. Relethford(auth.), Matt Cartmill, Kaye Brown(eds.)

HUMAN POPULATION
GENETICS
Foundations of Human Biology
SeriesEditors:
MattCartmill
KayeBrown
BostonUniversity
TheGrowthofHumanitybyBarryBogin
FundamentalsofForensicAnthropologybyLindaL.Klepinger
TheHumanLineagebyMattCartmillandFredH.Smith
HUMAN POPULATION
GENETICS
JOHN H. RELETHFORD
DepartmentofAnthropology
StateUniversityofNewYorkCollegeatOneonta
AJOHNWILEY&SONS,INC.,PUBLICATION
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LibraryofCongressCataloging-in-PublicationData:
Relethford,John.
Humanpopulationgenetics/JohnH.Relethford.
p.cm.
Includesindex.
Summary:‘‘HumanPopulationGeneticswillprovideanintroductiontomathematicalpopulation
genetics,alongwithrelevantexamplesfromhuman(andsomenon-humanprimate)populations,
andwillalsopresentconceptsandmethodsofpopulationgeneticsthatarespecifictothestudyof
humanpopulations.Thepurposeofthisbookistoprovideabasicbackgroundtextforadvanced
undergraduateandgraduatestudentsinterestinginthemechanismsofhuman
microevolution’’—Providedbypublisher.
ISBN978-0-470-46467-0(pbk.)
1. Humanpopulationgenetics. I. Title.
GN289.R452012
599.93’5—dc23
2011028962
PrintedintheUnitedStatesofAmerica
10987654321
CONTENTS
Foreword vii
Preface ix
1
GENETIC,MATHEMATICAL,ANDANTHROPOLOGICAL
BACKGROUND 1
I. TheScopeofPopulationGenetics 2
II. GeneticsBackground 5
III. PrinciplesofProbability 14
IV. TheAnthropologicalConnection 17
V. AClosingThought 21
2
HARDY–WEINBERGEQUILIBRIUM 23
I. GenotypeandAlleleFrequencies 24
II. WhatisHardy–WeinbergEquilibrium? 30
III. TheMathematicsofHardy–WeinbergEquilibrium 31
IV. UsingHardy–WeinbergEquilibrium 37
V. ExtensionsofHardy–WeinbergEquilibrium 40
VI. Hardy–WeinbergEquilibriumandEvolution 44
VII. Summary 45
3
INBREEDING 49
I. QuantifyingInbreeding 51
II. PopulationGeneticsandInbreeding 62
III. InbreedinginHumanPopulations 65
IV. Summary 75
4
MUTATION 77
I. TheNatureofMutations 77
II. ModelsofMutation 81
III. MutationalHistoryandAnthropologicalQuestions 88
IV. Summary 96
v
vi CONTENTS
5
GENETICDRIFT 101
I. WhatisGeneticDrift? 102
II. GeneticDriftandPopulationSize 112
III. EffectsonGeneticVariation 120
IV. MutationandGeneticDrift 121
V. CoalescentTheory 125
VI. Summary 131
6
MODELSOFNATURALSELECTION 139
I. HowDoesNaturalSelectionWork? 140
II. AGeneralModelofNaturalSelection 145
III. TypesofNaturalSelection 147
IV. OtherAspectsofSelection 160
V. Summary 167
7
NATURALSELECTIONINHUMANPOPULATIONS 181
I. CaseStudiesofNaturalSelectioninHumanPopulations 182
II. AreHumansStillEvolving? 198
III. Summary 203
8
GENEFLOW 205
I. TheEvolutionaryImpactofGeneFlow 206
II. ModelsofGeneFlow 208
III. GeneFlowandGeneticDrift 213
IV. EstimatingAdmixtureinHumanPopulations 226
V. Summary 230
9
HUMANPOPULATIONSTRUCTUREANDHISTORY 237
I. CaseStudiesofHumanPopulationStructure 238
II. TheOriginofModernHumans 242
III. CaseStudiesofPopulationOrigins 247
IV. Summary 255
Glossary 257
References 267
Index 279
FOREWORD
If, like us, you find yourself hard-pressed to follow the fast-paced scrimmages
of anthropological genetics from the sidelines, this is the book you have been
waiting for. John Relethford, one of the world’s leading contributors to these
debates, has written it to engage all of us in this important and rapidly evolving
areaofscientificinquiry.InHumanPopulationGenetics,heleadsusthroughclassic
studiesandcurrentdebatesinaneasy,clear,informalstylethatdrawsusinand
involves usintheaction andarguments. Relethford’s passionforunderstanding
thegeneticsofhumanpopulations,andhislow-stressapproachtowhatcanbea
difficultandesoterictopic,kindlealikepassioninthereaderandmakethisbook
thatrarethingamongtextbooks—asourceofexcitementandinspiration.
Populationgeneticsandstatisticaltheorywerebornasconjoinedtwinsinthe
monumental work of R. A. Fisher in the 1920s, which transformed evolutionary
biology into a full-fledged science capable of making and testing predictions
with numbers in them. But many people who are eager to learn about human
biologyandevolutionareturnedoffbythestatisticalfoundationsofevolutionary
theory.Almosteveryonewhoteachesthefundamentalsofoursciencehaslearned
to dread the dazed expressions that come over students’ faces the moment the
Hardy–Weinbergequationhitsthescreen.Relethfordshowsus,andthem,howto
getaroundthisstumblingblock.Drawingthereadereffortlesslyinthroughplain
andsimpleexamplesbeautifullychosentoclarifythemathematicsofprobability,
Relethford recruits his mastery of the subject and his skill as a teacher and
writertopresentthemathinauser-friendlywaythatdisplacesthehardworkof
derivingformulasintoadjacentappendices.Hisreadersfirstmastertheessentials
and later reward themselves by seeing the mathematics underlying the simple
modelstheyhavejustgrasped.Thisprocessoforderlypresentationleavesreaders
self-confidentandreadytotakeonevermorecomplexmaterial.
Throughoutthisbook,Relethfordsystematicallypreachesandteachesascien-
tificapproach toknowledge (‘‘Muchofscienceconsistsofdevelopingasimplemodel,
testing its fit in the real world, and then explaining why and how it fits and does not
fit’’) in a way that always solicits involvement by the reader (‘‘To see this, let
us try an example’’). In every topic he presents, he returns to the readers’ point
of view (‘‘What effect do you think selection has had on the allele frequencies?’’) and
includes them in the developing narrative. His readers will learn the concepts
thatarecrucialtoallfieldsofpopulationbiologybystudyingexamplesofspecial
relevancetobiologicalanthropology—howfamiliaritywithgeneticevidencecan
vii
viii FOREWORD
informusofourhistory(seetherichdiscussionontrackingtheappearanceofthe
CCR5-(cid:2)32alleleandsubsequentresistancetotheAIDSvirus),howadaptationhas
takenmanydifferentpathsinhumanhistory(seethediscussionondifferenthigh-
altitude adaptations in Tibetan and Andean people), and how cultural behavior
impacts genetic processes (see the discussion on agriculture and hemoglobin S).
‘‘Instead of cultural evolution negating genetic evolution,’’ he writes, ‘‘we are
findingevidenceofhowculturalchangehasacceleratedgeneticevolution.’’
That sentence, and the evidence behind it, would by itself make Human
Population Genetics worth having on your bookshelf. Every chapter of the book
sparkleswithconclusionsthatarejustassimple,straightforward,andfar-reaching.
AllofitsreaderscanrelyonJohnRelethfordtoleadthemintosomeofthemost
importantandexcitingscientificconversationsofourday.Ifyouareastudentof
biologicalanthropologyatanylevel,orascientistoreducatorwhoteachesthese
subjects,youwillfindhisnewbookaninvaluablesourceofnovelinsightsandfresh
illumination of key ideas. We are proud and delighted to see Human Population
Genetics added to the Wiley–Blackwell series of textbooks on the foundations of
humanbiology.
KayeBrown
MattCartmill
PREFACE
WHAT ARE WE DOING HERE?
Thisbookisabouttheintersectionofmathematics,biology,andanthropology.As
such,ithastwobasicgoals.First,thebookprovidesanintroductiontothestudyof
populationgenetics,whichprovidesthemathematicalbasisofevolutionarytheory
by describing changes in the frequency of genetic variants from one generation
to the next. Second, this introduction has been designed for specific application
to human populations. Although population genetics is a field that applies to
all organisms, the focus throughout this book, particularly in case studies, is on
human populations. As an anthropologist, my interest is by definition primarily
on human populations and genetic diversity. Not that this book has no utility
outsideofhumanpopulations—farfromit.Ihavedesignedthisbooktoprovide
asimpleintroduction topopulation genetics withminimal mathematics thatcan
beusedbyadvancedundergraduateandgraduatestudentsinavarietyoffields,
including anthropology, biology, and ecology. If you are using this book in one
of those other disciplines, rest assured that the same basic principles presented
here are applicable to organisms, and your instructor will likely provide other,
nonhuman,casestudiesforclarification.Youneednothaveadetailedbackground
ingenetics,althoughthisbookisintendedforstudentsthathavehadsomeinitial
grounding in genetics, such as one would obtain from an introductory course in
biologicalanthropologyorbiology.
FORMAT AND ORGANIZATION OF THE BOOK
Aquicklookthroughthepagesofthisbookwillrevealanumberofformulas.This
may seem intimidating, but it is not. Although some elementary mathematics is
neededtounderstandpopulationgenetics,wedonothavetouseveryadvanced
math to learn the basics. Throughout this book, we will use only simple algebra
ofthetypethatyoulikelylearnedinmiddleorseniorhighschoolandsomebasic
concepts of probability, which are developed in the text as we proceed. I also
use additional ways, beyond equations, to present the material. Although it is a
wonderful experience to glance at a mathematical formula and gain immediate
insight into what that formula says about reality, it is (at least for me) a rare
ix
x PREFACE
experience. I usually have to look at a graphic representation of the formula or
utilizeananalogytounderstandtheunderlyingideas.Thus,thistextusesalotof
graphsandanalogiestomakethebasicpointsandhelpyourelatetheevolutionary
processtomathematicalideas.
As with any field, population genetics has its own set of terms. Anything
specifictogeneticsorpopulationgeneticsisdefinedinthetext,withanadditional
glossary at the end of the book collecting all such terms. All glossary terms are
marked in boldface in the text the first time they appear. In-text citation is used
inthistext,wherespecificcitationsarereferencesbyauthor(s)name(s)andyear,
suchas‘‘Relethford(2004).’’
ACKNOWLEDGMENTS
IowemuchthankstoMattCartmillandKayeBrown,serieseditorsoftheWiley-
Blackwell Foundation of Human Biology series, for inviting me to write this book,
andfortheircarefulanalysisanddiscussionofthebook’sgoalsandstructure.Iam
alsoverygratefulfortheguidanceandadviceofmyeditor,KarenChambers.She
was a delight to work with on this project. Thanks also to Anna Ehler, Editorial
Assistant,andRosalynFarkas,ProductionEditor,foralloftheirhelpandattention
tomyconstantquestions.
Iwasfirstintroducedtothestudyofpopulationgeneticsin1975whenImet
mygraduateschooladvisor,FrancesLees.IoweFrankalotforhisguidanceand
friendship over the years in addition to his patience at teaching me population
genetics. He got me started both in my profession and in this particular field. I
amalsoverygratefultohisacademicadvisor,MichaelCrawford,forhelpingme
learn even more about population genetics over the course of several decades of
friendshipandcollaborationonresearchprojects.
Ihaveworkedwithothercolleaguesonresearchinhumanpopulationgenetics.
Two of these colleagues stand out in particular—John Blangero and Henry
Harpending.Myworkwiththemhasbeenahighpointofmycareer.
Lookingback,Icanidentifymanyfriendsandcolleaguesovertheyearswith
whomIhaveshareddiscussionsatsomeleveloranotheronpopulationgenetics.
Someofthesehavebeencoauthors,andothershavebeencolleagueswithsimilar
interests who have shared one or many conversations or emails. They all have
contributedtomyunderstandingofhumanpopulationgenetics.Needlesstosay,
myerrorsaremineandminealone.Thisisthelist(andmymostsincereapologies
if I have missed anyone): Guido Barbujani, Deborah Bolnick, the late Ellen
Brennan, Ranajit Chakraborty, Ric Devor, Ravi Duggarali, Elise Eller, Alan Fix,
Jon Friedlaender, Rosalind Harding, Mike Hammer, John Hawks, Jeff Heilveil,
KeithHunley,CashellJaquish,LynnJorde,LyleKonigsberg,TiborKoertvelyessy,
KenKorey,thelateGabeLasker,PaulLeslie,JeffLong,LorenaMadrigal,Andrea
Manica, Yoshiro Matsuo, Jim Mielke, Andy Merriwether, John Mitchell, Kari
North, Carolyn Olsen, Esteban Parra, Alan Rogers, Charles Roseman, Dennis
O’Rourke, Lisa Sattenspiel, Michael Schillaci, Tad Schurr, Steve Sherry, Peter
Smouse, Bob Sokal, Dawnie Steadman, Anne Stone, Mark Stoneking, Alan
Swedlund, Alan Templeton, Forrest Tierson, John VandeBerg, Noreen von