RECOMBINATION VARIABILITY AND EVOLUTION ALGORITHMS OF ESTIMATION AND I'OPL'LATION-GENETK MODELS Copyrighted material Copyrighted material Copyrighted material Recombination Variability and Evolution Copyrighted material Copyrighted material Recombination Variability and Evolution ALGORITHMS OF ESTIMATION AND POPULATION-GENETIC MODELS A.B Korol Institute of Evolution, University of Haifa, Israel LA Preygel Genetic Therapy Inc Gaithersburg USA and S.I Preygel Oncor, Inc., Bethesda USA El CHAPMAN & HALL London ■ Glasgow > Weinheim * New York - Tokyo ■ Melbourne ■ Madras T h i s One PZYN-UXU-D9HT Published b> Chapman and Hall - Boundary Row, London SEI 8IIN UK Cliapman and Hall - Boundary Row London SE! 8HN UK Blaekie Academic and Professional Wester Cleddens Road Bishopbrtggs Glasgow G64 2NZ UK Chapman and Hall GmbH Pappelallee Í 69469 Weinhelm Germany Chapman and Hall USA One Penn Plaza 41st Floor New York NY 10] 19* USA Chapman and Hall Japan, ITP-Iapan Kyowa Building, *F 2-2-1 HLrakawacho Chiyodn-ku» Tokyo 102 Japan Chapman and Hall Australia Thomas Nelson Australia 102 WxUis Street South Melbourne Victoria 1205 Australia Chapman and Hall India R Scshadri, 12 Second Main Road (IT East Madras bOO India Pint edition 1994 © 1994 A.B KoroL LA Preygel and S.I Preygel Adapted from Russian language edition - Variability of Crossin$over in tii$\ttr Organisms: Methods of analysis and Population Genetic Models - 1990 A.B Korol [.A Preygel and S.I Preygel Published by Shtilntsa Press Kishinev Moldova Typeset In IO/12 Photlna by Thomson Press lindia) Ltd New Delhi India Printed In Great Britain by T.| I*ress iPadstowl Ltd Padstow Cornwall ISBN O 412 4S410 Apart from any fair dealing for the purposes of research or private study, or criticism or review, as permitted under the UK Copyright Designs and Patents Act 198ft this publication may not be reproduced, stored, or transmitted, in any form or by any means, without the prior permission in writing of the publishers, or in the case of reprographic reproduction only in accordance with the terms of the licences issued by the Copyright licensing Agency in t h e ! "K or in accordance with the terms of licences issued by the appropriate Reproduction Rights Organization outside the UK Enquiries concerning reproduction outside the terms stated hen? should be sent to the publishers at the London address printed on this page The publisher makes no representation, express or implied, with regard to the accuracy of the information contained in this book and cannot accept any legal responsibility or liability for any errors or omissions that may be made A catalogue record for this book is available from the British Library Library oí Congress Catalog Card Number: 94-70270 (¿j Printed on acid-frcc text paper, manufactured in accordance with ANSI/ NIS0ZJ9.48-1992 and ANS1/NIS02J9 41* 1984 Permanence of Paper) Contents Prpfarp vil Acknowledgements ix Inlrmlnrtinn Part One | ESTIMATION Ol HH OMHINATION Z General survey of methods for estimating recombinational variability 1.1 Recombination ÜS a source of genetic variation 1.2 Spectrum of rcconibinalional variability 1.Í Kvaluatinu changes in variability spectrutn 1,4 Marker and evtolosical analysis of recombination 9 li l_h 24 Marker analysts 2.1 Formulation of genetic recombination 2.2 LstimathiR recombination from experimental data Í Some examples of crossing-over frequency estimation 2.4 Allowing for data heterogeneity In estimating linkage 2.5 Models of quasMmkage JO 50 i_7 4fi S_l 55 Marker analysis of quantitative traits L1 The Mendelian approach to quantitative variation L2 Estimating (JTI, marker linkage in controlled crosses 71 7] 76 Li Quantitative trait analysis with two and more markers 92 L4 L5 Marker analysis of a set of quantitative traits (ieneral discussion and prospects of the problem Part Two 11)1 104 POPULATION GENETIC MODELS OF INTERACTION BETWEEN SELECTION AND RECOMBINATION The genetic system and recombination 4.1 The 'genetic system* concept I_L5 117 117 Copyrighted material CONTENTS 4*2 4.3 4.4 Rernmhinalion n n n - r a n H n m n ^ Linkage of co-adapted and functionally related genes Parallelism of synlenic groups Effect of r e c o m b i n a t i o n o n p o p u l a t i o n genetic s t r u c t u r e 5.1 The genome integrity as a protection against excess variability InftTactinn between election and rccomhination LÍÜ JJJ Evolution of t h e system controlling r e c o m b i n a t i o n 6.1 A review of theoretical explanations 6.2 Genetic variation in exchange frequency and distribution 6.3 Artificial selection for altered recombination frequency 6.4 Two problems in explaining the rec system evolution ) 5ft 15£ 125 186 192 OS Selection for Increased r e c o m b i n a t i o n d u e to ^nilrnnmrnf^l niirtnafimiB Q» 7.1 7.2 7.3 7.4 13& 1Ü9 202 212 The problem Description of the model Results Experimental modelling of the rec system microevolullon & Species I n t e r a c t i o n s as a factor in t h e evolution of i recombination ÜJ [nimducUQD 8-2 A model of co-evolution with selection on gene combinations & J A model of r e v o l u t i o n with selection on the characters 'resistance' and Virulence' 8.4 The rec system evolution under intraspecitic competition 22 if) Í3 Evolutionary i n t e r p r e t a t i o n of r e c o m b i n a t i o n phenomenology 9.1 The role of recombination dependence on environment i 9,2 The evolution of dominance of rec genes i Linkage between the rec modifier and its target region: a possible evolutionary model a rt Three CONf I IDIOMS rnnrlnglnng 2JLZ 2S*J i References Inde» 294 155 Copyrighted material 356 INDEX Dominance at rec loci 190 221-2 241, 272-7,280 Drosophlla 24 33 58 59 76 108 119 126 131 133 148-51 160 166 176-7 178-82 18&-9 196 213-25 266 267 269.370-1.273 E coll 24 126 162 165.269 Effects ('functions1! of recombination repair 5.128.136.162.163, 164-7 169 see also DNA repair segregation 167-8 combinative (gene mixing) 162 165 192 regulation of gene activity 164 Enhancers oí recombination 162 168 176,273 Evolution of Mcndellan rules 59 196 Evolution of recombination non-randomness, adaptations! hypothesis 130 137, 196 289 'relay race' principle 19 Í theoretical models, see Models of recombination evolution Exchange distribution 14 27 130 139 160 196.280.283.284 289 see also Crossover distribution: Nonuniformity of exchanges Exchange frequency 14, 214 280 281.284.289 Feedback regulation of genetic variability 159 270-1.273.291-2 selection for recombination 169, 202.261.278 selection for it-properties 194-5 'Fine control' of recombination 127 129 Fitness components, see Selection Frttiltaria 24 281 F'System, see Genetic system 'Functions' i effects) of recombination conservative 170-1 192 195 197 prospective 170-1 197 270 see also Effects ("functions') of recombination Gametic correlation, see Linkage disequilibrium Gametic disequilibrium, see Unkage disequilibrium Gametic selection, see Selection Gene block 19.25 71, 75 120 | , 172,243 see also Gene clusters clusters 130* 134 244 conversion, see Conversion Genetic control of recombination 187 188 see also Recombination, system; Modifiers, of recombination; rec modifiers Genetic counselling 73 see also Unkage disequilibrium: Marker loci Genetic drift 141.146.151.154 Genetic flexibility 118, 120 157 239, 261 283 290 291 Genetic load 162 163 239 269 Genetic system classification 120 definition and functions 117-18 of individual adaptation (F-syslem) 118 156 195.291 and polymorphism 120 266, 267 of population adaptation (It-system) 72 118, 194-5 196 2$9 270 290-1 Genetic variation, see Variation Genome congealing 159 171, 264 Genotype-environment interaction 107-8.201.227 Graphical genotype representation 25 Grasshoppers 153 177, 284 Group selection 122 161 285 Gryllotalpa 151 Haemophilus influenza? 16 Haldane-Huxley rule 168.280 see also Sex difference in recombination Heteroch roma tin effect on recombination 59 123, 127 177 possible role in quasi-linkage 59 66 Heterogeneity of recombination rates 51—», 176-9 see also Recombination Hitch-hiking due to linkage 146,204,278 due to non-random mating 147 see also Modifiers Copyrighted material INDIA HLA system 146 151, 229, 244 Horizontal gene transfer i Host-parasite interaction 228-3 243-5 see also Models of recombination evolution Hotspots of recombination 25, 126 129 151,244 Human 24, 25, 45 126 128, 134, 146 160.280.281.284 see also Man Hybrid disgenesis connection with quasi-linkage 58 effect on recombination, see Mobile elements Importance of recombination 2-3 It) 141 153, 164.212 Imprinting 59 Information matrix 39 Insertional mutagenesis in targeting QTL 111-12 Intcrchromosomal effect on recombination 127, 222 Interference changes due to selection for thermoadaptation 219 221-2 connection with crossing over rale 33 definitions 31 32 effect of meiotic mutants 33, 129 negative 31 33,94,98, 180 positive 31, S3 Interspecific backcross (intercross! mapping, see Mapping, multilocus approach Interspecific transfer of recombinationrepair genes 136-7 Introgression 12 22« 35 73 153 Introns as 'traps* of recombination errors 128-9 Inversions, effect on frequency of lethals 166 recombination 176 Inversions, gametic disequilibria with markers 152-3 with other inversions 153 Kosamhi mapping function 35 50.61, 96 see also Mapping functions Lettuce , 55 357 Ulitwetie 160 Lima beans 190 Linkage and evolution of resistance to pesticides 135 of functionally related genes 30-3 of a modifier to its target region 207-12, 250.277-80 parallelism, see Synteny tightening 218 29} see also Genome congealing Unkage disequilibrium cytonuclear 153 definition 142 difficulties in interpretation 145-7 effect of three-locus interactions 146 in hybrid zones 145 153 implication for genetic counselling 51 for marker assisted breeding 73 151 in inbreeders 153-6 in outbreeders 132.149-53 oscillations due to intraspecific competition 257-8 due to species interaction 235-7 251-2 review of theoretical models 142-4 role in recombination evolution 170-1 173.213.226 within structural genes 151 I jzards 177 Locusts 121 190 Lod score 42,45,80, 98 Maize , , 5 , , 177 24K 267 281 Mammals 59, 126 133-4, 165 214 285 Man 24, 28, 56, 134 160 177 see also Human Map distance 30, 45 50 85 Mapping cloned sequences employing yeast recombination 29 multilocus approach 40 43-6 53 physical 28, 73 software 46 47 using hybrid somatic cells 28 using individual sperm cells 28 Mapping functions definition 30 33-4 Copyrighted material 558 INDEX Mapping functions contd differential equation approach 34-6 metrical theory approach 37 44-5 see also Kosambi mapping function Marker analysis of QTL dependence on environmental conditions 108 110 flexible specification of the trait density functions 81 interval analysis 93.98-9 maximum likelihood (Ml-), see Method of maximum likelihood method of moments, see Method of moments in QTL-marker linkage analysis mixture model of single marker analysis 77-8 multiple regression method 99-101 possible statistical approaches 79-80 resolution power 86-9 robustness of the models 80 89-92 105 Marker loci allozymes (isozymes) 149-50 154 distribution in the genome 124-5 130-3 heteroduplexes 26 micro- and minisatellltes 25 51 104 127 see also VNTR PCKandRAPD 26,95 104 potential applications 25.72-4,151 see also Quantitative variation: Marker analysis of QTL RFLP - 112 151 VNTR 26.70 Mean fitness arguments of recombination evolution 161 168 230 262^1 dependence on recombination rate 160 168.237-8.262 principle 168.237.264 Meiosis repair role, see Effects ('functions') of recombination vulnerability to unfavorable conditions 227 290 Melotic drive 196 see otso Segregation distortion 'MeioUc effect* 166 Melotic mutants effect on fitness 169 effect on recombination 27 129-30 167-8 196 effect on segregation 167 Mendellan analysis of quantitative variation, see Quantitative variation Method of genetic operators 201 248 257 Method of moments in QTL-markcr linkage analysis 82-5 connection with the multiple regression method 100-1 Method of maximum likelihood analysis of quasi-linkage see Quasilinkage, models estimation of linkage between marker loci 38-tO QTVmarker linkage analysis 80-1 98-9 103 MHC locus 126.244 see also HM system Minisatellltes as genetic markers, see Marker loci recombinogenic effect 126 127 244 Mobile elements effect on fitness 112.119.135.181 effect on recombination 126 128 181-2,222 stress induced transpositions 267 270 using in QTL targeting, see Insertional mutagenesis in targeting QTL Model organisms 1-2 24 76 Models of recombination evolution antagonistic species Interaction 227-41.245-55 classification 170-3 226 228 245 hierarchical 274, 279 intraspecific competition 172, 227 255-8 selection against harmful mutations 136 161-4 171-2, 173 selection in fluctuating environments 170-1, 202-6 276 Modifiers of co-selection 194.204.221 239-41 253-6 of dominance 272 274-7 of hitch-hiking 169, 171 204 209, 255 of interference 222 of mutation rate 175, 211 256 Copyrighted material i 59 IMJKX of recombination 168-9 176 207 221 see also Models of recombination evolution of recombination dependency on environment 264-5 Vtosqultoltsh 153 Mouse , 5 280 285 Mule 55 Mullers ratchet 161-2 163 Multigcne families and recombination 11 119 136 194 245 Multtlocus systems , - 154-5 221.246-55 Multiple exchanges 24 33.43,130, 180 see also Interference Multivariatc fmultitrait) analysis 18-22 99-101 102-4, 112 Mutationrate 2.160.162.175.194 284 Neurospora 55, 177 191 Neutrality of recombination controlling genes 168-9 Non-random fertilization (sperm selection) 151.285 Non-uniformitv of exchanges 112-^> 136.289 see also Exchange distribution: Crossover distribution Norm of reaction 72 108 261 Normal distribution 74 88 105 Oat 153,154 Orthogenesis 55 Oryzias latipes 281 Peas 24, 55, 177 Pepper 135 177 PhageT4 162 Pine 24 151 152 Plasmodium falciparum 14 Poecttia 56 Polymorphism maintenance 141.171.199.201-4 of molecular markers 26 for nv-genes 159 169 176 see also Heterogeneity of recombination rales see also Genetic system Potato 24, I 34-5 Power of linkage test of QTL-marker analysis 106-7 see also Marker analysis of QTL resolution power Primula 131 Quantitative trait loci (QTL) analysis of interaction 100-1 assumptions of the marker analysis 75 77 79 89-90 105 prospects for cloning 73, 111-12 Quantitative variation biometrical approach 71 Mendelian approach 72-5 144 robustness of the models 90-2 see also Marker analysis of QTL; Quantitative trait loci I QTL I Quasi-linkage definition 55 evidence 55-7, 64-70 hypotheses (mechanisms) 57-9 models 60-4 Rana 56 'Reacting' system of recombination, see Recombination, system 'reacting* component RecA gene 165 rec modifiers, see Modifiers, of recombination Recombinant inbred lines 41-2 107 Recombination artificial selection, see Selection, for recombination critical values, ensuring oscillator>' regimes of population dynamics 143 233 permanent linkage disequilibrium 142-4 150 and evolution of diploidy 162 165 19J frequency (r/l 30 functions, see Functions ('effects') of recombination and life history traits 112.122 178 241.258 intragenic 127 129-30 nodules 27 response to mutagenic factors 165 266 270 and segregation 167-8 in somatic cells 119 16 3, 164 Copyrighted material 360 INDEX Recombination contd as a source of genetic variation 9-10 spindle 17 system 'controlling' component 126 192 221 definition 120 'reacting* component 125 130 136 178 and transcription 128 30, 268-9 and transposable elements 181-2 see also Mobile elements upon distant crosses 40 182-6 Recombination changes caused by selection for body weight and litter size In mouse 214 flowering time in mustard plants 214 geotaxls In Drosophlla 222-4 resistance to DDT in Drosophlla 213-14 resistance to nutrient medium variation in yeast 214 thermoadaptation in Drosophila 217-22 Recombination, dependence on cytoplasm 177 distance to the centromere 123 127 environment 129 176 178 179 261, 267 genotype 176 178-9 heteroch roma tin see Heteroehromatin effect on recombination Inbreeding and crossing 42 organisms fitness 159 169, 270-1 sex 48 160 190.282 see also Sex difference in recombination Recombinational (synthetic) lethals 59 133 rec-system see Recombination, system Red Queen" hypothesis 227 'Reduction principle* of modifier evolution 158-9, 277 Repair, see DNA repair: Effects ('functions') of recombination RFLP, see Marker loci Rice 24 R-system see Genetic system Rust 243 ( 245 Rye 27.123 177 Scale transformation 90 Schizophyltum 177 191 Sciaria corpophila 56 Segregation distortion 38 47 196 285 see also Meiotic drive Selection cyclical 201^», 255 density-dependent, see Models of recombination evolution directional 198.212.224.255 frequency-dependent 170 228, 230, 233 257 see also Models of recombination evolution at gamete level 59,61.283-5 in hybrid zones, see linkage disequilibrium multilocus* estimation of components 155-6 for recombination direct 186-91 induced (secondary) 169 198 204-12.213 see also Recombination changes caused by selection for sexual, see Sex difference in recombination stabilizing 16.19.158.204.291 two-locus models 141 142-3 Sequential analysis in QTL mapping 110 Sex chromosome 281-2 Sex difference in recombination accounting of in genetic analysis 48-51 evidence 49-50.280-1,284 see also Recombination, dependence on sex Ncfs model of evolution 282 Trivers' model of evolution 283 Shizosaccharomyees pombe 31 Slb-competition 72, 227 257 see also Models of recombination evolution Silkworm 77 190 Snail 177 Stress 14.23 110 140, 155 169 222 266 270 292 Synaptonemal complex 281 Copyrighted material INDKX Synleny 133-5 Sugarbeet 24 Supergenes 131.135 143, 159 282 Tangled Bank' hypothesis 221 Telomeres, possible role in quasMinkage 58,66 Temporal* principle of genome organization 135 Terminal localization of exchanges, see Exchange distribution l-locus 285 Tobacco 55 Tomato 56 57 64-70 93 96-8 109 110 124 131-2 134 183-6.241.270-1.281 Transcription, see Recombination, and transcription Transformation complementation of repair mutants by foreign genes 137 QTL targeting, see Inscrtional mutagenesls In targeting QT1, Transgression 12.22 TransposaWe elements (TE) 112 181 see also Mobile elements Tribalium castamum 189-90 J61 Variation anomolous 12 free 10-11.266 potential 10-11.266 of recombination adaptatkmist interpretation 12 136 195-6 between species 160 166 extrabinomial 52 54 within the genome 122-30 within species 17&-9 187 188 ■■V ' also Recombination restriction 17-18 spectrum definition 14-16 estimation 18-23 set* also Multlvariate (multitrait) analysis VNTR see Marker loci Wheat 55 123 155 177,241 X chromosone, see Sex chromosome Yeast 126.127.160.214.270 Z4)NA effect on recombination 126 Copyrighted material Copyrighted material Copyrighted material Copyrighted material Copyrighted material Copyrighted material Copyrighted material Copyrighted material Copyrighted material Recombination Variability a n d Evolution A l g o r i t h m s of e s t i m a t i o n a n d p o p u l a t i o n - g e n e t i c models A B K o r o l , I.A Preygel a n d S.I Preygel Using an interdisciplinary approach, the authors provide an adaptionist interpretation of the basic features of recombination, its evolutionary significance as a key process in reproduction and its importance in genetic mapping The book synthesizes much recent Information in the fields of evolutionary genetics of recombination, the analysis of genetic markers and breeding applications The authors analyse recombination through a consideration of computer models, large Drosophifa populations and an empirical approach to current theories Practically-orientated readers will be interested in the discussion of a wide spectrum of mapping methods and the new algorithms proposed for genetic mapping of quantitative loci Abraham Korol is Professor at the Institute of Evolution, University of Haifa, Israel Ilya Preygel is a computer specialist at Genetic Therapy Inc., Gaithersburg, USA and Sophia Preygel works at the MIS depart ment of Oncor Inc based in Bethesda, USA Also available from Chapman & H a l The Evolution of Asexual Reproduction in Plants M Mogie Hardback (0 412 44220 5) 288 pages Evolutionary Developmental Biology 8.K Hall Hardback {0 412 27550 31 2B8 pages Non-neutral Evolution Theories and molecular data Golding Paperback (0 L about pages CHAPMAN & HALL London Glttgow Wtmhom Nwr YoA Tokyo Uafcoum* Mtfa» ...Copyrighted material Copyrighted material Copyrighted material Recombination Variability and Evolution Copyrighted material Copyrighted material Recombination Variability and Evolution ALGORITHMS OF ESTIMATION. .. the main process ( Copyrighted material I 11 RECOMBINATION AS A SOURCE OF (¡liNITIC VARIATION Free vanaDifrty AABB+aabb + aaSS ^ Aat)t> + ^ration / • Mutatton Migration Mutation Re~mb.na.cn... mechanisms and genetic control of recom bination (b) genome mapping and marker analysis of quantitative traits and {c) the evolution of recombination, unrelated as they might seem land really are»,