Foreword ...................................................... xiv
Richard Lewontin
Preface ....................................................... xvi
List of Contributors ......................................... xvii
1 Introduction ................................................. 1
Rama S. Singh, Jianping Xu, and Rob J. Kulathinal
1.1 A gradualist history .................................... 1
1.2 Mechanisms of rapid and episodic change ................. 2
1.2.1 Unconstrained neutral space ...................... 2
1.2.2 Horizontal gene transfer ......................... 3
1.2.3 Developmental macromutations ..................... 3
1.2.4 Evolution by gene regulation ..................... 3
1.2.5 Coevolutionary forces ............................ 4
1.2.6 Sexual selection and sexual arms races ........... 4
1.2.7 Population demography and genetic revolutions .... 5
1.2.8 Adaptive radiation ............................... 5
1.3 Punctuated equilibrium within a microevolution
framework ............................................... 5
1.4 Tempo, mode, and the genomic landscape .................. 6
1.5 'Rapidly evolving genes and genetic systems': a brief
overview ................................................ 7
1.6 Future prospects ........................................ 8
Part I From Theory to Experiment
2 Theoretical perspectives on rapid evolutionary change ....... 13
Sarah P. Otto
2.1 Introduction ........................................... 13
2.2 When is strong selection strong? ....................... 13
2.3 Does strong selection differ in kind from weak
selection? ............................................. 16
2.4 Concluding thoughts .................................... 20
3 Recombination reshuffles the genotypic deck, thus
accelerating the rate of evolution .......................... 23
Mihai Albu, Amir R. Kermany, and Donal A. Hickey
3.1 Introduction ........................................... 23
3.2 Simulating selection on multilocus genotypes ........... 24
3.3 Discussion ............................................. 27
3.4 Conclusions ............................................ 29
4 Heterogeneity in neutral divergence across genomic regions
induced by sex-specific hybrid incompatibility .............. 31
Seiji Kumagai and Marcy K. Uyenoyama
4.1 Introduction ........................................... 31
4.1.1 Detecting incompatibility factors ............... 31
4.1.2 Within-species polymorphisms for
incompatibility factors with sex-limited
transmission .................................... 31
4.2 Genealogical migration rate ............................ 32
4.2.1 Definition ...................................... 32
4.2.2 Non-sex-specific incompatibility ................ 33
4.2.3 Sex-specific incompatibility .................... 33
4.3 Applications ........................................... 33
4.3.1 Mitochondrial introgression ..................... 33
4.3.2 Interpreting region-specific Fst ................ 35
4.4 Conclusions ............................................ 37
5 Rapid evolution in experimental populations of major life
forms ....................................................... 40
Jianping Xu
5.1 Introduction ........................................... 40
5.2 Features of experimental evolution ..................... 41
5.3 Types of experimental evolution ........................ 42
5.3.1 Directional selection ........................... 42
5.3.2 Adaptation ...................................... 42
5.3.3 Mutation accumulation ........................... 42
5.4 Rapid change and divergence among mutation
accumulation population lines .......................... 43
5.4.1 Microbial growth rate ........................... 43
5.4.2 Other microbial traits .......................... 45
5.4.3 Plants and animals .............................. 45
5.5 Adaptation and directional selection experiments ....... 47
5.5.1 Adaptation of E. coli populations ............... 47
5.5.2 Adaptation of viral populations ................. 47
5.5.3 Adaptation and directional selection in fruit
flies ........................................... 48
5.5.4 Adaptation in yeast ............................. 48
5.5.5 Directional selection in mammals ................ 48
5.5.6 Correlated changes between traits ............... 49
5.5.7 Acquisition of novel phenotypes ................. 49
5.6 Genomic analysis of experimental evolution
populations ............................................ 50
5.7 Conclusions and perspectives ........................... 50
Part II Rapidly Evolving Genetic Elements
6 Rapid evolution of low complexity sequences and single
amino acid repeats across eukaryotes ........................ 55
Wilfried Haerty and G. Brian Golding
6.1 Introduction ........................................... 55
6.2 Rapid evolution of low complexity sequences ............ 55
6.2.1 Mutational processes ............................ 56
6.3 Rapid divergence of LCRs and their impact on
surrounding sequences .................................. 57
6.3.1 LCRs as indicators of regions of lowered
purifying selective pressures ................... 57
6.3.2 Mutagenic effect of LCRs ........................ 58
6.4 Low complexity sequences under selection ............... 59
6.4.1 Deleterious effects of LCR size variation ....... 59
6.4.2 DNA composition ................................. 59
6.4.3 LCR distribution ................................ 60
6.4.4 Phenotypic effects of LCR size variation ........ 60
6.4.5 Selection for low information content ........... 61
6.5 Perspectives ........................................... 61
7 Fast rates of evolution in bacteria due to horizontal gene
transfer .................................................... 64
Weilong Hao
7.1 Introduction ........................................... 64
7.2 Quantifying horizontal gene transfer ................... 65
7.3 Understanding the variation of gene gain and loss ...... 66
7.4 Horizontal gene transfer in duplicated genes ........... 67
7.5 Pseudogenization of horizontally transferred genes ..... 67
7.6 Mobile sequences and gene movement ..................... 68
7.7 Gene exchange goes fine-scale .......................... 69
7.8 Conclusions ............................................ 69
8 Rapid evolution of animal mitochondrial DNA ................. 73
Xuhua Xia
8.1 Introduction ........................................... 73
8.2 Mitochondrial replication, strand bias, and
evolutionary rates ..................................... 74
8.3 The change in genetic code and evolutionary rate ....... 77
8.4 The change in tRNA genes and evolutionary rate ......... 79
8.5 Conclusions ............................................ 81
9 Rapid evolution of centromeres and centromeric/kinetochore
proteins .................................................... 83
Kevin C. Roach, Benjamin D. Ross, and Harmit S. Malik
9.1 Centromeres in'the fast lane' .......................... 83
9.2 Rapidly evolving centromeric histones .................. 83
9.3 Bewildering centromeric DNA complexity and evolution ... 85
9.4 The 'centromere paradox': conflict, not coevolution .... 87
9.5 Support for the centromere drive model ................. 89
9.6 Taxonomic differences in susceptibility to centromere
drive .................................................. 89
9.7 Rapid evolution of other centromeric proteins .......... 90
9.8 Centromere drive and postzygotic isolation between
species ................................................ 91
9.9 Future directions ...................................... 91
10 Rapid evolution via chimeric genes .......................... 94
Rebekah L. Rogers and Daniel L. Hartl
10.1 Introduction ........................................... 94
10.2 Mechanisms of formation ................................ 94
10.3 Selection .............................................. 96
10.4 Genomic stability ...................................... 96
10.5 Function ............................................... 97
10.6 Non-coding DNA ......................................... 98
10.7 Future directions ...................................... 99
11 Evolutionary interactions between sex chromosomes and
autosomes .................................................. 101
Manyuan Long, Maria D. Vibranovski, and Yong E. Zhang
11.1 Introduction .......................................... 101
11.2 Gene traffic between sex chromosome and autosomes ..... 102
11.2.1 Gene traffic in Drosophila ..................... 102
11.2.2 Gene traffic in mammals ........................ 103
11.2.3 The cause and consequence of gene traffic ...... 104
11.3 The generality of gene traffic out of the X in the
genus Drosophila ...................................... 105
11.3.1 Gene traffic in Drosophilidae and RNA-based
and DNA-based duplication ...................... 105
11.3.2 Independent tests of gene traffic .............. 105
11.4 Mechanisms underlying gene traffic out of the X: the
detection of meiotic sex chromosome inactivation ...... 107
11.4.1 Evolutionary genetic models .................... 107
11.4.2 Molecular mechanistic models ................... 107
11.5 The X-recruitment of young male-biased genes and
gene traffic out of the X chromosome .................. 108
11.5.1 Age-dependence in Drosophila ................... 109
11.5.2 Age-dependence in mammals ...................... 110
11.5.3 The slow enrichment of X-linked female genes ... 110
11.6 Concluding remarks .................................... 111
12 Evolutionary signatures in non-coding DNA .................. 115
Dara G. Torgerson and Ryan D. Hernandez
12.1 Introduction .......................................... 115
12.2 Challenges to studying the evolution of non-coding
DNA ................................................... 116
12.2.1 Identifying functional non-coding DNA .......... 116
12.2.2 Estimating the neutral evolutionary rate ....... 117
12.2.3 Limitations of identifying rapid evolution in
non-coding DNA ................................. 117
12.3 Patterns of evolution in non-coding DNA ............... 117
12.3.1 Selection in conserved non-coding sequences? ... 118
12.3.2 Detecting selection in promoters and TFBSs ..... 120
12.3.3 Emerging trends in microRNA binding sites ...... 121
12.3.4 Coding versus non-coding ....................... 121
12.4 Future prospects ...................................... 122
Part III Sex- and Reproduction-Related Genetic Systems
13 Evolution of sperm-egg interaction ......................... 127
Melody R. Palmer and Willie J. Swanson
13.1 Introduction .......................................... 127
13.2 Evolution at each step of sperm-egg interaction ....... 127
13.3 Causes of rapid evolution ............................. 130
13.4 Methods to identify interacting proteins .............. 132
13.5 Conclusions ........................................... 132
14 Rates of sea urchin bindin evolution ....................... 136
H.A. Lessios and Kirk S. Zigler
14.1 Introduction .......................................... 136
14.2 Function and structure of bindin ...................... 136
14.3 Rate of bindin evolution .............................. 137
14.4 Possible reasons for different evolutionary rates in
bindin ................................................ 139
14.5 Conclusions and future prospects ...................... 141
15 Evolution of Drosophila seminal proteins and their
networks ................................................... 144
Alex Wong and Mariana F. Wolfner
15.1 Introduction .......................................... 144
15.2 Drosophila seminal fluid as a model system for
rapidly evolving proteins ............................. 144
15.3 Extensive variation in rates of SFP evolution ......... 147
15.4 Selection on a network? ............................... 149
15.5 Conclusions ........................................... 150
16 Evolutionary genomics of the sperm proteome ................ 153
Timothy L. Karr and Steve Dorus
16.1 Introduction .......................................... 153
16.2 Characterization of the Drosophila sperm proteome ..... 154
16.3 Molecular evolution of the Drosophila sperm proteome .. 154
16.4 Evolution of novel Drosophila sperm components ........ 155
16.4.1 Novel genes in the sperm proteome .............. 156
16.4.2 Expansion and diversification of S-LAP gene
family ......................................... 157
16.5 The mouse sperm proteome: intensified selection on
sperm membrane and acrosome genes ..................... 157
16.6 Rapid evolution of immunity-related genes in
mammalian sperm ....................................... 160
16.7 Sexual selection and compartmentalized adaptation in
reproductive genetic systems .......................... 161
16.8 Future perspectives ................................... 162
17 Fast evolution of reproductive genes: when is selection
sexual? .................................................... 165
Alberto Civetta
17.1 Introduction .......................................... 165
17.2 What has been the role of selection during the
evolution of male reproductive genes? ................. 167
17.3 When is selection sexual? The phylogenetic approach ... 168
17.4 Testing sexual selection in the era of genomes ........ 168
17.5 The need for association studies and functional
assays ................................................ 171
17.6 Conclusions ........................................... 172
18 Rapid morphological, behavioral, and ecological evolution
in Drosophila: comparisons between the endemic Hawaiian
Drosophila and the cactophilic repleta species group ....... 176
Patrick M. O'Grady and Therese Ann Markow
18.1 Introduction .......................................... 176
18.1.1 Ecological adaptations ......................... 177
18.1.2 Morphological adaptations ...................... 177
18.1.3 Behavioral adaptations ......................... 178
18.2 Hawaiian Drosophila radiation ......................... 179
18.2.1 Phylogenetic relationships ..................... 179
18.2.2 Sexual adaptations to morphology and behavior .. 179
18.2.3 Ecological adaptations to morphology and
behavior ....................................... 179
18.3 Cactophilic Drosophila radiation in the New World ..... 180
18.3.1 Phylogenetic relationships ..................... 180
18.3.2 Rapid evolution of ecological adaptations ...... 180
18.3.3 Rapid evolution of behavioral traits ........... 182
18.4 Conclusions: adaptive radiation versus adaptive
infiltration .......................................... 183
19 Ancient yet fast: rapid evolution of mating genes and
mating systems in fungi .................................... 187
Timothy Y. James
19.1 Introduction .......................................... 187
19.2 Incompatibility systems in fungi ...................... 189
19.3 Fungal reproductive proteins show evidence for
positive and balancing selection ...................... 190
19.4 Evidence for rapid evolution of fungal
incompatibility genes and systems ..................... 193
19.4.1 Sequence evolution ............................. 194
19.4.2 Mating systems and loci ........................ 194
19.5 Evidence for ancient alleles and mating systems ....... 196
19.6 Conclusions ........................................... 198
Part IV Pathogens and their Hosts
20 Rapid evolution of innate immune response genes ............ 203
Brian P. Lazzaro and Andrew G. Clark
20.1 The evolution of immunity ............................. 203
20.2 Orthology and gene family evolution in antimicrobial
immunity .............................................. 204
20.3 Molecular evolution of the antimicrobial immune
system ................................................ 205
20.4 The evolution of defense against viruses and
transposable elements ................................. 206
20.5 Concluding remarks .................................... 208
21 Rapid evolution of the plague pathogen ..................... 211
Ruifu Yang, Yujun Qui, and Dongsheng Zhou
21.1 Introduction .......................................... 211
21.2 Plasmid acquisition in Y. pest is ..................... 212
21.3 The impact of phages on genome structure .............. 213
21.4 Prophages in the Y. pestis genome ..................... 213
21.5 CRISPRs diversity and the battle between phage and
Y. pestis ............................................. 214
21.6 Gene acquisition, loss, and inactivation .............. 216
21.7 Rearrangements and copy number variants ............... 217
21.8 Neutral versus adaptive evolution ..................... 219
21.9 Conclusions ........................................... 220
22 Evolution of human erythrocyte-specific genes involved in
malaria susceptibility ..................................... 223
Wen-Ya Ко, Felicia Gomez, and Sarah A. Tishkoff
22.1 Introduction .......................................... 223
22.2 Adaptive evolution in erythrocyte-specific genes ...... 224
22.2.1 Genetic variants causing erythrocytic
structural, regulatory, or enzymatic
deficiency: candidates for heterozygote
advantage ...................................... 224
22.2.2 Positive selection on erythrocyte-surface
receptors ...................................... 226
22.3 Evolutionary response of the human genome to malaria
infection ............................................. 227
22.3.1 Maintenance of deleterious mutations due to
selective pressure of malaria .................. 227
22.3.2 Effects of population substructure on genetic
variation in malaria-endemic human
populations .................................... 230
22.3.3 Effects of gene conversion between homologous
sequences on genetic variation at loci
associated with malarial susceptibility ........ 232
22.4 Future perspectives ................................... 232
Part V From Gene Expression to Development to Speciation
23 The rapid evolution of gene expression ..................... 237
Carlo G. Artieri
23.1 Introduction .......................................... 237
23.2 One genome harbors many transcriptomes ................ 238
23.3 Transcriptome divergence is complex ................... 239
23.4 Factors affecting the rate of evolution of gene
expression ............................................ 240
23.4.1 Spatial heterogeneity .......................... 240
23.4.2 Temporal heterogeneity ......................... 241
23.5 Beyond comparisons of expression levels ............... 242
23.6 Open questions and future directions .................. 243
24 Rate variation in the evolution of development:
a phylogenetic perspective ................................. 246
Artyom Kopp
24.1 Introduction .......................................... 246
24.2 Examples of rate variation in the evolution of
development ........................................... 247
24.2.1 Same clade, different pathways: evolution of
vulval development in rhabditid nematodes ...... 247
24.2.2 Same pathway, different clades: evolution of
sex combs and pigmentation in Drosophila ....... 248
24.2.3 Same clade, same pathway, different genes:
evolution of embryonic development and sex
determination in insects ....................... 251
24.3 Technical and conceptual challenges to quantifying
the evolution of development .......................... 252
24.4 Future directions: the promise of phylogenetic
approaches to the evolution of development ............ 253
25 Natural hybridization as a catalyst of rapid evolutionary
change ..................................................... 256
Michael L. Arnold, Jennafer A.P. Hamlin, Amanda N.
Brothers, and Evangeline S. Ballerini
25.1 Introduction .......................................... 256
25.2 Adaptive trait introgression: when strange is really
good .................................................. 256
25.2.1 Adaptive trait transfer in Canis: wolves in
dogs' clothing ................................. 257
25.2.2 Adaptive trait origin in Saccharomyces
cerevisiae: hybrids make the best wine ......... 258
25.3 Hybrid speciation: when opposites attract ............. 259
25.3.1 Homoploid hybrid speciation: hybrid
butterflies (quickly) change their spots ....... 259
25.3.2 Allopolyploid speciation: Tragopogon hybrid
polyploids form again, and again, and again
in less than 100 years ......................... 260
25.4 Natural hybridization and adaptive radiations:
hybrid speciation on steroids ......................... 261
25.4.1 Hybridization and adaptive radiations of Lake
Malawi cichlids: from hybrid swarm to 800
species, in one lake? .......................... 261
25.4.2 Hybridization and adaptive radiations in
Alpine lake whitefish: Swiss fish diversify
after the last big thaw ........................ 262
25.4.3 Hybridization and adaptive radiations in
Hawaiian silverswords: allopolyploids in an
island paradise ................................ 263
25.5 Conclusions and future prospects ...................... 264
26 Rapid evolution of pollinator-mediated plant reproductive
isolation .................................................. 266
Annika M. Мое, Wendy L. Clement, and George D. Weiblen
26.1 Plant-insect diversification .......................... 266
26.2 Pollination and reproductive isolation ................ 266
26.3 Ficus versus Castilleae ............................... 267
26.4 A pollinator-mediated model for fig speciation ........ 269
26.5 Future directions: plant-pollinator interactions and
rapid evolution ....................................... 271
27 Sexual system genomics and speciation ...................... 274
Rob J. Kulathinal and Rama S. Singh
27.1 In the beginning: Darwin and Wallace on sexual
selection and speciation .............................. 274
27.2 The Modern Synthesis and the development of
speciation theory ..................................... 275
27.3 A new paradigm: the genomics of sexual systems and
the origin of species ................................. 276
27.3.1 Functional genomics: organization into sexual
and non-sexual systems ......................... 277
27.3.2 Higher variation among reproductive systems .... 277
27.3.3 Strength of sexual selection ................... 278
27.3.4 Sexual systems interaction, coevolution, and
rapid change ................................... 279
27.3.5 Rapid breakdown of sexual systems in species
hybrids ........................................ 280
27.4 Towards a post-genomics synthesis of speciation ....... 280
27.5 Future prospects: sex as a major force in evolution ... 281
Index ......................................................... 285
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