Conservation and the Genetics of Populations

Fred W. Allendorf is a Regents Professor at the University of Montana and a Professorial Research Fellow at Victoria University of Wellington in New Zealand.  He has published over 200 articles on the population genetics and conservation of fish, amphibians, mammals, invertebrates, and plants.  He is a past President of the American Genetic Association, and has served as Director of the Population Biology Program of the National Science Foundation.  He has taught conservation genetics at the University of Montana, University of Oregon, University of Minnesota, University of Western Australia, Victoria University of Wellington, and the US National Conservation Training Center. Gordon Luikart is an Associate Professor at the Flathead Lake Biological Station of the University of Montana and a Visiting Scientist in the Center for Investigation of Biodiversity and Genetic Resources at the University of Porto, Portugal.  He is also an award winning (Bronze Medal) Research Scientist with the Centre National de la Recherche Scientifique at the University Joseph Fourier in Grenoble, France. His research focuses on the conservation and genetics of wild and domestic animals, and includes over 100 publications.  He was a Fulbright Scholar at La Trobe University, Melbourne, and he is a member of the IUCN Specialist Group for Caprinae (mountain ungulates) conservation. Sally N. Aitken is a Professor in the Department of Forest Sciences and Director of the Centre for Forest Conservation Genetics at the University of British Columbia. She studies the population, conservation, ecological genetics, and genomics of forest trees. She received her PhD from the University of California, Berkeley, and she was a faculty member at Oregon State University. She has received the Canadian Forestry Scientific Achievement Award, a Killam Faculty Research Fellowship, and a Killam Teaching Prize. She teaches forest biology, alpine ecology, and conservation genetics, and she is involved in forest genetic conservation initiatives in North America and Europe. 

Guest Box authors, ix

Preface to the second edition, xi

Preface to the first edition, xiii

List of symbols, xv

PART I: INTRODUCTION, 1

1 Introduction, 3

1.1 Genetics and civilization, 4

1.2 What should we conserve?, 5

1.3 How should we conserve biodiversity?, 9

1.4 Applications of genetics to conservation, 10

1.5 The future, 12

Guest Box 1: L. Scott Mills and Michael E. Soulé, The role of genetics in conservation, 13

2 Phenotypic variation in natural populations, 14

2.1 Color pattern, 17

2.2 Morphology, 20

2.3 Behavior, 23

2.4 Phenology, 25

2.5 Differences among populations, 27

2.6 Nongenetic inheritance, 31

Guest Box 2: Chris J. Foote, Looks can be deceiving: countergradient variation in secondary sexual color in sympatric morphs of sockeye salmon, 32

3 Genetic variation in natural populations: chromosomes and proteins, 34

3.1 Chromosomes, 35

3.2 Protein electrophoresis, 45

3.3 Genetic variation within natural populations, 48

3.4 Genetic divergence among populations, 50

Guest Box 3: E. M. Tuttle, Chromosomal polymorphism in the white-throated sparrow, 52

4 Genetic variation in natural populations: DNA, 54

4.1 Mitochondrial and chloroplast organelle DNA, 56

4.2 Single-copy nuclear loci, 60

4.3 Multiple locus techniques, 68

4.4 Genomic tools and markers, 69

4.5 Transcriptomics, 72

4.6 Other ‘omics’ and the future, 73

Guest Box 4: Louis Bernatchez, Rapid evolutionary changes of gene expression in domesticated Atlantic salmon and its consequences for the conservation of wild populations, 74

PART II: MECHANISMS OF EVOLUTIONARY CHANGE, 77

5 Random mating populations: Hardy- Weinberg principle, 79

5.1 Hardy-Weinberg principle, 80

5.2 Hardy-Weinberg proportions, 82

5.3 Testing for Hardy-Weinberg proportions, 83

5.4 Estimation of allele frequencies, 88

5.5 Sex-linked loci, 90

5.6 Estimation of genetic variation, 92

Guest Box 5: Paul Sunnucks and Birgita D. Hansen, Null alleles and Bonferroni ‘abuse’: treasure your exceptions (and so get it right for Leadbeater’s possum), 93

6 Small populations and genetic drift, 96

6.1 Genetic drift, 97

6.2 Changes in allele frequency, 100

6.3 Loss of genetic variation: the inbreeding effect of small populations, 101

6.4 Loss of allelic diversity, 102

6.5 Founder effect, 106

6.6 Genotypic proportions in small populations, 110

6.7 Fitness effects of genetic drift, 112

Guest Box 6: Menna E. Jones, Reduced genetic variation and the emergence of an extinction-threatening disease in the Tasmanian devil, 115

7 Effective population size, 117

7.1 Concept of effective population size, 118

7.2 Unequal sex ratio, 119

7.3 Nonrandom number of progeny, 121

7.4 Fluctuating population size, 125

7.5 Overlapping generations, 125

7.6 Variance effective population size, 126

7.7 Cytoplasmic genes, 126

7.8 Gene genealogies, the coalescent, and lineage sorting, 129

7.9 Limitations of effective population size, 130

7.10 Effective population size in natural populations, 132

Guest Box 7: Craig R. Miller and Lisette P. Waits, Estimation of effective population size in Yellowstone grizzly bears, 134

8 Natural selection, 136

8.1 Fitness, 138

8.2 Single locus with two alleles, 138

8.3 Multiple alleles, 144

8.4 Frequency-dependent selection, 147

8.5 Natural selection in small populations, 149

8.6 Natural selection and conservation, 151

Guest Box 8: Paul A. Hohenlohe and William A. Cresko, Natural selection across the genome of the threespine stickleback fish, 154

9 Population subdivision, 156

9.1 F-Statistics, 158

9.2 Spatial patterns of relatedness within local populations, 161

9.3 Genetic divergence among populations and gene flow, 163

9.4 Gene flow and genetic drift, 165

9.5 Continuously distributed populations, 168

9.6 Cytoplasmic genes and sex-linked markers, 169

9.7 Gene flow and natural selection, 172

9.8 Limitations of FST and other measures of subdivision, 174

9.9 Estimation of gene flow, 179

9.10 Population subdivision and conservation, 184

Guest Box 9: M.K. Schwartz and J.M. Tucker, Genetic population structure and conservation of fisher in western North America, 185

10 Multiple loci, 187

10.1 Gametic disequilibrium, 188

10.2 Small population size, 192

10.3 Natural selection, 192

10.4 Population subdivision, 196

10.5 Hybridization, 196

10.6 Estimation of gametic disequilibrium, 199

10.7 Multiple loci and conservation, 200

Guest Box 10: Robin S. Waples, Estimation of effective population size using gametic disequilibrium, 203

11 Quantitative genetics, 205

11.1 Heritability, 206

11.2 Selection on quantitative traits, 212

11.3 Finding genes underlying quantitative traits, 217

11.4 Loss of quantitative genetic variation, 220

11.5 Divergence among populations, 223

11.6 Quantitative genetics and conservation, 225

Guest Box 11: David W. Coltman, Response to trophy hunting in bighorn sheep, 229

12 Mutation, 230

12.1 Process of mutation, 231

12.2 Selectively neutral mutations, 235

12.3 Harmful mutations, 239

12.4 Advantageous mutations, 239

12.5 Recovery from a bottleneck, 241

Guest Box 12: Michael W. Nachman, Color evolution via different mutations in pocket mice, 242

PART III: GENETICS AND CONSERVATION, 245

13 Inbreeding depression, 247

13.1 Pedigree analysis, 248

13.2 Gene drop analysis, 252

13.3 Estimation of F with molecular markers, 253

13.4 Causes of inbreeding depression, 256

13.5 Measurement of inbreeding depression, 258

13.6 Genetic load and purging, 264

13.7 Inbreeding and conservation, 267

Guest Box 13: Lukas F. Keller, Inbreeding depression in song sparrows, 268

14 Demography and extinction, 270

14.1 Estimation of census population Size, 272

14.2 Inbreeding depression and extinction, 274

14.3 Population viability analysis, 277

14.4 Loss of phenotypic variation, 286

14.5 Loss of evolutionary potential, 288

14.6 Mitochondrial DNA, 289

14.7 Mutational meltdown, 289

14.8 Long-term persistence, 291

14.9 The 50/500 rule, 292

Guest Box 14: A. G. Young, M. Pickup, and B. G. Murray, Management implications of loss of genetic diversity at the selfincompatibility locus for the button wrinklewort, 293

15 Metapopulations and fragmentation, 296

15.1 The metapopulation concept, 297

15.2 Genetic variation in metapopulations, 298

15.3 Effective population size of metapopulations, 301

15.4 Population divergence and connectivity, 303

15.5 Genetic rescue, 304

15.6 Landscape genetics, 306

15.7 Long-term population viability, 311

Guest Box 15: Robert C. Vrijenhoek, Fitness loss and genetic rescue in stream-dwelling topminnows, 313

16 Units of conservation, 316

16.1 What should we protect?, 318

16.2 Systematics and taxonomy, 320

16.3 Phylogeny reconstruction, 322

16.4 Genetic relationships within species, 327

16.5 Units of conservation, 336

16.6 Integrating genetic, phenotypic, and environmental information, 346

16.7 Communities, 348

Guest Box 16: David J. Coates, Identifying units of conservation in a rich and fragmented flora, 350

17 Hybridization, 352

17.1 Natural hybridization, 353

17.2 Anthropogenic hybridization, 358

17.3 Fitness consequences of hybridization, 360

17.4 Detecting and describing hybridization, 364

17.5 Hybridization and conservation, 370

Guest Box 17: Loren H. Rieseberg, Hybridization and the conservation of plants, 375

18 Exploited populations, 377

18.1 Loss of genetic variation, 378

18.2 Unnatural selection, 381

18.3 Spatial structure, 385

18.4 Effects of releases, 388

18.5 Management and recovery of exploited populations, 391

Guest Box 18: Guðrún Marteinsdóttir, Long-term genetic changes in the Icelandic stock of Atlantic cod in response to harvesting, 393

19 Conservation breeding and restoration, 395

19.1 The role of conservation breeding, 398

19.2 Reproductive technologies and genome banking, 400

19.3 Founding populations for conservation breeding programs, 403

19.4 Genetic drift in captive populations, 405

19.5 Natural selection and adaptation to captivity, 407

19.6 Genetic management of conservation breeding programs, 410

19.7 Supportive breeding, 412

19.8 Reintroductions and translocations, 414

Guest Box 19: Robert C. Lacy, Understanding inbreeding depression: 25 years of experiments with Peromyscus mice, 419

20 Invasive species, 421

20.1 Why are invasive species so successful?, 422

20.2 Genetic analysis of introduced species, 425

20.3 Establishment and spread of invasive species, 429

20.4 Hybridization as a stimulus for invasiveness, 430

20.5 Eradication, management, and control, 431

20.6 Emerging diseases and parasites, 433

Guest Box 20: Richard Shine, Rapid evolution of introduced cane toads and native snakes, 438

21 Climate change, 440

21.1 Predictions and uncertainty about future climates, 441

21.2 Phenotypic plasticity, 442

21.3 Maternal effects and epigenetics, 445

21.4 Adaptation, 446

21.5 Species range shifts, 448

21.6 Extirpation and extinction, 449

21.7 Management in the face of climate change, 451

Guest Box 21: S. J. Franks, Rapid evolution of flowering time by an annual plant in response to climate fluctuation, 453

22 Genetic identification and monitoring, 455

22.1 Species identification, 457

22.2 Metagenomics and species composition, 464

22.3 Individual identification, 465

22.4 Parentage and relatedness, 469

22.5 Population assignment and composition analysis, 471

22.6 Genetic monitoring, 477

Guest Box 22: C. Scott Baker, Genetic detection of illegal trade of whale meat results in closure of restaurants, 481

Appendix: Probability and statistics, 484

A1 Paradigms, 485

A2 Probability, 487

A3 Statistical measures and distributions, 489

A4 Frequentist hypothesis testing, statistical errors, and power, 496

A5 Maximum likelihood, 499

A6 Bayesian approaches and MCMC (Markov Chain Monte Carlo), 500

A7 Approximate Bayesian Computation (ABC), 504

A8 Parameter estimation, accuracy, and precision, 504

A9 Performance testing, 506

A10 The coalescent and genealogical Information, 506

Guest Box A: James F. Crow, Is mathematics necessary?, 511

Glossary, 513

References, 531

Index, 587

Color plates section between page 302 and page 303