Lecture 14: Selection Experiments & Experimental Evolution

1. Lecture 14: • Selection Experiments & Experimental Evolution • Irschick, D. J., and D. Reznick. 2009. Field experiments, introductions, and experimental evolution: a review and practical guide. Pages 173-193 in Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments. T. Garland, Jr. and M. R. Rose, eds. University of California Press, Berkeley, California.

2. 4 Ways to Study Physiological Evolution • 1. Phylogenetic Comparisons of Species (or populations) • Shows what has happened in past evolution • 2. Biology of Natural Populations: • extent of individual variation (repeatability)heritability and genetic correlationsnatural and sexual selectionfield manipulations and introductions • Shows present evolution in action • 3. Selection Experiments • Shows, experimentally, what might happen during future evolution • 4. Compare Real Organisms with Theoretical Models • Shows how close selection can get to producing optimal solutions

3. Selection Experiments: • The earliest form of “genetic engineering” • An experimental way to study “evolution in action” • A way to produce “useful” organisms • The most direct and convincing test of whether a trait shows any additive genetic variance in the population (narrow-sense heritability) • 5. A modern corollary to the August Krogh Principle. If a suitable model does not exist, then create one!Bennett, A. F. 2003. Experimental evolution and the Krogh Principle: generating biological novelty for functional and genetic analyses. Physiological and Biochemical Zoology 76:1-11.

4. Selection Experiments: • A way to probe the interrelations among traits(correlated responses indicate genetic correlations) • A way to test hypotheses about trade-offs and constraints • A way to help find the genes that underlie phenotypic variation. Crossing a selected population with a non-selected or oppositely-selected population facilitates genetic mapping.

5. Selection Experiments: 9. A powerful way to demonstrate mechanism, i.e., how organisms work: a. Select on an organismal trait b. Observe correlated response in lower- level trait that you hypothesize causes the organismal difference c. Test that hypothesis by performing a second experiment, selecting on the lower-level trait d. Does the organismal trait change as predicted?

6. Hypothetical Example 1 a. Select for long life span in mice b. Observe correlated increase in anti-oxidant enzyme activities c. Select for high anti-oxidant enzyme activities (e.g., biopsy individuals to score their phenotype and then choose breeders) d. Does life span increase as predicted?

7. Hypothetical Example 2 a. Select for high maximal O2 consumption b. Observe increase in blood [hemoglobin] c. Select for high blood [hemoglobin] d. Does VO2max increase as predicted?

8. Recent Physiological Perspectives Gibbs, A. G. 1999. Laboratory selection for the comparative physiologist. Journal of Experimental Biology 202:2709-2718. Harshman, L. G. , and A. A. Hoffmann. 2000. Laboratory selection experiments using Drosophila: what do they really tell us? Trends in Ecology and Evolution 15:32-36. Bennett, A. F. 2003. Experimental evolution and the Krogh Principle: generating biological novelty for functional and genetic analyses. Physiological and Biochemical Zoology 76:1-11. Garland, T., Jr. 2003. Selection experiments: an under-utilized tool in biomechanics and organismal biology. Pages 23-56 in V. L. Bels, J.-P. Gasc, A. Casinos, eds. Vertebrate biomechanics and evolution. BIOS Scientific Publishers, Oxford, U.K. Bradley, T. J., and D. G. Folk. 2004. Analyses of physiological evolutionary response. Physiological and Biochemical Zoology 77:1-9. Swallow, J. G., and T. Garland, Jr. 2005. Selection experiments as a tool in evolutionary and comparative physiology: insights into complex traits - An introduction to the symposium. Integrative and Comparative Biology 45:387-390. Swallow, J. G., J. P. Hayes, P. Koteja, and T. Garland, Jr. 2009. Selection experiments and experimental evolution of performance and physiology. Pages 301-351 in Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments, T. Garland, Jr., and M. R. Rose, eds. Univ. of Calif. Press, Berkeley. Feder, M. E., T. Garland, Jr., J. H. Marden, and A. J. Zera. 2010. Locomotion in response to shifting climate zones: not so fast. Annu. Rev. Physiol. 72:167-190.

9. Types of "Selection Experiments" Domestication: The process may vary widely, e.g., dogs, cats, cattle, horses, corn. At some point, it involves some unintentional selection (e.g., ability of organisms to reproduce in altered conditions). Domestication often also involve some intentional selection for particular characteristics, such as tameness or coloration. Further selection may occur for particular traits (e.g., milk yield in cows) or to differentiate breeds based on various traits.

10. Domestication followed by Intentional Selection:

11. Modern European radiation Parker et al. 2004 Science304: 1160-4

12. Aggressive breeds have higher daily metabolizable energy intake (MEI) r = 0.83 N = 9 P = 0.02 2.90 2.85 No mention of selection on food consumption… Changed as a correlated response to selection on aggressiveness? What physiological or neurobiological mechanism might cause that? 2.80 Mass-adjusted Log(MEI) 2.75 2.70 2.65 2.60 70 80 90 100 110 120 130 Aggressiveness score Loadings: Aggression to dogs and territorial defence Careau et al. Am Nat 2010

13. Pasi, B. M., and D. R. Carrier. 2003. Functional trade-offs in the limb muscles of dogs selected for running vs. fighting. Journal of Evolutionary Biology 16:324-332. Kemp, T. J., K. N. Bachus, J. A. Nairn, and D. R. Carrier. 2005. Functional trade-offs in the limb bones of dogs selected for running versus fighting. J. Exp. Biol. 208:3475-3482.

14. Domestication: (http://ngm.nationalgeographic.com/2011/03/taming-wild-animals/ratliff-text/2) Siberia - Dmitri K. Belyaev developed colonies of silver foxes, river otters, minks, and rats, starting in 1959.

15. Domestication: Siberia - Dmitri K. Belyaev developed colonies of silver foxes, river otters, minks, and rats, starting in 1959. Frank Albert, a graduate student at the Max Planck Institute for Evolutionary Anthropology in Germany, is studying two colonies of tame and hyperaggressive Siberian rats to determine the genetics behind their differences. A handful of genes could be responsible. http://www.nytimes.com/imagepages/2006/07/25/science/25rats2_ready.html http://ngm.nationalgeographic.com/2011/03/taming-wild-animals/musi-photography

16. Artificial Selection: Captive populations in which individuals in each generation are measured for a phenotypic trait (or combination of traits). Some top or bottom fraction of individuals is then chosen as the breeders to produce the next generation. This is called "truncation selection" or "mass selection." One variation is taking the highest-scoring (or lowest-scoring) male and female from within each family. Within-family selection increases the effective population size (Ne), reduces rate of inbreeding, and helps to eliminate confounding influences of some maternal effects. But, it also reduces the possible intensity of selection as compared with "mass selection," which involves choosing breeders without regard to their family membership.

17. Male miceat 42 days of age 100gens. The longest- runningvertebrateartificial selection experiment: 67 grams Body Mass (g) 30 grams Generation Mice Bunger, L., A. Laidlaw, G. Bulfield, E. J. Eisen, J. F. Medrano, G. E. Bradford, F. Pirchner, U. Renne, W. Schlote, and W. G. Hill. 2001. Inbred lines of mice derived from long-term growth selected lines: unique resources for mapping growth genes. Mammalian Genome 12:678-686.

18. Laboratory Natural Selection: Individual phenotypes are not measured each generation, nor are breeders specifically chosen by the investigator. Rather, a freely breeding population is exposed to altered environmental conditions, such as different temperatures or salinities, or to altered husbandry conditions, which could favor changes in demographic schedules. Assuming that additive genetic variance exists for relevant traits, the population will adapt to the new conditions. Most common with non-vertebrates, including Drosophila, bacteria, and viruses, but have also been employed with vertebrates: Barnett and Dickson housed mouse colonies at room temperature or around 0o Celsius.

19. Barnett, S. A., and R. G. Dickson. 1984b. Milk production and consumption and growth of young of wild mice after ten generations in a cold environment. Journal of Physiology 346:409-417. In only 10 generations, "Eskimo mice" evolved to be larger and to have more body fat for their body size.

20. Intentional Field Introductions & Manipulations: David Reznick's guppies in Trinidad Reznick, D. N., F. H. Shaw, F. H. Rodd, and R. G. Shaw. 1997. Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275:1934-1937. Plus comment on page 1880. Anolis lizards introduced to Caribbean islands (Tom Schoener, Jonathan Losos) Losos, J. B., K. I. Warheit, and T. W. Schoener. 1997. Adaptive differentiation following experimental island colonization in Anolis lizards. Nature 387:70-73. Losos, J. B., D. A. Creer, D. Glossip, R. Goellner, A. Hampton, G. Roberts, N. Haskell, P. Taylor, and J. Ettling. 2000. Evolutionary implications of phenotypic plasticity in the hindlimb of the lizard Anolis sagrei. Evolution 54:301-305. Losos, J. B., T. W. Schoener, and D. A. Spiller. 2004. Predator-induced behaviour shifts and natural selection in field-experimental lizard populations. Nature 432:505-508.

21. "Accidental" Introductions & Manipulations: Drosophila introduced to North America Huey, R. B., G. W. Gilchrist, M. L. Carlson, D. Berrigan, and L. Serra. 2000. Rapid evolution of a geographic cline in size in an introduced fly. Science 287:308-309. Calboli, F. C. F., G. W. Gilchrist, and L. Partridge. 2003. Different cell size and cell number contribution in two newly established and one ancient body size cline of Drosophila subobscura. Evolution 57:566-573. House SparrowsParkin, D. T., and S. R. Cole. 1985. Genetic differentiation and rates of evolution in some introduced populations of the House Sparrow, Passer domesticus in Australia and New Zealand. Heredity 54:15-23. Adaptations of fishes to ponds heated by nuclear power plants Smith, M. H., M. W. Smith, S. L. Scott, E. H. Liu, and J. C. Jones. 1983. Rapid evolution in a post-thermal environment. Copeia 1983:193-197. Adaptations of plants to living on mine tailingsMacnair, M. R. 1987. Heavy metal tolerance in plants: A model evolutionary system. Trends in Ecology and Evolution 2:354-359. Adaptations of rodents to poisons Smith, P., M. G. Townsend, and R. H. Smith. 1991. A cost of resistance in the brown rat? Reduced growth rate in warfarin-resistant lines. Functional Ecology 5:441-447.

22. Examples of Selection Experiments

23. Falconer, D. S. 1992. Early selection experiments. Annu. Rev. Genet. 26:1-14. All the experiments described so far were done by geneticists. Tryon, in contrast, was a psychologist and he was not primarily concerned with the process of selection itself. ... The objectives of applying selection were to find out how the learning ability was inherited, to produce divergent strains, and to identify the behavioral and physiological traits associated with the maze learning. … The experiment was started in 1926 and the first publication was in 1929. Selection was made in both directions for the number of errors made in running the maze, and was carried on for 21 generations. Unfortunately inbreeding was practiced, as in most experiments at that time. ... The responses continued for about seven generations, after which there was hardly any overlap between the distributions of the two lines. … The experiment provided very convincing evidence that heredity was one of the factors contributing to the differences between individual rats in their ability to learn a maze. Crosses between the selected lines showed that the inheritance was polygenic. Subsequent … studies … showed that the differences were not in general learning ability, but were rather specific; for example, the maze-dull rats were more easily distracted by the noises made by the mechanical maze used for the selection (11).

24. Falconer, D. S. 1992. Early selection experiments. Annu. Rev. Genet. 26:1-14. All the experiments described so far were done by geneticists. Tryon, in contrast, was a psychologist and he was not primarily concerned with the process of selection itself. ... The objectives of applying selection were to find out how the learning ability was inherited, to produce divergent strains, and to identify the behavioral and physiological traits associated with the maze learning. … The experiment was started in 1926 and the first publication was in 1929. Selection was made in both directions for the number of errors made in running the maze, and was carried on for 21 generations. Unfortunately inbreeding was practiced, as in most experiments at that time. ... The responses continued for about seven generations, after which there was hardly any overlap between the distributions of the two lines. … The experiment provided very convincing evidence that heredity was one of the factors contributing to the differences between individual rats in their ability to learn a maze.Crosses between the selected lines showed that the inheritance was polygenic. Subsequent … studies … showed that the differences were not in general learning ability, but were rather specific; for example, the maze-dull rats were more easily distracted by the noises made by the mechanical maze used for the selection (11).

25. Falconer, D. S. 1992. Early selection experiments. Annu. Rev. Genet. 26:1-14. All the experiments described so far were done by geneticists. Tryon, in contrast, was a psychologist and he was not primarily concerned with the process of selection itself. ... The objectives of applying selection were to find out how the learning ability was inherited, to produce divergent strains, and to identify the behavioral and physiological traits associated with the maze learning. … The experiment was started in 1926 and the first publication was in 1929. Selection was made in both directions for the number of errors made in running the maze, and was carried on for 21 generations. Unfortunately inbreeding was practiced, as in most experiments at that time. ... The responses continued for about seven generations, after which there was hardly any overlap between the distributions of the two lines. … The experiment provided very convincing evidence that heredity was one of the factors contributing to the differences between individual rats in their ability to learn a maze. Crosses between the selected lines showed that the inheritance was polygenic. Subsequent … studies … showed that the differences were not in general learning ability, but were rather specific; for example, the maze-dull rats were more easily distracted by the noises made by the mechanical maze used for the selection (11).

26. Rats Tryon, R. C. 1929. The genetics of learning ability in rats. Univ. Calif. Publ. Psychol. 4:71-89.

27. Rats Ridley, 1996, p. 45 Hunt, H. R., C. A. Hoppert, and S. Rosen. 1955. Genetic factors in experimental rat caries. Pages 66-81 in R. F. Sognnaes, ed. Advances in experimental caries research. American Association for the Advancement of Science, Washington, D.C.

28. Selection for Ethanol Sleep Time in Laboratory MiceHuman alcoholism involves both liking of alcohol and physical effects of (e.g., tolerance to) alcohol. This experiment targeted the latter only. 167 min 41.7 min Plomin, R., J. C. DeFries, and G. E. McClearn. 1990. Behavioral genetics: A primer. 2nd ed. W. H. Freeman, New York. 455 pp.

29. Selection for Ethanol Sleep Time in Laboratory Mice Note complete separation of short- and long-selected lines 33.3 min 200 min Plomin, R., J. C. DeFries, and G. E. McClearn. 1990. Behavioral genetics: A primer. 2nd ed. W. H. Freeman, New York. 455 pp.

30. The Importance of Replication A study of genetic differences between any two lines will likely find many that have nothing to do with the phenotypic difference of interest.

31. The Importance of Replication Line differences in the trait under selection may be caused by: 1. the selective breeding 2. founder effects 3. subsequent genetic drift 4. unique mutations 5. different adaptive responses

32. The Importance of Replication Line differences in other traits(correlated responses) may be caused by: 1. the selective breeding pleiotropic genetic effects genetic linkage 2. founder effects 3. subsequent genetic drift 4. unique mutations 5. different adaptive responses

33. Selection on Open-field Activity in Mice Method developed by C. S. Hall in 1930s to measure levels of fear and “emotional reactivity” in rodents Video camera

34. DeFries, J. C., J. R. Wilson, and G. E. McClearn. 1970. Open-field behavior in mice: selection response and situational generality. Behavior Genetics 1:195-211.

35. "The foundation population for the selection experiment consisted of 40 F3 litters which were descendants from an original cross of two inbred strains of mice (BALB/cJ and C57BL/6J)." DeFries, J. C., J. R. Wilson, and G. E. McClearn. 1970. Open-field behavior in mice: selection response and situational generality. Behavior Genetics 1:195-211.

36. Mice Total movement is ~91 m, at an average (although movement is actually periodic) velocity of 0.51 m/s 91 cm square arena; # of photobeams crossed in 3 minutes, summed over 2 days 600 beam breaks is at most ~ 91 m Important features of experimental design: replication up, down, and control lines The direct response to selection. Note consistency of response between replicates.

37. A correlated response to selection. Note somewhat lower consistency of correlated response between replicates.

38. Coat color also changes! An example of pleiotropy, one of the main causes of genetic correlations. Again, note consistency of replicates.

39. "Two inbred strains of mice (BALB/cJ and C57BL/6J) which differ widely in open-field behavior were crossed …" Abstract. In segregating F2, F3, and F4 generations, albino mice had lower activity and higher defecation scores than pigmented animals when tested in a brightly lighted open field. These differences persisted when members of an F5 generation were tested under white light, but largely disappeared under red light. Thus it was concluded that there is a major gene effect on the quantitative traits of open-field activity and defecation which is mediated by the visual system and that albino mice are more photophobic than pigmented mice under conditions of bright illumination. DeFries, J. C., J. P. Hegmann, and M. W. Weir. 1966. Open-field behavior in mice: evidence for a major gene effect mediated by the visual system. Science 154:1577-1589.

40. Selection for Thermoregulatory Nesting Lynch, C. B. 1980. Response to divergent selection for nesting behavior in Mus musculus. Genetics 96:757-765. The base population was a genetically heterogeneous stock of lab mice (Mus musculus) originally derived from an 8-way cross among inbred strains. May be considered the first rodent selection experiment in "evolutionary physiology."

41. Selection for Thermoregulatory Nesting Lynch, C. B. 1994. Evolutionary inferences from genetic analyses of cold adaptation in laboratory and wild populations of the house mouse. Pages 278-301 in C. R. B. Boake, ed. Quantitative genetic studies of behavioral evolution. Univ. Chicago Press.

42. Selection for Thermoregulatory Nesting The overall realized heritability pooled across lines and replicates was 0.18 + 0.02 (0.15 + 0.03 for high nesting scores and 0.23 + 0.04 for low nesting scores), or 0.28+ 0.05 when adjusted for within-family selection. r = h2s h2 = r/s

43. Selection for Thermoregulatory Nesting Lynch, C. B. 1994. Evolutionary inferences from genetic analyses of cold adaptation in laboratory and wild populations of the house mouse. Pages 278-301 in C. R. B. Boake, ed. Quantitative genetic studies of behavioral evolution. Univ. Chicago Press. 60 50 40 30 20 10 0 High Cotton Used in 4 Days (g) Control Low 0 5 10 15 20 25 30 35 40 45 Generation Cause of limit in low lines is obvious: you cannot go below zero.

44. What Caused the Selection Limit in the High Lines?

45. Traditional, Interesting, Black Box Why a Selection Limit? Quantitative-Genetic Answers: Exhausted Additive Genetic Variance Genetic Correlations with Other Traits Counterposing Natural Selection

46. Why a Selection Limit? Abstract: To test the hypothesis that large, well-built, nests are an important component of fitness, we kept 12 mating pairs of two high-selected, two control, and two low-selected lines, selected for thermoregulatory nest-building behavior, at 22 and 4 degrees C with access to 10 g of cotton to build a nest, for a period of 180 days. Measurements included number of lifters born per family, number of young per litter born and surviving up to 40 days of age, nest type built by the parents, and weight gain of the young from weaning (20 days of age) to 40 days of age. In all lines the production and survival of offspring was substantially decreased at 4 degrees C compared to 22 degrees C, but the high-selected lines produced more and better-quality offspring, surviving up to 40 days of age at both temperatures compared to the control and low-selected lines. This indicates that thermoregulatory nest-building behavior and evolutionary fitness are closely associated. So, we do not seem to have Counterposing Natural Selection. Bult, A., and C. B. Lynch. 1997. Nesting and fitness: lifetime reproductive success in house mice bidirectionally selected for thermoregulatory nest-building behavior. Behavior Genetics 27:231-240.

47. Why a Selection Limit? Functional Answers: Motivation to build nest at a maximum Not enough time or space to build larger Not enough time or space to eat Energetic cost is too high Hyperthermia (literally overheating) or possibly negative feedback to the thermoregulatory behavior of nest-building Stopped here 19 Feb. 2015 Not mutually exclusive, May elucidate mechanisms of evolutionary “constraints”

48. Selection for Treadmill Endurance in Laboratory Rats "The starting population was 96 male and 96 female genetically heterogeneous rats (N:NIH stock) obtained from a colony maintained at the National Institutes of Health. Each rat in the founder population was of different parentage, so selection was not among brothers and sisters, which broadens the genetic variance." Koch, L. G., and S. L. Britton. 2001. Artificial selection for intrinsic aerobic endurance running capacity in rats. Physiological Genomics 5:45-52.

49. Selection for Treadmill Endurance in Laboratory Rats Koch, L. G., and S. L. Britton. 2001. Artificial selection for intrinsic aerobic endurance running capacity in rats. Physiological Genomics 5:45-52.

50. Selection for Treadmill Endurance in Laboratory Rats Males Females Distance Run (m)