Lecture 17: Measuring Selection in the Wild

1. Lecture 17: • Measuring Selectionin the Wild

2. Definitions (again): Natural Selection = individual variation in Darwinian fitness that is correlated with variation in one or more phenotypic traits. Darwinian Fitness (simply) = number of offspring left to the next generation by a given individual (measure at same stage, zygote-to-zygote best, difficult in practice) Components of Darwinian Fitness, e.g., survivorship, fecundity, # of mates These are often studied because it is too difficult to measure lifetime reproductive success.

3. We all know what (potential) selection looks like, but how do we measure it?

4. Remember: if all of that mortality depicted on the previous slide was random with respect to all phenotypes, then no natural selection is occurring. Mortality alone does not equal selection. Differential reproduction alone does not equal selection.These just give the potential for selection.

5. An influential paper: Lande, R., and S. J. Arnold. 1983. The measurement of selection on correlated characters. Evolution 37:1210-1226. "Natural selection acts on phenotypes, regardless of their genetic basis, and produces immediate phenotypic effects within a generation that can be measured without recourse to principles of heredity or evolution. In contrast, evolutionary response to selection, the genetic change that occurs from one generation to the next, does depend on genetic variation. ... Upon making this critical distinction ... precise methods can be formulated for the measurement of phenotypic natural selection." This verbal definition of selection, inheritance, and evolution is crucial, because it allows clear operational definitions of the three things consistent with r = h2s. Many discussions and definitions of natural selection confound phenotypic selection and inheritance, so be careful when you are reading!

6. "It cannot be too strongly argued that the problem of animal evolution is essentially a statistical problem ..." Weldon, W. F. R. 1893. On certain correlated variations inCarcinus moenas. Proc. Roy. Soc. London 54:318-329. Raphael Weldon was a pioneer in the application of statistics to biology and a founder of the journal Biometrika. Worked with Karl Pearson. http://www-groups.dcs.st-and.ac.uk/~history/Mathematicians/Weldon.html "He was by nature a poet, and these give the best to science, for they give ideas." (K. Pearson, 1906)

7. "... the questions raised by the Darwinian hypothesis are purely statistical, and the statistical method is the only one at present obvious by which that hypothesis can be experimentally checked." (Weldon, 1894) • Testing for a correlation between phenotype and lifetime fitness is best, but we can also get interesting information by correlating phenotype with some component of fitness, such as survival from year to year or during a particular episode. • The basic question: • Are survivors a random sample of the original population before selection?

8. Young, K. V., E. D. Brodie Jr., E. D. Brodie III. 2004. How the horned lizard got its horns. Science 304:65.

9. Bumpus, H. C. 1899. The elimination of the unfit as illustrated by the introduced sparrow, Passer domesticus. Biol. Lectures, Marine Biol. Lab., Woods Hole 6:209-226. In February, 1898, a severe winter storm with rain, sleet, and snow occurred near Providence, RI. 136 English sparrows were found freezing and brought to Dr. Bumpus’ laboratory at Brown University. 72 survived and 64 died. Bumpus took advantage of the opportunity to study an episode of natural selection. He weighed and made 8 linear measurements of the birds and compared survivors with non-survivors. However, he did not employ the standard statistical tests that we would apply today. But, he did publish all of his data! Thank God! (yes, I am being ironic)

10. “WE are so in the habit of referring carelessly to the process of natural selection, and of invoking its aid whenever some pet theory seems a little feeble, that we forget we are really using a hypothesis that still remains unproved, and that specific examples of the destruction of animals of known physical disability are very infrequent. Even if the theory of natural selection were as firmly established as Newton's theory of the attraction of gravity, scientific method would still require frequent examination of its claims, and scientific honesty should welcome such examination and insist on its thoroughness.” Bumpus, H. C. 1899. The elimination of the unfit as illustrated by the introduced sparrow, Passer domesticus. Biol. Lectures, Marine Biol. Lab., Woods Hole 6:209-226.

11. “… it is the purpose of this lecture to show that the birds which perished, perished not through accident, but because they were physically disqualified, and that the birds which survived, survived because they possessed certain physical characters. These characters enabled them to withstand the intensity of this particular phase of selective elimination, and distinguish them from their more unfortunate companions.” Bumpus, H. C. 1899. The elimination of the unfit as illustrated by the introduced sparrow, Passer domesticus. Biol. Lectures, Marine Biol. Lab., Woods Hole 6:209-226.

12. Directional Stabilizing "The birds which perished … are longer than those which endured, and we are justified in concluding that when nature selects, through the agency of winter storms of this particular kind of severity, those sparrows which are relatively short stand a better chance of surviving." "… the birds which survived invariably average less in weight than those which perished, and that among the males this difference amounts to more than a gram" "The process of selective elimination is most severe with extremely variable individuals, no matter in what direction the variations may occur. It is quite as dangerous to be conspicuously above a certain standard of organic excellence as it is to be conspicuously below the standard. It is the type that nature favors." Bumpus, H. C. 1899. The elimination of the unfit as illustrated by the introduced sparrow, Passer domesticus. Biol. Lectures, Marine Biol. Lab., Woods Hole 6:209-226.

13. All Traits log Transformed. P values from 2-tailed tests. = evidence for Directional Selection … but not for Stabilizing Selection These t-tests do not assume equal variances

14. The correlations among traits make it difficult to know what selection was really acting upon. Pairwise Pearson product-moment correlations. N = 49. All correlations are significant at P < 0.001 (2-tailed).

15. For example, if only those birds with humeri > -0.3 on the natural log scale survived, then the survivors would also have larger beaks & heads. t-test 2-tailed P < 0.001 Survivor Mean = 3.4656 ln Beak & Head Length (mm) Overall Mean = 3.4434 ln Humerus Length (inches)

16. Remember the breeder's equation: • r = h2s • r = response to selection • h2 = narrow-sense heritability • s = directional selection differential • = difference in mean phenotype between the original whole population before selection and the mean of the individuals who actually breed to produce the next generation

17. b directional selection gradient Multivariate Selection Theory DZ = G P-1 s additive genetic variance covariance matrix inverse of phenotypic variance covariance matrix multivariate response to selection a vector indicating the cross-generational change of character means or traits Z1, Z2, Z3, etc. vector of directional selection differentials Lande, R. 1979. Quantitative genetic analysis of multivariate evolution, applied to brain:body size allometry. Evolution 33:402-416. Lande, R., and S. J. Arnold. 1983. The measurement of selection on correlated characters. Evolution 37:1210-1226.

18. b can be calculated as the vector of partial regression coefficients in a multiple regression to predict fitness. Fitness = bo + b1Z1 + b2Z2 + b3Z3 + residuals If all relevant traits have been included in the analysis, then these describe selection that is acting directly on the individual traits.

19. Hypothetical Example: Imagine a population of birds in which we measure clutch size at fledging, which is a major component of Darwinian fitness, for 50 nests. In this species, males help to take care of the young, both feeding them and protecting the nest. So, for each nest, we also measure male body mass and take a blood sample to determine his circulating testosterone level. C:\174\PPT 2007 Win\Multiple Regression Example.SPS

20. Clutch Size Body Mass (grams) Clutch Size = 0.824 + 0.107 * Body Mass, r2 = 0.187 Standardized Regression Coefficient = 0.433

21. Clutch Size Testosterone (ng/ml) Clutch Size = 8.594 - 3.458 * Testosterone, r2 = 0.304 Standardized Regression Coefficient = -0.551

22. Testosterone (ng/ml) Body Mass (grams) r = 0.263, 2-tailed P = 0.065

23. Clutch Size = 0.824 + 0.107 * Body Mass, r2 = 0.187 Standardized Regression Coefficient = 0.433 Clutch Size = 8.594 - 3.458 * Testosterone, r2 = 0.304 Standardized Regression Coefficient = -0.551 Multiple Regression(a 3-dimensional plane): Clutch Size = 3.429 + 0.154 * Body Mass - 4.482 * Testosterone Multiple r2 = 0.662 Standardized Partial Regression Coefficients Body Mass = 0.621 Testosterone = -0.714

24. Clutch Size = 3.429 + 0.154 * Body Mass - 4.482 * Testosterone C:\174\PPT 2007 Win\Multiple Regression Example.SPS

25. In Bumpus' sparrow sample, selection favored shorter males. Selection also favored lighter males. The P values are lower than in the univariate t-tests. The significant negative selection on female weight was not detected by the t-tests (see next slide). Bumpus, H. C. 1899. The elimination of the unfit as illustrated by the introduced sparrow, Passer domesticus. Biol. Lectures, Marine Biol. Lab., Woods Hole 6:209-226.

26. All Traits log Transformed. 2-tailed tests. These t-tests do not assume equal variances

27. Stabilizing or disruptive selection can be detected by including the quadratic terms for traits in the multiple regression model: Trait A * Trait A Y = Fitness X = Trait A Significant downward curvature indicates stabilizing selection.

28. Stabilizing or disruptive selection can be detected by including the quadratic terms for traits in the multiple regression model:Trait A * Trait A Correlational selection can be detected by including cross-products terms: Trait A * Trait B Example: Brodie, E. D., III. 1992. Correlational selection for color pattern and antipredator behavior in the garter snake Thamnophis ordinoides. Evolution 46:1284-1298.

29. Explain garter snakes, measures of performance, reversals, etc. http://www.californiaherps.com/snakes/pages/t.ordinoides.html Active in the daytime. Mostly terrestrial, escaping into vegetation not water when threatened, but capable of swimming. When first handled, often releases cloacal contents and musk, but rarely bites. Escape behavior of this snake is related to pattern: striped snakes will escape by crawling away, since the stripes make it difficult to determine the snake's speed, while spotted or plain snakes will crawl, suddenly change direction, then hold still, as their pattern tends to blend in with the background. (E. D. Brodie III)

31. Correlational selection can be detected by including cross-products terms: Trait A * Trait B

33. Brodie, E. D., III. 1992. Correlational selection for color pattern and antipredator behavior in the garter snake Thamnophis ordinoides. Evolution 46:1284-1298. "This prediction precisely fits the pattern of correlational selection observed in the Tenmile population of T. ordinoides, where the snakes with the highest probability of survival perform uninterrupted flight if striped but flee evasively if spotted or unstriped."

34. This pattern of selection within a population is consistent with the pattern of differences seen among species of snakes. Jackson, J. F., W. Ingram, III, and H. W. Campbell. 1976. The dorsal pigmentation pattern of snakes as an antipredator strategy: a multivariate approach. American Naturalist 110:1020-1053. "Irregularly banded and blotched-spotted patterns are associated with an antipredator strategy of defense rather than flight, and these patterns likely function disruptively to minimize initial detection by predators. Striped and unicolored-speckled patterns are associated with antipredator strategies emphasizing flight more than defense."

35. Husak, J. F. 2006b. Does survival depend on how fast you can run or how fast you do run? Functional Ecology 20:1080-1086. "ecological performance" = % of maximal performance exhibited in nature The Collared Lizard, Crotaphytus collaris Studied yearling and adult lizards. Measured: 1. Maximum sprint speed in the laboratory 2. "Foraging" speed in field: attacking a fishing fly 3. "Escape" speed in field: approach of human "predator"

36. Husak, J. F. 2006b. Does survival depend on how fast you can run or how fast you do run? Functional Ecology 20:1080-1086. Before Selection After Selection (survived to following year)

37. McGlothlin, J. W., J. M. Jawor, and E. D. Ketterson. 2007. Natural variation in a testosterone-mediated trade-off between mating effort and parental effort. American Naturalist 170:864-875. Abstract: Male birds frequently face a trade-off between acquiring mates and caring for offspring. Hormone manipulation studies indicate that testosterone often mediates this trade-off, increasing mating effort while decreasing parental effort. … These relationships suggest that natural variation in testosterone, specifically the production of short-term increases, may underlie individual variation in the mating effort/parental effort trade-off. … Male dark-eyed junco (Junco hyemalis)

38. McGlothlin, J. W., J. M. Jawor, and E. D. Ketterson. 2007. Natural variation in a testosterone-mediated trade-off between mating effort and parental effort. American Naturalist 170:864-875. Because we were interested in generalized territorial aggression, and because territorial behaviors were intercorrelated, we extracted a single principal component to describe response to simulated territorial intrusions. The first principal component, which described 47% of variance, was loaded as in table 1 and was used as our measurement of aggression in the statistical analyses.

39. McGlothlin, J. W., J. M. Jawor, and E. D. Ketterson. 2007. Natural variation in a testosterone- mediated trade-off between mating effort and parental effort. American Naturalist 170:864-875.

40. Some General Reviews of Selection in the Wild

41. Endler, J. A. 1986. Natural selection in the wild. Princeton University Press, Princeton, New Jersey. 336 pp. • Conclusions of Endler's book: • Selection intensities in nature often are as strongas those implemented by animal breeders. • Differences in fitness of > 10% are not uncommonfor polymorphic traits. • Selection related to survival is generally less strong than selection related to mating ability, fertility or fecundity. • As of yet, few if any cases have quantified selection acting over the entire lifecycle of an organism (e.g., zygote to zygote). • If quantitative traits, such as size, shape or metabolic rate are affected by many genes, then even relatively strong selection on them may still allow genetic drift to determine the fate of most mutations at such loci.

42. Kingsolver, J. G., H. E. Hoekstra, J. M. Hoekstra, D. Berrigan, S. N. Vignieri, C. E. Hill, A. Hoang, P. Gibert, and P. Beerli. 2001. The strength of phenotypic selection in natural populations. American Naturalist 157:245-261. • Abstract: • We tabulated 63 published studies of 62 species that reported over 2,500 estimates of linear or quadratic selection. More than 80% of the estimates were for morphological traits; there is very little data for behavioral or physiological traits. • Most published selection studies were unreplicated and had sample sizes below 135 individuals, resulting in low statistical power to detect selection of the magnitude typically reported for natural populations. • The absolute values of linear selection gradients |b| were exponentially distributed with an overall median of 0.16, suggesting that strong directional selection was uncommon.

43. Kingsolver, J. G., H. E. Hoekstra, J. M. Hoekstra, D. Berrigan, S. N. Vignieri, C. E. Hill, A. Hoang, P. Gibert, and P. Beerli. 2001. The strength of phenotypic selection in natural populations. American Naturalist 157:245-261. • Abstract: • Comparisons of estimated linear selection gradients and differentials suggest that indirect components of phenotypic selection were usually modest relative to direct components. • The absolute values of quadratic selection gradients |g| were exponentially distributed with an overall median of only 0.10, suggesting that quadratic selection is typically quite weak. • The distribution of g values was symmetric about 0, providing no evidence that stabilizing selection is stronger or more common than disruptive selection in nature. "gradients" account for trait correlations

44. Kingsolver, J. G., and S. E. Diamond. 2011. Phenotypic selection in natural populations: what limits directional selection? American Naturalist 177:346-357. Abstract: Our analyses provide little evidence that fitness trade-offs, correlated selection, or stabilizing selection strongly constrains the directional selection reported for most quantitative traits.

45. Extra Slides Follow This was about 15 min short in 2011, but Gabe handed back the exams. For 2012, Ted added some Husak slides, and it was still about 10 minutes short. Husak, J. F. 2006b. Does survival depend on how fast you can run or how fast you do run? Functional Ecology 20:1080-1086. For 2013, I added three slides from: McGlothlin, J. W., J. M. Jawor, and E. D. Ketterson. 2007. Natural variation in a testosterone-mediated trade-off between mating effort and parental effort. American Naturalist 170:864-875. This was about 10 min short in 2013 This was a couple minutes too long in 2014 This was ~8 minutes SHORT in 2014 Need to add graphs explaining PCA Could still add some from this, but is complicated story: Koteja_Natural_Sel_Voles_UCR_27_April_2012_v1.pptx Calsbeek, R. 2008. An ecological twist on the morphology–performance–fitness axis. Evolutionary Ecology Research 10:197-212. [path analysis via CALIS procedure in SAS v8] Calsbeek, R., and D. J. Irschick. 2007. The quick and the dead: Locomotor performance and natural selection in island lizards. Evolution 61:2493-2503. [Correlational selection on limb length, speed, and habitat preference -- check. Endurance is on circular track, and sort of miscites Garland 1999.] Hereford, J., Hansen, T. F. & Houle, D. 2004. Comparing strengths of directional selection: How strong is strong? Evolution: 58: 2133-2143. Irschick, D. J., J. J. Meyers, J. F. Husak, and J.-F. Le Galliard. 2008. How does selection operate on whole-organism functional performance capacities? A review and synthesis. Evolutionary Ecology Research 10:177-196. Kingsolver, J. G., and S. E. Diamond. 2011. Phenotypic selection in natural populations: what limits directional selection? American Naturalist 177:346-357. Abstract: Studies of phenotypic selection document directional selection in many natural populations. What factors reduce total directional selection and the cumulative evolutionary responses to selection? We combine two data sets for phenotypic selection, representing more than 4,600 distinct estimates of selection from 143 studies, to evaluate the potential roles of fitness trade-offs, indirect (correlated) selection, temporally varying selection, and stabilizing selection for reducing net directional selection and cumulative responses to selection.We detected little evidence that trade-offs among different fitness components reduced total directional selection in most study systems. Comparisons of selection gradients and selection differentials suggest that correlated selection frequently reduced total selection on size but not on other types of traits. The direction of selection on a trait often changes over time in many temporally replicated studies, but these fluctuations have limited impact in reducing cumulative directional selection in most study systems. Analyses of quadratic selection gradients indicated stabilizing selection on body size in at least some studies but provided little evidence that stabilizing selection is more common than disruptive selection for most traits or study systems. Our analyses provide little evidence that fitness trade-offs, correlated selection, or stabilizing selection strongly constrains the directional selection reported for most quantitative traits.

46. http://en.wikipedia.org/wiki/Natural_selection#mediaviewer/File:Life_cycle_of_a_sexually_reproducing_organism.svghttp://en.wikipedia.org/wiki/Natural_selection#mediaviewer/File:Life_cycle_of_a_sexually_reproducing_organism.svg

47. Miles, D. B. 2004. The race goes to the swift: fitness consequences of variation in sprint performance in juvenile lizards. Evolutionary Ecology Research 6:63-75. From November to June P < 0.03 = 0.14

48. Miles, D. B. 2004. The race goes to the swift: fitness consequences of variation in sprint performance in juvenile lizards. Evolutionary Ecology Research 6:63-75. r = 0.56, P < 0.0001 ● Survivors o Non-survivors Multiple logistic regression indicates speed, not size, predicts survivorship

49. Miles, D. B. 2004. The race goes to the swift: fitness consequences of variation in sprint performance in juvenile lizards. Evolutionary Ecology Research 6:63-75. However, multiple logistic regression with all traits indicated that stride length was the best predictor of survivorship.

50. Miles, D. B. 2004. The race goes to the swift: fitness consequences of variation in sprint performance in juvenile lizards. Evolutionary Ecology Research 6:63-75. "Two key patterns emerged from the analysis of differential survivorship in juvenile U. ornatus. First, larger individuals were more likely to survive than smaller individuals. However, inclusion of the performance data also indicated that size alone did not completely explain the patterns of survival. Including body size and burst velocity simultaneously in a regression analysis resulted in only burst velocity significantly predicting survivorship. This result indicates that performance is a better predictor of survivorship in juvenile lizards than body size. Second, the selection analyses revealed a complex pattern of linear, quadratic and correlational selection on locomotor performance. There was evidence for strong directional selection on stride length. However, the quadratic selection analyses revealed a disparate pattern of selection acting on locomotor performance."