1. 1 Lecture 11: Individual Variation

2. 2 The biological importance of individual variation has recently been reemphasized in the fields of comparative physiology, functional morphology, animal behavior, behavioral ecology, as well as eco/evo physiology. It is also coming into medicine, spurred by the availability of genetic data (e.g., SNPs) that clearly demonstrate differences among individuals (and among "racial" groups, although that is a political hot potato!): Childs, B., C. Wiener, and D. Valle. 2005. A science of the individual: Implications for a medical school curriculum. Annual Review of Genomics and Human Genetics 6:313-330. Sometimes these genetic variants correlate with disease susceptibility, psychiatric conditions, etc.

3. 3 However, an appreciation of the fundamental importance of individual variation is not new to these and related fields. For example, Tryon, R. C. 1942. Individual differences. Pages 330-365 in F. A. Moss, ed. Comparative psychology. Prentice-Hall, New York. outlined four main problems that should be addressed when studying individual variation. He was talking about psychology, but his points also apply to physiology, morphology, etc. https://mikemcclaughry.files.wordpress.com/2013/02/robert_choate_tryon_-_oss_r__a_division.png

4. 4 Four main problems that should be addressed when studying individual variation (Tryon 1942): 1. How consistently do individuals differ and how large are those differences? 2. Does individual variation in one (behavioral) domain correlate with variation in other types of (behavior)?

5. 5 Four main problems that should be addressed when studying individual variation (Tryon 1942): 1. How consistently do individuals differ and how large are those differences? 2. Does individual variation in one (behavioral) domain correlate with variation in other types of (behavior)? This leads to the question of whether non- human animals have personalities? This is a controversial topic …

6. 6 It is now generally accepted that human personality includes five primary factors: extraversion openness conscientiousness neuroticism agreeableness each of which includes a number of subordinate facets. Human personality is typically measured via questionnaires, not specific tests of people in various settings.

7. 7 "In the introduction of his presidential address to the American Society of Naturalists in 1938, the eminent primatologist, Robert Yerkes underscored the idea that personality could be found in animals: "I am assuming that personality is the correct and adequate term for what is now known concerning the integrated behavior of the chimpanzee. Indeed, in my present thinking there is no question about the reality of chimpanzee mind, individuality, and personality" (Yerkes, 1939, p. 97). Yet in 1954, Hebb and Thompson described receiving looks of "open astonishment" (p. 532) when they presented the idea that animals should be of interest to psychologists interested in social behavior. Even today, the idea of "animal personality" is often treated with skepticism or even ridicule. However, as this article documents, the body of research on animal personality is growing. If properly implemented and interpreted, this research may be able to provide important insights into the genetic, biological, and environmental determinants of personality that could not be achieved by relying on human research alone." Gosling, S.D., 2001. From mice to men: What can we learn about personality from animal research? Psychological Bulletin 127:45-86.

8. 8 Behavioral ecologists also recently became interested in animal personality. Different definitions of animal personality have emerged in this field. Under the broad definition of personality, any repeatable behavior can technically be termed a personality trait, as repeatability implies that differences among individuals show at least some statistical consistency.

9. 9 More useful is a narrow-sense definition of personality (Reale et al. 2007) which, as presently construed, emphasizes: general activity exploration boldness aggressiveness sociability because these traits potentially underlie an individual’s behavior in many different contexts (e.g., mating, parental care, agonistic interactions, foraging, dispersal).

10. 10 Personality Factors HumanNon-Human extraversiongeneral activity opennessexploration conscientiousnessboldness neuroticismaggressiveness agreeablenesssociability The five commonly recognized personality factors are not the same in humans and other animals.

11. 11 Personality Factors HumanNon-HumanNon-Human Measure extraversiongeneral activityhome-cage activity opennessexplorationnovel open-field test conscientiousnessboldnessreaction to a predator neuroticismaggressivenessmirror test agreeablenesssociabilityreaction to conspecific

12. 12 Four main problems that should be addressed when studying individual variation (Tryon 1942): 1. How consistently do individuals differ and how large are those differences? 2. Does individual variation in one (behavioral) domain correlate with variation in other types of (behavior)? 3. Does individual variation in behavior relate to underlying differences in physiology and morphology? 4. Are individual differences caused by genetic differences among individuals?

13. 13 Remember that individual variation is the raw material on which selection acts, so to those four we can add the more field-oriented question not mentioned by Tryon (1942): 5. Does individual variation in morphology, physiology or behavior correlate with Darwinian fitness in nature. In other words, is selection acting on the individual variation that presently exists for a trait? This is one direct way to study "adaptation" in the genetic, evolutionary sense.

14. 14 We will discuss all of these components in more detail, and how they can actually be measured. For now, we need to know how to quantify and study individual variation. Individual differences can be documented by measuring each of a series of individuals multiple times and testing for significant "repeatability" of the differences among individuals.

15. 15 "Repeatability" has a specific definition in quantitative genetics, but for now just think of it as any statistic that takes on a high value when individuals are consistently different and a low value when they are not. For example, is the rank order of individual values consistent across trial days?

16. 16 The Western Fence Lizard, Sceloporus occidentalis

17. 17 The rank order of sprint speed, measured on a photocell-timed racetrack, is rather consistent (and statistically significant) across 5 successive trial days. Bennett, A. F. 1987. Inter-individual variability: an underutilized resource. Pages 147-169 in M. E. Feder, A. F. Bennett, W. W. Burggren, and R. B. Huey, eds. New directions in ecological physiology. Cambridge Univ. Press, Cambridge, U.K.

18. 18 How do we treat "outliers" (unusual observa- tions)?

19. 19 Was this a measurement error? Having a bad day? How do we treat "outliers" (unusual observa- tions)?

20. 20 10 Individual Frogs, each measured 3 times: both resting and active metabolic rate show reproducible differences among individuals, but resting and active values do not appear to be correlated. Figure 1. Mass-adjusted values of VO 2 rest and VO 2 act in 10 males of Scinax sp. 1. Bars are standard errors of three measurements. To facilitate visual comparisons, we present graphs of residuals of a regression analysis of the logarithm of body mass that have been adjusted to the overall mean body mass (3.20 g) and then reconverted to the original arithmetic scale. Gomes, F. R., J. G. Chauí-Berlinck, J. E. P. W. Bicudo, C. A. Navas. 2004. Intraspecific relationships between resting and activity metabolism in anuran amphibians: influence of ecology and behavior. Physiological and Biochemical Zoology 77:197-208. Resting Active

21. 21 Daily blood pressure measurements taken on one human subject at random times over 4 months (11/79-2/80). Iberall, A. S. 1984. An illustration of the experimental range of variation of blood pressure. Am. J. Physiol. 246 (Regulatory Integrative Comp. Physiol. 15):R516-R532. Fig. 1.

22. 22 Problems with and/or Objections to Studies of Individual Variation 1. Extreme values are atypical or abnormal and do not reflect the true response of most individuals. Essentially a restatement of the typological species concept. Real populations do have highly unusual individuals! These "abnormal" individuals do exist and hence must be considered. Selection and inheritance in the real world applies to them.

23. 23 Example: Garland, T., Jr. 1988. Genetic basis of activity metabolism. I. Inheritance of speed, stamina, and antipredator displays in the garter snake Thamnophis sirtalis. Evolution 42:335-350. The 46 dams gave birth between 2 August and 6 September 1984. Litter size ranged from one to 26 (mean = 12.2, SD = 5.15). Of the 562 offspring produced, 23 were born dead (frequencies were 10, 5, 2, 2, 1, 1, 1, and 1 individuals born dead in each of eight different families); another 13 were born with obvious deformities (eight with kinked tails, bodies, or necks; one with deformed ventral scales; four with one or both eyes small or absent); there were no more than two deformed individuals in any one family.

24. 24 Example: 249 of the offspring were tested for maximal sprint speed on a photocell-lined racetrack and for endurance on a motorized treadmill moving at 0.4 km/h. Both tests were done twice, on consecutive days. This is a histogram for the higher endurance: Endurance (min) log 10 Endurance (min) Range = 1-23 min But this does not account for the individuals born dead or severely deformed!

25. 25 2. Extreme points are attributable to instrumentation or procedural error; do not result from real biological differences. Typical physiological procedure might be to do 5-10 preparations (e.g., isolated muscles in ergometer), then throw out the 1 or 2 that were fairly different from the rest. Unusual points assumed to represent preparation errors, e.g., a damaged muscle. Difficult to know if the measure cannot be repeated on a single individual. If the "preparation" can be repeated, e.g., most measures of whole-animal physiological traits, then we can rule out this possibility.

26. 26 3. The variation is real (errors of measurement apparatus are not very large) but reflects random and unrepeatable responses of individuals; intra-individual variability is so high that there is no significant inter-individual component to total variance. Significant repeatability across trials answers this.

27. 27 Most typically, repeatability is quantified by measuring individuals on each of two days. A scatterplot is made. The Pearson product-moment correlation coefficient, r, indicates repeatability.

28. 28 R = 0.066 N = 50 No Repeatability 1:1 line looks like a shotgun blast, random scatter

29. 29 R = 0.894 N = 50 High Repeatability often found for morphometric traits, e.g., relative leg length 1:1 line

30. 30 R = 0.517 N = 50 Typical Repeatability fairly typical for behavioral and physiological traits 1:1 line

31. 31 Example: Harris, M. A., and K. Steudel. 2002. The relationship between maximum jumping performance and hind limb morphology/physiology in domestic cats (Felis silvestris catus). J. Exp. Biol. 205:3877-3889. 1:1

32. 32 Example: Garland, T., Jr. 1988. Genetic basis of activity metabolism. I. Inheritance of speed, stamina, and antipredator displays in the garter snake Thamnophis sirtalis. Evolution 42:335-350. log 10 Endurance (min) Day 1 log 10 Endurance (min) Day 2 N = 231, r = 0.696 1:1

33. 33 Lacerta vivipara from southern France Sorci et al. 1995. Physiological Zoology 68:698-720. This species gives birth, rather than laying eggs, and the newborns are ready to run!

34. 34 Newborn Lacerta vivipara Treadmill endurance is more repeatable than sprint speed, possibly because the latter is determined more by inherent physiological capacities for exercise, whereas the former is more determined by motivation? Note double log transform! Sorci et al. 1995. Physiological Zoology 68:698-720. Raw data are highly right- skewed. A few individuals are exceptional.

35. 35 Long-term Field Repeatability * * * * * indicates P < 0.05 van Berkum et al. 1989. Functional Ecology 3:97-105. not measured Hatchling body size does not predict yearling body size.

36. 36 Long-term Field Repeatability * indicates P < 0.05 * * * * van Berkum et al. 1989. Functional Ecology 3:97-105. Hatchling sprint speed does not significantly predict yearling sprint speed.

37. 37 Long-term Field Repeatability * * * * * van Berkum et al. 1989. Functional Ecology 3:97-105. Hatchling endurance does predict yearling endurance.

38. 38 Angilletta, M. J., Jr., P. H. Niewiarowski, and C. A. Navas. 2002. The evolution of thermal physiology in ectotherms. Journal of Thermal Biology 27:249-268.

39. 39 Why is repeatability important? If a trait is not consistent, but varies wildly from day-to-day, then selection has no clear "target." Teleologically and anthropomorphically, selection cannot penalize the bad individuals and reward the good ones, because these get mixed up every time selection "looks." Similarly, if the "quality" of parents varies wildly from day-to-day, then they cannot pass it on to their offspring. In general, repeatability sets an upper limit to heritability.

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41. 41 Natural & Sexual Selection Behavior Act On Organismal Performance Abilities Constrain Morphology, Physiology, Biochemistry Deter- mine This is the general model we usually have in mind in ecological/evolutionary physiology. Garland, Jr., T., and P. A. Carter. 1994. Evolutionary physiology. Annual Review of Physiology 56:579-621. http://en.wikipedia.org/wiki/Evolutionary_physiology

42. 42 Natural & Sexual Selection Behavior Act On Organismal Performance Abilities Constrain Morphology, Physiology, Biochemistry Deter- mine After some background, let's look at some examples in which individual variation was used to address this part of the overall model.

43. 43 Comparative physiologists have routinely looked at differences among species. Example: urine concentrating ability and length of loops of Henle in kidneys: a significant correlation among species (or among populations) suggests that the latter causes the former. But interspecific comparisons are fraught with difficulties: Garland, Jr., T., and S. C. Adolph. 1994. Why not to do two-species comparative studies: limitations on inferring adaptation. Physiological Zoology 67:797-828. Garland, Jr., T., A. F. Bennett, and E. L. Rezende. 2005. Phylogenetic approaches in comparative physiology. Journal of Experimental Biology 208:3015-3035. Rezende, E. L., and J. A. F. Diniz-Filho. 2012. Phylogenetic analyses: comparing species to infer adaptations and physiological mechanisms. Comprehensive Physiology 2:639-674. http://en.wikipedia.org/wiki/Phylogenetic_comparative_methods

44. 44 For example, we may be comparing apples and oranges (e.g., burrowing owl vs. bobwhite quail have been compared physiologically because both are birds of about the same body size). Also, species do not represent independent data points, and so we need independent phylogenetic information to perform proper statistical analyses: this may not be available for the organisms that we study. One way to avoid such problems is to stick within a single species. If relationships really do exist, then we should be able to demonstrate them.

45. 45... assuming that the "signal" is large enough to be detected over the "noise" of short-term variability within individuals! Hence the importance of first demonstrating that a physiological or behavioral measurement is repeatable.

46. 46 Example: Harris, M. A., and K. Steudel. 2002. The relationship between maximum jumping performance and hind limb morphology/physiology in domestic cats (Felis silvestris catus). J. Exp. Biol. 205:3877-3889. Fig. 8. (B) Significant positive relationship between maximum takeoff velocity (TOV) and the ratio of extensor muscle mass/body mass (r=0.647, P=0.004, y=7571x+220.9). Conclusions We found that cats with longer hind limbs and lower fat mass relative to their lean body mass achieved higher TOVs. These two variables explained significant variation in maximum TOV in a manner consistent with predictions based on the work done by extensor muscles to increase both kinetic and potential energy during takeoff. This study is the first to confirm the limb length–jump performance relationship in an endothermic vertebrate. Contrary to predictions, however, extensor muscle mass relative to lean body mass and percentage composition of MHC IIx were not found to significantly predict TOV. This is an ordinary least-squares linear regression predicting organismal performance from the lower-level (subordinate) trait of relative muscle mass. It would be more appropriate to report r 2 rather than r.

47. 47 Example: Hammond, K. A., M. A. Chappell, R. A. Cardullo, R.-S. Lin, T. S. Johnsen. 2000. The mechanistic basis of aerobic performance variation in red jungle fowl. Journal of Experimental Biology 203:2053-2064. Used residuals from regressions on body mass. Both maximal and basal metabolic rate are related to some lower-level traits in both sexes, but the predictors are not very consistent. Hct is a positive predictor of VO 2 max in both sexes, as might be expected.

48. 48 Example: What predicts locomotor performance in the Spiny-tailed Iguana (Ctenosaura similis) from Costa Rica? Garland, T., Jr. 1984. Physiological correlates of locomotory performance in a lizard: an allometric approach. Am. J. Physiol. 247 (Regulatory Integrative Comp. Physiol. 16):R806-R815.

49. 49 Ctenosaura similis Calculate residuals (vertical deviations from least-squares linear regressions) to remove effects of body size. Garland, T., Jr. 1984. Physiological correlates of locomotory performance in a lizard: an allometric approach. Am. J. Physiol. 247 (Regul. Integr. Comp. Physiol. 16):R806-R815.

50. 50 Then see if the residual subordinate traits can predict individual variation in the organismal performance trait with an OLS regression. This is a highly statistically significant positive relationship, and it makes biological sense.

51. 51 Combinations of the residual subordinate traits can predict more of the individual variation in the organismal performance traits than can a single lower-level trait. Garland, T., Jr. 1984. Physiological correlates of locomotory performance in a lizard: an allometric approach. Am. J. Physiol. 247 (Regul. Integr. Comp. Physiol. 16):R806-R815.

52. 52 Path Analysis: … allows multiple dependent variables and even multiple levels of dependent variables. Garland, T., Jr., and J. B. Losos. 1994. Ecological morphology of locomotor performance in squamate reptiles. Pages 240-302 in P. C. Wainwright and S. M. Reilly, eds. Ecological morphology: integrative organismal biology. Univ. Chicago Press, Chicago.

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54. 54 This can be very difficult to study in the wild Natural & Sexual Selection Behavior Act On Organismal Performance Abilities Constrain Morphology, Physiology, Biochemistry Deter- mine

55. 55 This, too, can be difficult to study in the wild Natural & Sexual Selection Behavior Act On Organismal Performance Abilities Constrain Morphology, Physiology, Biochemistry Deter- mine

56. 56 Laboratory Studies to get at Relations of Performance, Behavior, and Selection: A correlational study: Do locomotor abilities correlate with social dominance? Male Sceloporus occidentalis Size matched because size differences are known to have major effect on dominance interactions Measured social dominance in the lab by letting pairs compete for access to basking site Measured locomotor performance in the lab Compared winners-losers by paired t-test

57. 57 The Western Fence Lizard, Sceloporus occidentalis No difference in treadmill endurance

58. 58 The Western Fence Lizard, Sceloporus occidentalis Significant difference in sprint speed on photocell- timed racetrack

59. 59 But the lizards did not sprint at high speeds during behavioral interactions, so why would speed predict social dominance? Perhaps both traits are correlated with a third variable … One candidate would be testosterone levels

60. 60 A possible experimental study: Does testosterone (T) manipulation affect locomotor abilities and/or social dominance? Use silastic implants of T to increase circulating hormone levels. Compare performance and behavior with animals that received control implant (no T). Mills, S. C., L. Hazard, L. Lancaster, T. Mappes, D. Miles, T. A. Oksanen, and B. Sinervo. 2008. Gonadotropin hormone modulation of testosterone, immune function, performance, and behavioral trade-offs among male morphs of the lizard Uta stansburiana. American Naturalist 171:339-357. Figure 7: Regression of sprint speed on plasma testosterone for all experimental males (y = 0.6370 +.008x; R 2 p 0.19, P <.001, N = 73). Symbols indicate male morphotype: circles = by, asterisks = yy, dashes = bb, and triangles = oo.

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62. 62 Extra Slides Follow This was about 10 minutes short in 2011, but then I added slides # 46 and 47 on Hammond et al. (2000), and expanded slide 60 with figure from Mills et al. (2008). In 2012, it was about 5 minutes short, in 2013 about 11 minutes short, in 2014 after adding "personality" it was right on. But, then I moved the Definitions --> r=h2s and bell-shaped curves over to the QG lecture and made 174-15- Winter_11_xx-Feb_Individual_Variation.ppt renamed to 11 Nov. in Dec. 2014 174-15-Winter_11_10-Feb_Individual_Variation_for_IDEA.ppt was made 29 Jan. 2015 In 2015, this was about 5-10 min short. I did not like it. Need to cut some of the Bennett verbiage and redundancy, add in Tony at Simon Fraser, draw bread loaf from Feder 1987 chapter, improved the organization. Add Figure 3.4 from: Feder, M. E. 1987. The analysis of physiological diversity: the prospects for pattern documentation and general questions in ecological physiology. Pp. 38–75 in M. E. Feder, A. F. Bennett, W. W. Burggren, and R. B. Huey, eds. New directions in ecological physiology. Cambridge University Press, Cambridge, U.K. Zotero Selection Surface Bread Loaf Need to add Huey sample sizes, P values. Maybe replace van Berkum et al. (1989) with Huey/Dunham stuff. Shrink "objections" section??? Add more Careau and Garland (2012) stuff …

63. 63 Updates to be Done for 2012 Spring for IV: Ball, G. F., and J. Balthazart. 2007. Individual variation and the endocrine regulation of behaviour and physiology in birds: a cellular/molecular perspective. Phil. Trans. R. Soc. B doi:10.1098/rstb.2007.0010 No good graphs. Brandt, Y. 2003. Lizard threat display handicaps endurance. Proc. R. Soc. Lond. B 270:1061-1068. Guderley, H., and P. Couture. 2005. Stickleback fights: Why do winners win? Influence of metabolic and morphometric parameters. Physiological and Biochemical Zoology 78:173-181. No good graphs. Hammond, K. A., M. A. Chappell, R. A. Cardullo, R.-S. Lin, T. S. Johnsen. 2000. The mechanistic basis of aerobic performance variation in red jungle fowl. Journal of Experimental Biology 203:2053-2064. Huey, R. B., and A. E. Dunham. 1987. Repeatability of locomotor performance in natural populations of the lizard Sceloporus merriami. Evolution 41:1116-1120. One good graphs of speed between years. Huey, R. B., A. E. Dunham, K. L. Overall, and R. A. Newman. 1990. Variation in locomotor performance in demographically known populations of the lizard Sceloporus merriami. Physiol. Zool. 63:845-872. Iberall, A. S. 1984. An illustration of the experimental range of variation of blood pressure. Am. J. Physiol. 246 (Regulatory Integrative Comp. Physiol. 15):R516-R532. Jayne, B. C., and A. F. Bennett. 1989. The effect of tail morphology on locomotor performance of snakes: a comparison of experimental and correlative methods. J. Exp. Zool. 252:126-133. Krol, E., M. S. Johnson, and J. R. Speakman. 2003. Limits to sustained energy intake VIII. Resting metabolic rate and organ morphology of laboratory mice lactating at thermoneutrality. J. Exp. Biol. 206:4283-4291. Perry, G., K. LeVering, I. Girard, and T. Garland, Jr. 2004. Locomotor performance and social dominance in male Anolis cristatellus. Animal Behaviour 67:37-47. Good graphs. Winners had higher endurance, but not higher speed. Robson, M. A., and D. B. Miles. 2000. Locomotor performance and dominance in male Tree Lizards, Urosaurus ornatus. Functional Ecology 14:338-344. Histograms of winners and lossers, winners faster & higher endurance. Steyermark, A. C. 2002. A high standard metabolic rate constrains juvenile growth. Zoology 105:147-151. Vanhooydonck, B., R. Van Damme, T. J. M. Van Dooren, and D. Bauwens. 2001. Proximate causes of intraspecific variation in locomotor performance in the lizard Gallotia galloti. Physiological and Biochemical Zoology 74:937-946. No good graphs. Williams, T. D. 2008. Review. Individual variation in endocrine systems: moving beyond the 'tyranny of the Golden Mean'. Phil. Trans. R. Soc. B doi:10.1098/rstb.2007.0003. Published online. No good graphs. Zani, P. A. 2001. Clinging performance of the Western fence lizard, Sceloporus occidentalis. Herpetologica 57:423-432. No good graphs, but interesting paper with dead lizards and habitat differences and thermoregulation interaction! Personality things from Careau and Garland (2012)…

64. 64 Hayes, J.P., Jenkins, S.H., 1997. Individual variation in mammals. Journal of Mammalogy 78:274-293.

65. 65 Population Before Selection Mean Before Mean After Population After Selection These Individuals Breed Next Generation Mean Next Generation

66. 66 Midterm 1 Fall 2004 NMeanSDMinMax 21 UG82.611.6458.598.0 8 Grads87.5 6.8474.594.0 All 2984.010.65 ANOVA of UG vs. Grads, 2-tailed P = 0.278 Levene’s test to compare variances, 2-tailed P = 0.063