7. W. J. Freeland, “Pathogens and the Evolution of Primate Sociality,” Biotropica 8, no. 1 (1976).
8. R. Dawkins, The Selfish Gene (New York: Oxford University Press, 1976).
9. J. Keisecker et al., “Behavioral Reduction of Infection Risk,” Proceedings of the National Academy of Sciences USA 96 (1999).
10. J. Krause and J.-G. J. Godin, “Influence of Parasitism on the Shoaling Behaviour of Banded Killifish, Fundulus diaphanus,” Canadian Journal of Zoology 72 (1994).
11. D. C. Behringer, M. J. Butler, and J. D. Shields, “Avoidance of Disease by Social Lobsters,” Nature 441 (2006).
12. Freeland, “Pathogens and the Evolution of Primate Sociality.” Some doubt has been cast on these proposals by primatologists; the issue of primate social disease defense still requires definitive study.
13. D. W. Pfennig, M. L. G. Loeb, and J. P. Collins, “Pathogens as a Factor Limiting the Spread of Cannibalism in Tiger Salamanders,” Oecologia 88 (1991).
14. M. Oaten, R. J. Stevenson, and T. I. Case, “Disease Avoidance as a Functional Basis for Stigmatization,” Philosophical Transactions of the Royal Society B 366, no. 1583 (2011).
15. De Barra, “Attraction and Aversion.”
16. H. Schulenburg and S. Muller, “Natural Variation in the Response of Caenorhabditis elegans towards Bacillus thuringiensis,” Parasitology 128 (2004).
17. Cremer, Armitage, and Schmid-Hempel, “Social Immunity.”
18. A. Karvonen, O. Seppala, and E. T. Valtonen, “Parasite Resistance and Avoidance Behaviour in Preventing Eye Fluke Infections in Fish,” Parasitology 129, no. 2 (2004).
19. G. S. Wilkinson, “Social Grooming in the Common Vampire Bat, Desmodus rotundus,” Animal Behaviour 34, no. 6 (1986).
20. M. S. Mooring, A. A. McKenzie, and B. L. Hart, “Grooming in Impala: Role of Oral Grooming in Removal of Ticks and Effects of Ticks in Increasing Grooming Rate,” Physiology and Behavior 59 (1996).
21. P. R. Ehrlich, D. S. Dobkin, and D. Wheye, “The Adaptive Significance of Anting,” Auk 103, no. 4 (1986).
22. J. T. Longino, “True Anting by the Capuchin, Cebus capucinus,” Primates 25, no. 2 (1984); M. Zito, S. Evans, and P. J. Weldon, “Owl Monkeys (Aotus spp.) Self-Anoint with Plants and Millipedes,” Folia Primatologica 74, no. 3 (2003).
23. R. Norval et al., “The Effect of the Bont Tick (Amblyomma hebraeum) on the Weight Gain of Africander Steers,” Veterinary Parasitology 33, no. 3 (1989), cited in Mooring, McKenzie, and Hart, “Grooming in Impala.”
24. C. B. Weddle, “Effects of Ectoparasites on Nestling Body Mass in the House Sparrow,” Condor 102, no. 3 (2000).
25. M. D. Gumert, “Payment for Sex in a Macaque Mating Market “Animal Behaviour 74, no. 6 (2007).
26. D. H. Clayton, “Coevolution of Avian Grooming and Ectoparasite Avoidance,” in Bird-Parasite Interactions: Ecology, Evolution, and Behaviour, ed. J. E. Loye and M. Zuk (Oxford: Oxford University Press, 1991).
27. S. J. O’Hara and P. C. Lee, “High Frequency of Post-Coital Penis Cleaning in Budongo Chimpanzees,” Folia Primatologica 77, no. 5 (2006).
28. B. L. Hart, E. Korinek, and P. Brennan, “Postcopulatory Genital Grooming in Male Rats: Prevention of Sexually Transmitted Infections,” Physiology and Behavior 41, no. 4 (1987).
29. M. Pagel and W. Bodmer, “A Naked Ape Would Have Fewer Parasites,” Biology Letters 270, no. S1 (2003).
30. K. Norris, “A Trade-Off between Energy Intake and Exposure to Parasites in Oystercatchers Feeding on a Bivalve Mollusc,” Proceedings of the Royal Society of London B 266, no. 1429 (1999).
31. G. S. Aeby, “Trade-Offs for the Butterflyfish, Chaetodon multicinctus, when Feeding on Coral Prey Infected with Trematode Metacercariae,” Behavioral Ecology and Sociobiology 52 (2002).
32. S. Temple, “Do Predators Always Capture Substandard Individuals Disproportionately from Prey Populations?” Ecology 68, no. 3 (1987).
33. N. R. Franks et al., “Tomb Evaders: House-Hunting Hygiene in Ants,” Biology Letters 1 (2005).
34. E. Diehl-Fleig and M. E. Lucchese, “Reações comportamentais de operárias de Acromyrmex striatus (Hymenoptera, Formicidae) na presença de fungos entomopatogênicos,” Revista Brasileira de Entomologia 35 (1991). However, Sylva Cremer has just shown that sometimes ants will cluster around conspecifics infested with fungal pathogens and collect the spores, and so get the benefit of immunization. M. Konrad et al., “Social Transfer of Pathogenic Fungus Promotes Active Immunisation in Ant Colonies,” PLOS Biology 10, no. 4 (2012).
35. E. Decaestecker, L. De Meester, and D. Ebert, “In Deep Trouble: Habitat Selection Constrained by Multiple Enemies in Zooplankton,” Proceedings of the National Academy of Sciences USA 99, no. 8 (2002).
36. A. Oppliger, H. Richner, and P. Christie, “Effect of an Ectoparasite on Lay Date, Nest Site Choice, Desertion and Hatching Success in the Great Tit (Parus major),” Behavioural Ecology 5, no. 2 (1994).
37. S. A. Hosoi and S. I. Rothstein, “Nest Desertion and Cowbird Parasitism: Evidence for Evolved Responses and Evolutionary Lag,” Animal Behaviour 59, no. 4 (2000).
38. M. R. Hutchings et al., “The Herbivores’ Dilemma: Trade-Offs between Nutrition and Parasitism in Foraging Decisions,” Oecologia 124 (2000).
39. Dung-based nematodes tend to increase egg laying during the spring calving. A. Gunn and R. J. Irvine, “Subclinical Parasitism and Ruminant Foraging Strategies: A Review,” Wildlife Society Bulletin 31, no. 1 (2003). Other parasites, such as warble fly, have been shown to cause more of a problem the less migratory the host species: I. Folstad, O. Halvorsen, and A. C. Nilssen, “Parasite Avoidance: The Cause of Post-Calving Migrations in Rangifer?” Canadian Journal of Zoology 69, no. 9 (1991).
40. Martin Kavaliers, personal communication.
41. M. R. Weiss, “Good Housekeeping: Why Do Shelter-Dwelling Caterpillars Fling Their Frass?” Ecology Letters 6, no. 4 (2003).
42. J. E. Weaver and R. A. Sommers, “Life History and Habits of the Short-Tailed Cricket, Anurogryllus muticus, in Central Louisiana,” Annals of the Entomological Society of America 62, no. 2 (1969).
43. V. G. Dethier, The World of the Tent-Makers: A Natural History of the Eastern Tent Caterpillar (Amherst: University of Massachusetts Press, 1980).
44. T. Eisner, E. van Tassell, and J. E. Carrel, “Defensive Use of a ‘Fecal Shield’ by a Beetle Larva,” Science 158 (1967).
45. A. G. Hart and F. L. W. Ratnieks, “Task Partitioning, Division of Labour and Nest Compartmentalisation Collectively Isolate Hazardous Waste in the Leafcutting Ant Atta cephalotes,” Behavioral Ecology and Sociobiology 49, no. 5 (2001); P. Schmid-Hempel, Parasites in Social Insects (Princeton, NJ: Princeton University Press, 1998).
46. M. J. West and R. D. Alexander, “Sub-Social Behavior in a Burrowing Cricket Anurogryllus muticus (De Geer),” Ohio Journal of Science 63 (1963); Y. Sato, Y. Saito, and T. Sakagami, “Rules for Nest Sanitation in a Social Spider Mite, Schizotetranychus miscanthi Saito (Acari: Tetranychidae),” Ethology 109, no. 9 (2003).
47. M. R. Pie, R. B. Rosengaus, and J. F. A. Traniello, “Nest Architecture, Activity Pattern, Worker Density and the Dynamics of Disease Transmission in Social Insects,” Journal of Theoretical Biology 226, no. 1 (2004).
48. B. Hölldobbler and E. O. Wilson, The Ants (Cambridge, MA: Harvard University Press, 1990).
49. Ibid.
50. Cremer, Armitage, and Schmid-Hempel, “Social Immunity.”
51. R. Krone et al., “Defecation Behaviour of the Lined Bristletooth Surgeonfish Ctenochaetus striatus (Acanthuridae),” Coral Reefs 27, no. 3 (2008).
52. G. E. Brown, D. P. Chivers, and R. J. F. Smith, “Localized Defecation by Pike: A Response to Labelling by Cyprinid Alarm Pheromone?” Behavioral Ecology and Sociobiology 36, no. 2 (1995).
53. N. V. C. Polunin and I. Koike, “Temporal Focusing of Nitrogen Release by a Periodically Feeding Herbivorous Reef Fish,” Journal of Experimental Marine Biology and Ecology 111, no. 3 (1987).
54. J
. S. Brashares and P. Arcese, “Scent Marking in a Territorial African Antelope: II. The Economics of Marking with Faeces,” Animal Behaviour 57, no. 1 (1999).
55. There are examples of all these behaviors in multiple species of birds. See, for example, R. H. Blair and B. W. Tucker, “Nest Sanitation,” British Birds 34 (1941); W. A. Montevecchi, “Eggshell Removal by Laughing Gulls,” Bird-Banding 47, no. 2 (1976); S. Hurtrez!-Boussès et al., “Effects of Ectoparasites of Young on Parents’ Behaviour in a Mediterranean Population of Blue Tits,” Journal of Avian Biology 31, no. 2 (2000); H. Mayfield, “Nesting Success Calculated from Exposure,” Wilson Bulletin (1961); A. Mennerat et al., “Aromatic Plants in Nests of the Blue Tit Cyanistes caeruleus Protect Chicks from Bacteria,” Oecologia 161, no. 4 (2009); F. R. Gehlbach and R. S. Baldridge, “Live Blind Snakes (Leptotyphlops dulcis) in Eastern Screech Owl (Otus asio) Nests: A Novel Commensalism,” Oecologia 71, no. 4 (1987).
56. V. B. Meyer-Rochow and J. Gal, “Pressures Produced When Penguins Pooh: Calculations on Avian Defaecation,” Polar Biology 27 (2003).
57. P. T. Fretwell and P. N. Trathan, “Penguins from Space: Faecal Stains Reveal the Location of Emperor Penguin Colonies,” Global Ecology and Biogeography 18, no. 5 (2009).
58. These swallows can be seen at http://www.youtube.com/watch?v=Fa5CluKJxGM.
59. C. Petit et al., “Blue Tits Use Selected Plants and Olfaction to Maintain an Aromatic Environment for Nestlings,” Ecology Letters 5 (2002).
60. P. H. Wimberger, “The Use of Green Plant Material in Bird Nests to Avoid Ectoparasites,” Auk 101, no. 3 (1984); L. Clark and J. R. Mason, “Use of Nest Material as Insecticidal and Anti-Pathogenic Agents by the European Starling,” Oecologia 67, no. 2 (1985).
61. Hurtrez-Boussès et al., “Effects of Ectoparasites of Young”; J. Banbura et al., “Sex Differences in Parental Care in a Corsican Blue Tit Parus caeruleus Population,” Ardea 89, no. 3 (2001).
62. Gehlbach and Baldridge, “Live Blind Snakes.”
63. The word parasite itself—which comes from para-sitos, meaning “beside-bread”—has its origins in the custom of ancient Greece. Priests shared their food at temples; those who relied on such handouts came to be seen as hangers-on and welfare cheats. Robert Parker, personal communication.
64. J. Garcia, D. Forthman-Quick, and B. White, “Conditioned Disgust and Fear from Mollusk to Monkey,” in Primary Neural Substrates of Learning and Behavioral Change (New York: Cambridge University Press, 1984), 57.
65. A common use of serotonin in avoidance behavior across animals is possible. M. Rubio-Godoy, R. Aunger, and V. Curtis, “Serotonin: A Link between Disgust and Immunity?” Medical Hypotheses 68, no. 1 (2007).
66. The standard model of disgust seems to imply this, e.g., Rozin, Haidt, and McCauley, “Disgust.”
Chapter Three
1. D. W. Pfennig, S. G. Ho, and E. A. Hoffman, “Pathogen Transmission as a Selective Force against Cannibalism,” Animal Behaviour 55, no. 5 (1998).
2. J. B. H. Savigny and A. Corréard, Narrative of a Voyage to Senegal in 1816: Undertaken by Order of the French Government, Comprising an Account of the Shipwreck of the Medusa, the Sufferings of the Crew, and the Various Occurrences on Board the Raft, in the Desert of Zaara, at St. Louis, and at the Camp of Daccard . . . (London: H. Col-burn, 1818).
3. The big five dimensions of personality are openness, conscientiousness, extraversion, agreeableness, and neuroticism. J. Hennig, P. Pössel, and P. Netter, “Sensitivity to Disgust as an Indicator of Neuroticism: A Psychobiological Approach,” Personality and Individual Differences 20, no. 5 (1996). But for a differing view, see J. M. Tybur et al., “Sex Differences and Sex Similarities in Disgust Sensitivity,” Personality and Individual Differences 51, no. 3 (2011).
4. D. Nettle, Personality: What Makes You the Way You Are (Oxford: Oxford University Press, 2007).
5. D. Nettle, “The Evolution of Personality Variation in Humans and Other Animals,” American Psychologist 61, no. 6 (2006).
6. M. Wolf and F. J. Weissing, “Animal Personalities: Consequences for Ecology and Evolution,” Trends in Ecology and Evolution 27, no. 8 (2012).
7. A. Sih, A. Bell, and J. C. Johnson, “Behavioral Syndromes: An Ecological and Evolutionary Overview,” Trends in Ecology and Evolution 19, no. 7 (2004).
8. V. Curtis, R. Aunger, and T. Rabie, “Evidence That Disgust Evolved to Protect from Risk of Disease,” Proceedings of the Royal Society B 271, supplement 4 (2004).
9. Rozin, Haidt, and McCauley, “Disgust.”
10. See Unilever’s award-winning ad for Lynx deodorant at http://www.youtube.com/watch?v=ensckApupW0, for example.
11. D. M. T. Fessler, S. J. Eng, and C. D. Navarrete, “Elevated Disgust Sensitivity in the First Trimester of Pregnancy: Evidence Supporting the Compensatory Prophylaxis Hypothesis,” Evolution and Human Behavior 26 (2005).
12. S. M. Flaxman and P. W. Sherman, “Morning Sickness: A Mechanism for Protecting Mother and Embryo,” Quarterly Review of Biology 75, no. 2 (2000); G. V. Pepper and S. C. Roberts, “Rates of Nausea and Vomiting in Pregnancy and Dietary Characteristics across Populations,” Proceedings of the Royal Society B 273, no. 1601 (2006).
13. D. S. Fleischman and D. M. T. Fessler, “Progesterone’s Effects on the Psychology of Disease Avoidance: Support for the Compensatory Behavioral Prophylaxis Hypothesis,” Hormones and Behavior 59, no. 2 (2011).
14. M. Schaller et al., “Mere Visual Perception of Other People’s Disease Symptoms Facilitates a More Aggressive Immune Response,” Psychological Science 21, no. 5 (2010).
15. Rubio-Godoy, Aunger, and Curtis, “Serotonin: A Link between Disgust and Immunity?”
16. O. Curno et al., “Mothers Produce Less Aggressive Sons with Altered Immunity When There Is a Threat of Disease during Pregnancy,” Proceedings of the Royal Society of London B 276, no. 1659 (2009).
17. A. Hoefling et al., “When Hunger Finds No Fault with Moldy Corn: Food Deprivation Reduces Food-Related Disgust,” Emotion 9, no. 1 (2009).
18. D. Ariely, Predictably Irrational: The Hidden Forces That Shape Our Decisions (London: HarperCollins, 2008).
19. Otherwise known as the learned taste aversion.
20. Garcia, Forthman-Quick, and White, “Conditioned Disgust and Fear.” Pond snails also acquire differential conditioned taste aversion to either sucrose or carrot juice paired with lithium chloride (LiCl). R. Sugai et al., “Taste Discrimination in Conditioned Taste Aversion of the Pond Snail Lymnaea stagnalis,” Journal of Experimental Biology 209, no. 5 (2006).
21. M. E. P. Seligman, “Phobias and Preparedness,” Behavior Therapy 2, no. 3 (1971).
22. R. Soussignan et al., “Facial and Autonomic Responses to Biological and Artificial Olfactory Stimuli in Human Neonates: Re-examining Early Hedonic Discrimination of Odors,” Physiology and Behavior 62, no. 4 (1997); Y. Yeshurun and N. Sobel, “An Odor Is Not Worth a Thousand Words: From Multidimensional Odors to Unidimensional Odor Objects,” Annual Review of Psychology 61 (2010).
23. At the recent disgust conference in Bielefeld, I learned from Martin Kavaliers, who studies aversions in rodents, that mice tend to avoid mice who have been in contact with sick mice. This is close to the human ability to detect contamination using the memory of what has been in contact with what, but a chemical pathway can’t be ruled out.
24. R. F. Baumeister, K. D. Vohs, and C. Nathan DeWall, “How Emotion Shapes Behavior: Feedback, Anticipation, and Reflection, Rather Than Direct Causation,” Personality and Social Psychology Review 11, no. 2 (2007).
25. G. C. L. Davey et al., “A Cross-Cultural Study of Animal Fears,” Behaviour Research and Therapy 36 (1998); B. O. Olatunji, J. P. Forsyth, and A. Cherian, “Evaluative Differential Conditioning of Disgust: A Sticky Form of Relational Learning That Is Resistant to Extinction,” Journal of Anxiety Disorders 21 (2007).
26. S. Rachman, “Fear of Contamination,” Behaviour Research and Therapy 42 (2004).
27. D. F. Tolin, P. Worhunsky, and N. Maltby, “Sym
pathetic Magic in Contamination-Related OCD,” Journal of Behavior Therapy and Experimental Psychiatry 35, no. 2 (2004).
28. I will discuss controversies about group selection in chapter 6.
29. This idea is highly controversial at present. Two recent additions to the debate are from Steven Pinker, who does not subscribe to group selection as a force in human evolution: “The False Allure of Group Selection,” Edge, http://edge.org/conversation/the-false-allure-of-group-selection (2012); and E. O. Wilson, who champions it: The Social Conquest of Earth (New York: Liveright Publishing, 2012).
30. S. Lindenbaum, “Understanding Kuru: The Contribution of Anthropology and Medicine,” Philosophical Transactions of the Royal Society B 363, no. 1510 (2008); D. C. Gajdusek, “Unconventional Viruses and the Origin and Disappearance of Kuru,” in Nobel Lectures in Physiology or Medicine, 1971–1980, ed. J. Lindsten (Stockholm: Karolinska Institute, 1977).
31. G. Cochran and H. Harpending, The 10,000 Year Explosion: How Civilization Accelerated Human Evolution (New York: Basic Books, 2010).
32. Thanks to master gamer Justin Aunger for providing the gory details.
33. W. Arens, The Man-Eating Myth: Anthropology and Anthropophagy (Oxford: Oxford University Press, 1979).
34. J. M. Diamond, “Archaeology: Talk of Cannibalism,” Nature 407, no. 6800 (2000).
35. R. A. Marlar et al., “Biochemical Evidence of Cannibalism at a Prehistoric Puebloan Site in Southwestern Colorado,” Nature 407, no. 6800 (2000).
36. For a more complete account of disgust as an adaptive system, see Curtis, de Barra, and Aunger, “Disgust as an Adaptive System.”
Chapter Four
1. S. L. Carter, Civility: Manners, Morals, and the Etiquette of Democracy (New York: Basic Books, 1998).
2. Norbert Elias’s book The Civilizing Process (1939; trans E. Jephcott [Malden, MA: Blackwell, 2000]) made the biggest contribution, suggesting that changing social attitudes molded standards of behavior regarding bodily functions, clothing, and forms of speech from the courtly behavior of the late Middle Ages to the present day. The structuralist sociologist Pierre Bourdieu (“Social Space and Symbolic Power,” Sociological Theory 7, no. 1 [1989]) has manners a part of the human habitus, the taken-for-granted, tacit codes of conduct into which we are socialized and which serve primarily to symbolize and signal our social status. Following this line of thought, Michèle Lamont’s book Money, Morals, and Manners (Chicago: University of Chicago Press, 1992) explored how the upper classes in the United States and France distinguish themselves as a group apart: “High-class people despise vulgarity and bad manners and greatly appreciate charm and intelligence” (167). However, Lamont does not attempt to explain manners. Nor does Claude Lévi-Strauss in the volume of his magnum opus Mythologiques entitled The Origin of Table Manners (Chicago: University of Chicago Press, 1990).
Don't Look, Don't Touch, Don't Eat: The Science Behind Revulsion Page 13
