3. This experiment is described in Douglas J. Emlen, Ian A. Warren, Annika Johns, Ian Dworkin, and Laura Corley Lavine, “A Mechanism of Extreme Growth and Reliable Signaling in Sexually Selected Ornaments and Weapons,” Science 337 (2012): 860–64.
4. J. L. Tomkins, “Environmental and Genetic Determinants of the Male Forceps Length Dimorphism in the European Earwig Forficula auricularia L.,” Behavioral Ecology and Sociobiology 47 (1999): 1–8.
5. P. David, A. Hingle, D. Greig, A. Rutherford, A. Pomiankowski, and K. Fowler, “Male Sexual Ornament Size but Not Asymmetry Reflects Condition in Stalk-Eyed Flies,” Proceedings of the Royal Society of London, Series B 265 (1998): 2211–16; R. J. Knell, A. Fruhauf, and K. A. Norris, “Conditional Expression of a Sexually Selected Trait in the Stalk-Eyed Fly Diasemopsis aethiopica,” Ecological Entomology 24 (1999): 323–28.
6. F. E. French, L. C. McEwen, N. D. Magruder, R. H. Ingram, and R. W. Swift, “Nutrient Requirements for Growth and Antler Development in the White-Tailed Deer,” Journal of Wildlife Management 20 (1956): 221–32; W. Leslie Robinette, C. Harold Baer, Richard E. Pillmore, and C. Edward Knittle, “Effects of Nutritional Change on Captive Mule Deer,” Journal of Wildlife Management 37 (1974): 312–26.
7. Studies of antler growth in red deer (basically, European elk) have begun to elucidate the developmental mechanisms coupling antler growth with nutrition, and the mechanisms they find are thrillingly similar to what we observe in beetle horns. Cells in growing tips of antlers are sensitive to signaling through the insulin/insulin-like growth factor (IGF) pathway, a physiological mechanism that dials cell proliferation up or down depending on the nutritional state of an animal. For relevant studies, see J. M. Suttie, I. D. Corson, P. D. Gluckman, and P. F. Fennessy, “Insulin-Like Growth Factor 1, Growth and Body Composition in Red Deer Stags,” Animal Production 53 (1991): 237–42; J. L. Elliott, J. M. Oldham, G. W. Asher, P. C. Molan, and J. J. Bass, “Effect of Testosterone on Binding of Insulin-Like Growth Factor-I (IGF-I) and IGF-II in Growing Antlers of Fallow Deer (Dama dama),” Growth Regulation 6 (1996): 214; J. R. Webster, I. D. Corson, R. P. Littlejohn, S. K. Martin, and J. M. Suttie, “The Roles of Photoperiod and Nutrition in the Seasonal Increases in Growth and Insulin-Like Growth Factor-1 Secretion in Male Red Deer,” Animal Science 73 (2001): 305–11.
8. P. Fandos, “Factors Affecting Horn Growth in Male Spanish Ibex (Capra pyrenaica),” Mammalia 59 (1995): 229–35; M. Giacometti, R. Willing, and C. Defila, “Ambient Temperature in Spring Affects Horn Growth in Male Alpine Ibexes,” Journal of Mammalogy 83 (2002): 245–51.
9. M. Mulvey and J. M. Aho, “Parasitism and Mate Competition: Liver Flukes in White-Tailed Deer,” Oikos 66 (1993): 187–92. Several studies have also shown that parasites cause antlers to be less symmetrical, rather than simply shorter. For example, see Ivar Folstad, Per Arneberg, and Andrew J. Karte, “Antlers and Parasites,” Oecologia 105 (1996): 556–58; Eystein Markusson and Ivar Folstad, “Reindeer Antlers: Visual Indicators of Individual Quality?” Oecologia 110 (1997): 501–7.
10. Ezenwa and Jolles, “Horns Honestly Advertise Parasite Infection,” 2013–21.
11. B. W. Tucker, “On the Effects of an Epicaridan Parasite, Gyge branchialis, on Upogebia littoralis,” Quarterly Journal of Microscope Science 74 (1930): 1–118; R. G. Hartnoll, “Entionella monensis sp. nov., an Entoniscis Parasite of the Crab Eurynome aspera (Pennant),” Journal of the Marine Biology Association of the United Kingdom 39 (1960): 101–7; T. Yamaguchi and H. Aratake, “Morphological Modifications Caused by Sacculina polygenea in Hemigrapsus sanguineus (De Haan) (Brachyura: Grapsidae),” Crustacean Research 26 (1997): 125–145; Mariappan, Balasundaram, and Schmitz, “Decapod Crustacean Chelipeds,” 301–13.
12. A number of sources speak to the incredible cost of arms and armor of medieval knights, including F. Kottenkamp, History of Chivalry and Ancient Armour (London: Willis and Sotheran Publishers, 1857); G. Duby, The Chivalrous Society, trans. Cynthia Poston (Berkeley: University of California Press, 1977); R. L. O’Connell, Of Arms and Men: A History of War, Weapons, and Aggression (Oxford: Oxford University Press, 1989); J. France, Western Warfare in the Age of the Crusades; 1000–1300 (Ithaca, NY: Cornell University Press, 1999); Constance Brittain Bouchard, Knights: In History and Legend (Lane Cove, Australia: Global Book Publishing, 2009).
13. O’Connell, Of Arms and Men; Bouchard, Knights.
14. Bouchard, Knights.
15. Ibid.
16. Duby, Chivalrous Society; O’Connell, Of Arms and Men; France, Western Warfare in the Age of the Crusades; Bouchard, Knights.
17. Ibid.
18. Ibid.
19. Hypervariability is a signature characteristic of the showiest, most exaggerated ornaments and weapons of sexual selection. For papers discussing this phenomenon in ornaments, see R. V. Alatalo, J. Höglund, and A. Lundberg, “Patterns of Variation in Tail Ornament Size in Birds,” Biological Journal of the Linnean Society of London 34 (1988): 363; S. Fitzpatrick, “Patterns of Morphometric Variation in Birds’ Tails: Length, Shape and Variability,” Biological Journal of the Linnean Society of London 62 (1997): 145; J. J. Cuervo and A. P. Møller, “The Allometric Pattern of Sexually Size Dimorphic Feather Ornaments and Factors Affecting Allometry,” Journal of Evolutionary Biology 22 (2009): 1503. For papers discussing hypervariability in weapons, see H. Frederik Nijhout and Douglas J. Emlen, “The Development and Evolution of Exaggerated Morphologies in Insects,” Annual Review of Entomology 45 (2000): 661–708; Astrid Kodric-Brown, Richard M. Sibly, and James H. Brown, “The Allometry of Ornaments and Weapons,” Proceedings of the National Academy of Sciences 103 (2006): 8733–38; Douglas J. Emlen, “The Evolution of Animal Weapons,” Annual Review of Ecology, Evolution, and Systematics 39 (2008): 387–413.
20. Lots of theoretical models delve into the characteristics of honest signals in animal communication, especially with reference to ornaments and weapons of sexual selection. Early models proposing that the unusual variability of these traits would amplify subtle differences among males are provided in Oren Hasson, “Sexual Displays as Amplifiers: Practical Examples with an Emphasis on Feather Decorations,” Behavioral Ecology 2 (1991): 189–97. Excellent overviews of signaling theory, and of the ingredients of honest signals of male quality, are offered by John Maynard Smith and David Harper, Animal Signals (Oxford: Oxford University Press, 2003); William A. Searcy and Stephen Nowicki, The Evolution of Animal Communication: Reliability and Deception in Signaling Systems (Princeton, NJ: Princeton University Press, 2010); and Jack W. Bradbury and Sandra L. Vehrencamp, Principles of Animal Communication, 2nd ed. (Sunderland, MA: Sinauer Associates, 2011).
21. A number of theoretical models also conclude that small, poor-quality males pay a steeper price for big ornaments or weapons and that, as a result, it’s not cost-effective for them to invest in full-sized structures. For example, see Astrid Kodric-Brown and Jim H. Brown, “Truth in Advertising: The Kinds of Traits Favored by Sexual Selection,” American Naturalist 124 (1984): 309–23; Nadav Nur and Oren Hasson, “Phenotypic Plasticity and the Handicap Principle,” Journal of Theoretical Biology 110 (1984): 275–98; David W. Zeh and Jeanne A. Zeh, “Condition-Dependent Sex Ornaments and Field Tests of Sexual-Selection Theory,” American Naturalist 132 (1988): 454–59; Russell Bonduriansky and Troy Day, “The Evolution of Static Allometry in Sexually Selected Traits,” Evolution 57 (2003): 2450–58; Kodric-Brown, Sibly, and Brown, “The Allometry of Ornaments and Weapons,” 8733–38.
9. Deterrence
1. The beach we hiked into is called Playa Naranjo, in Santa Rosa National Park.
2. Two papers resulting from John Christy’s dissertation work on Devilfish Key are J. H. Christy, “Adaptive Significance of Reproductive Cycles in the Fiddler Crab Uca pugilator: a Hypothesis,” Science 199 (1978): 453–55; and J. H. Christy, “Female Choice in the Resource-Defense Mating System of the Sand Fiddler Crab, Uca pugilator,” Behavioral Ecology and Sociobiology 12 (1983): 169–80.
3. The specific t
ype of interaction described here is called “sequential assessment,” and foundational papers using game theory to model how and when assessment evolves include J. Maynard Smith, “The Theory of Games and the Evolution of Animal Conflicts,” Journal of Theoretical Biology 47 (1974): 209–21; G. A. Parker, “Assessment Strategy and the Evolution of Animal Conflicts,” Journal of Theoretical Biology 47 (1974): 223–43; J. Maynard Smith and G. Parker, “The Logic of Asymmetric Contests,” Animal Behaviour 24 (1976): 159–65; M. Enquist and O. Leimar, “Evolution of Fighting Behaviour: Decision Rules and Assessment of Relative Strength,” Journal of Theoretical Biology 102 (1983): 387–410. More recent overviews of animal signaling, including types of assessment, are provided by J. Maynard Smith and D. Harper, Animal Signals (Oxford: Oxford University Press, 2003); W. A. Searcy and S. Nowicki, The Evolution of Animal Communication: Reliability and Deception in Signaling Systems (Princeton, NJ: Princeton University Press, 2010); J. W. Bradbury and S. L. Vehrencamp, Principles of Animal Communication, 2nd ed. (Sunderland, MA: Sinauer Associates, 2011).
4. Numerous studies demonstrate that males with bigger claws win fights over burrows, including J. Crane, “Combat, Display and Ritualization in Fiddler Crabs (Ocypodidae, genus Uca),” Philosophical Transactions of the Royal Society of London, Series B 251 (1966): 459–72; G. W. Hyatt and M. Salmon, “Combat in the Fiddler Crabs Uca pugilator and U. pugnax: A Quantitative Analysis,” Behaviour 65 (1978): 182–211; M. D. Jennions and P. R. Backwell, “Residency and Size Affect Fight Duration and Outcome in the Fiddler Crab Uca annulipes,” Biological Journal of the Linnean Society 57 (1996): 293–306; A. E. Pratt, D. K. McLain, and G. R. Lathrop, “The Assessment Game in Sand Fiddler Crab Contests for Breeding Burrows,” Animal Behaviour 65 (2003): 945–55. In a fun study using strain gauges, Jeff Levinton and Michael Judge showed that males with bigger claws exert more powerful closing forces. J. S. Levinton and M. L. Judge, “The Relationship of Closing Force to Body Size for the Major Claw of Uca pugnax (Decapoda: Ocypodidae),” Functional Ecology 7 (1993): 339–45.
5. Descriptions of the behavior of sand fiddler crabs, including contests over burrows, are provided in J. H. Christy, “Burrow Structure and Use in the Sand Fiddler Crab, Uca pugilator,” Animal Behaviour 30 (1982): 687–94; Christy, “Female Choice in the Resource-Defense Mating System”; M. Salmon and G. W. Hyatt, “Spatial and Temporal Aspects of Reproduction in North Carolina Fiddler Crabs (Uca pugilator),” Journal of Experimental Marine Biology and Ecology 70 (1983): 21–43; J. Christy and M. Salmon, “Ecology and Evolution of Mating Systems of Fiddler Crabs (genus Uca),” Biological Reviews (1984): 483–509.
6. Stages of fiddler crab fights are described in Crane, “Combat, Display and Ritualization in Fiddler Crabs,” 459–72; Hyatt and Salmon, “Combat in the Fiddler Crabs,” 182–211; Jennions and Backwell, “Residency and Size Affect Fight Duration and Outcome in the Fiddler Crab Uca annulipes,” 293–306.
7. Hyatt and Salmon, “Combat in the Fiddler Crabs,” 182–211.
8. Ibid.
9. Ibid.
10. Maynard Smith, “Theory of Games and the Evolution of Animal Conflicts,” 209–21; Parker, “Assessment Strategy and the Evolution of Animal Conflicts,” 223–43; Smith and Parker, “Logic of Asymmetric Contests,” 159–65; Enquist and Leimar, “Evolution of Fighting Behaviour,” 387–410.
11. Takahisa Miyatake, “Territorial Mating Aggregation in the Bamboo Bug, Notobitus meleagris, Fabricius (Heteroptera: Coreidae),” Journal of Ethology 13 (1995): 185–89; Miyatake, “Multi-Male Mating Aggregation in Notobitus meleagris (Hemiptera: Coreidae),” Annals of the Entomological Society of America 95 (2002): 340–44. For descriptions of similar behavior in additional species of Coreid bug, see Miyatake, “Male-Male Aggressive Behavior Is Changed by Body-Size Difference in the Leaf-Footed Plant Bug, Leptoglossus australis, Fabricius (Heteroptera, Coreidae),” Journal of Ethology 11 (1993): 63–65; Miyatake, “Functional Morphology of the Hind Legs as Weapons for Male Contests in Leptoglossus australis (Heteroptera: Coreidae),” Journal of Insect Behavior 10 (1997): 727–35; W. G. Eberhard, “Sexual Behavior of Acanthocephala declivis guatemalana (Hemiptera: Coreidae) and the Allometric Scaling of Their Modified Hind Legs,” Annals of the Entomological Society of America 91 (1998): 863–71.
12. P. Bergeron, S. Grignolio, M. Apollonio, B. Shipley, and M. Festa-Bianchet, “Secondary Sexual Characters Signal Fighting Ability and Determine Social Rank in Alpine Ibex (Capra ibex),” Behavioral Ecology and Sociobiology 64 (2010): 1299–307.
13. C. Barrette and D. Vandal, “Sparring, Relative Antler Size, and Assessment in Male Caribou,” Behavioral Ecology and Sociobiology 26 (1990): 383–87.
14. The “paradox of peace” is predicted by game theory models of assessment. Theoretically, a perfect cue would result in total peace, since all disputes would be settled conventionally, without battle. See, for example, G. Parker, “Assessment Strategy and the Evolution of Animal Conflicts,” Journal of Theoretical Biology 47 (1974): 223–43.
15. Here I build this story around costs; specifically, the observation that costs are steeper for individuals with fewer resources. This idea is an integral assumption of most models of animal signaling, and it surely applies most of the time. But there are exceptions. As I was writing this book, a doctoral student in my lab, Erin McCullough, was systematically unraveling this notion for the rhinoceros beetle we study. Her work shook the field, because everyone—including myself—assumed that the giant pitchfork horns in these beetles were costly. How could they not be? These weapons are two-thirds the length of the beetle, and they splay forward in front of the animal’s face like a massive pitchfork. Yet, these horns turned out to be remarkably inexpensive to produce, and virtually cost-free to fly around with. For readers interested her work, see E. L. McCullough, P. R. Weingarden, and D. J. Emlen, “Costs of Elaborate Weapons in a Rhinoceros Beetle: How Difficult Is It to Fly with a Big Horn?” Behavioral Ecology 23 (2012): 1042–48; E. L. McCullough and B. W. Tobalske, “Elaborate Horns in a Giant Rhinoceros Beetle Incur Negligible Aerodynamic Costs,” Proceedings of the Royal Society of London, Series B 280 (2013): 1–5; and E. L. McCullough and D. J. Emlen, “Evaluating Costs of a Sexually Selected Weapon: Big Horns at a Small Price,” Animal Behaviour 86 (2013) 977–85.
16. Most observers don’t count these early stages in their tallies because they dissipate so quickly. Barrette and Vandal did include them in their two-year study of caribou contests. Of the 11,640 male-male interactions they observed, 10,332 ended at this initial stage. Barrette and Vandal, “Sparring, Relative Antler Size, and Assessment in Male Caribou,” 383–87.
17. A. Berglund, A. Bisazza, and A. Pilastro, “Armaments and Ornaments: An Evolutionary Explanation of Traits of Dual Utility,” Biological Journal of the Linnean Society 58 (1996): 385–99.
18. D. S. Pope, “Testing Function of Fiddler Crab Claw Waving by Manipulating Social Context,” Behavioral Ecology and Sociobiology 47 (2000): 432–37; M. Murai and P. R. Y. Backwell, “A Conspicuous Courtship Signal in the Fiddler Crab Uca perplexa: Female Choice Based on Display Structure,” Behavioral Ecology and Sociobiology 60 (2006): 736–41; D. K. McLain and A. E. Pratt, “Approach of Females to Magnified Reflections Indicates That Claw Size of Waving Fiddler Crabs Correlates with Signaling Effectiveness,” Journal of Experimental Marine Biology and Ecology 343 (2007): 227–38.
19. T. Detto, “The Fiddler Crab Uca mjoebergi Uses Colour Vision in Mate Choice,” Proceedings of the Royal Society, Series B 274 (2007): 2785–90.
20. Dietrich Burkhardt and Ingrid de la Motte, “Big ‘Antlers’ are Favoured: Female Choice in Stalk-Eyed Flies (Diptera, Insecta), Field Collected Harems and Laboratory Experiments,” Journal of Comparitive Physiology A 162 (1988): 649–52; G. S. Wilkinson and P. R. Reillo, “Female Choice Response to Artificial Selection on an Exaggerated Male Trait in a Stalk-Eyed Fly,” Proceedings of the Royal Society of London, Series B 255 (1994): 1–6; G. S. Wilkinson, H. Kahler, and R. H. Baker, “Evolution of Fem
ale Mating Preferences in Stalk-Eyed Flies,” Behavioral Ecology 9 (1998): 525–33.
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