38. For information about the biology of mammoths I recommend Adrian Lister and Paul Bahn, Mammoths: Giants of the Ice Age (Berkeley: University of California Press, 2009). For a broader treatment of the extraordinary beasts of this age, I recommend Ian Lange, Ice Age Mammals of North America: A Guide to the Big, the Hairy, and the Bizarre (Missoula, MT: Mountain Press, 2002). And for an exciting narrative account of adventure in search of frozen mammoths, read Richard Stone, Mammoth: The Resurrection of An Ice Age Giant (Cambridge, MA: Perseus, 2002). For a comprehensive and technical treatment of fossil elephants and their relatives, I recommend J. Shoshani and P. Tassy, eds., The Proboscidea: Evolution and Paleoecology of Elephants and Their Relatives (Oxford: Oxford University Press, 1996).
39. I recommend the beautiful treatise on stag beetles by T. Mizunuma and S. Nagai, The Lucanid Beetles of the World, part of Mushi Sha’s Iconographic Series of Insects, 1st ed., ed. H. Fijita (Tokyo: Mushi-Sha publishers, 1994). This book is written in Japanese, but has an English summary, and the illustrations speak for themselves!
40. Tadatsugu Hosoya and Kunio Araya, “Phylogeny of Japanese Stag Beetles (Coleoptera: Lucanidae) Inferred from 16s mtrRNA Gene Sequences, with References to the Evolution of Sexual Dimorphism of Mandibles,” Zoological Science 22 (2005): 1305–18.
41. David Grimaldi and Gene Fenster, “Evolution of Extreme Sexual Dimorphisms: Structural and Behavioral Convergence Among Broad-Headed Male Drosophilidae (Diptera),” American Museum Novitates 2939 (1989): 1–25.
42. A comprehensive and well-written treatise on fossil ungulates and ungulate evolution is Donald Prothero and Robert Schoch, Horns, Tusks, and Flippers: The Evolution of Hoofed Mammals (Baltimore: Johns Hopkins University Press, 2003). I also recommend the more recent volume edited by Donald Prothero and Scott Foss, The Evolution of Artiodactyls (Baltimore: Johns Hopkins University Press, 2007); and the book by Elizabeth Vrba and George Schaller, eds., Antelopes, Deer, and Relatives: Fossil Record, Behavioral Ecology, Systematics, and Conservation (New Haven, CT: Yale University Press, 2000). All of these cover the major patterns of evolution (and weapon radiation) in ungulates. Several authors have also used diversity in behavior and morphology of living ungulates to suggest how and why weapons have diversified. For example, see the book by Valerius Geist, Deer of the World: Their Evolution, Behaviour, and Ecology (Mechanicsburg, PA: Stackpole Books, 1998); and these papers: T. M. Caro, C. M. Graham, C. J. Stoner, and M. M. Flores, “Correlates of Horn and Antler Shape in Bovids and Cervids,” Behavioral Ecology and Sociobiology 55 (2003): 32–41; G. A. Lincoln, “Teeth, Horns and Antlers: The Weapons of Sex,” in The Differences Between the Sexes, ed. R. V. Short and E. Balaban (Cambridge: Cambridge University Press, 1994): 131–58; J. Bro-Jørgensen, “The Intensity of Sexual Selection Predicts Weapon Size in Male Bovids,” Evolution 61 (2007): 1316–26; and B. Lundrigan, “Morphology of Horns and Fighting Behavior in the Family Bovidae,” Journal of Mammology 77 (1996): 462–75.
7. Costs
1. The beetle species I studied is a tiny brown dung beetle called Onthophagus acuminatus. They are active primarily in the early morning, but also throughout the daytime, and they specialize on dung from howler monkeys. They fly only inches above the leaf litter of the forest floor, hovering in gentle back-and-forth undulations as they clumsily make their way toward fresh dung. Once they find the dung, they burrow inside it and into the soil below (one reason they are almost never noticed).
2. All those forays into the forest were not without adventure. I remember one morning with frightful clarity. It had been one of the dreaded days when the monkeys were not at all close to my room. I had not heard the dawn chorus and, as a result, I’d had to hike three miles into the forest in search of dung. My first finds had all been tiny—not nearly enough to feed the hundreds of beetles waiting in their tubes in the lab. The problem with “false starts” such as these is that at each collection I use one of the pairs of surgical gloves I kept stashed in my pocket. After several insufficient stops I begin to run out of gloves. Mucking with monkey dung is unpleasant enough as it is; having disposable gloves gives me at least a modicum of cleanliness. This way, when I’m done, I can strip my gloves, turning them inside out and trapping the filth inside them as I go. This leaves my hands relatively clean and keeps dung out of my lunch, water bottle, and binoculars.
Three miles from the lab and well into my last pair of gloves, I finally found the stash of dung that I needed. However, as I was filling my bags, I brushed against a palm frond that was covered with ticks. Any tropical biologist can tell you about “seed ticks,” the bundles of babies (technically nymphs) that clump together on the tips of big leaves. Hundreds can pile together into a ball the size of a marble. Bump them and they hurl themselves onto your body and begin to disperse. For this reason, standard forest garb is long pants tucked into socks, and a loose-fitting long-sleeved cotton shirt tucked into the pants. This works pretty well to keep stinging ants or tiny ticks from getting directly onto your skin. The other trick is to carry tape. Masking tape is best, and for easy access most of us would stick several strips along our pants legs over our thighs. When we happened upon a ball of ticks we could grab the tape and use it to blot the babies off of us in seconds, before they got past our clothing barrier.
My dilemma that morning was that I was on my last pair of gloves, and they had already started to tear. If I peeled them off I would never be able to get them back on again. I couldn’t manage the tape with the gloves on, and I didn’t want to harvest all the dung bare-handed, so I ignored the ticks for the moment and finished filling my bags. It took only another five minutes or so before I was done but, to my horror, that was too long. I ripped the gloves off, grabbed the tape, and looked for the ticks. They were gone. In those few short minutes they had dispersed across my body, and I couldn’t find them.
The three-mile run back to the lab was agony. I could feel the ticks crawling inside my shirt, down my legs and crotch, in my hair, behind my ears, even in my nose and around my eyes as I ran. I flung the dung bags into the lab and dashed to my room, jumping out of my clothes into a scalding and soapy shower, to no avail. They would not wash off. It took more than an hour with tweezers under an intense bright light to peel the ticks from my skin, plucking them from the places they had lodged themselves and sticking them onto strips of tape like so many flecks of pepper. In the end I counted almost eight hundred ticks on those clogged strips of tape. Though it had only been an hour since I bumped that unfortunate frond, most of the ticks had already injected their anticoagulant salivary juices, and the itching that commenced was unreal. I chewed antihistamines for a week. Convinced that she would think I was exaggerating, I promptly sent the tick-laden strips of tape to my girlfriend (now wife) back at Duke, where she was at that time a doctoral student. You can imagine how well that went down. Apparently, field-biologist bravado is not the same thing as romance.
3. D. J. Emlen, “Artificial Selection on Horn Length-Body Size Allometry in the Horned Beetle Onthophagus acuminatus,” Evolution 50 (1996): 1219–30.
4. Trade-offs among developing structures are widespread in insects, and they constitute a dramatic cost of growing elaborate weapons. But this particular cost—stunted growth of other structures—applies primarily to insects such as beetles, flies, ants, and bees. It does not apply to any animals that I am aware of outside of insects. The reason almost certainly has to do with the way these particular insects develop. Specifically, it has to do with when, during development, all of the various adult structures are formed.
Exaggerated weapons of sexual selection always grow at the end of development, around the time when males reach sexual maturity. Deer, elk, and moose all begin antler growth only after males are young adults. Elephants and boars grow their tusks after they are adults. Even shrimp and crabs begin the process of enlargement of their fighting claws around the time that their gonads mature. In all of these animals, bodies have already grown and organs, tissues, and appendages ar
e already at or near their adult proportions, long before the weapons begin to grow.
Weapons cannot stunt the growth of other traits in these animals because all of the other structures are produced first. In contrast, beetles, bees, flies, and ants all undergo metamorphosis as they develop, and this means that they grow their adult body parts at the same time as their weapons. Simultaneous growth exposes these structures to the insidious effects of resource limitation and allocation trade-offs.
5. The most convincing ways to show this all involve some type of experimental perturbation to growing animals. When I selected for longer horns in dung beetles, increased horn growth led to reduced eye size. Using a hot needle to kill the cells of the developing horn in another dung beetle species produced adults with unusually large testes, implicating a resource allocation trade-off between weapons and testes. L. W. Simmons and D. J. Emlen, “Evolutionary Trade-Off Between Weapons and Testes,” Proceedings of the National Academy of Sciences 103 (2006): 16346–51. A reverse experiment, ablating cells of the developing genitalia, increased horn length in still another species. A. P. Moczek and H. F. Nijhout, “Trade-Offs During the Development of Primary and Secondary Sexual Traits in a Horned Beetle,” American Naturalist 163 (2004): 184–91. In species after species, when males produce disproportionately large weapons other structures suffer, including traits critical for reproduction such as testes.
6. K. Kawano, “Horn and Wing Allometry and Male Dimorphism in Giant Rhinoceros Beetles (Coleoptera: Scarabaeidae) of Tropical Asia and America,” Annals of the Entomological Society of America 88 (1995): 92–99.
7. K. Kawano, “Cost of Evolving Exaggerated Mandibles in Stag Beetles (Coleoptera: Lucanidae),” Annals of the Entomological Society of America 90 (1997): 453–61.
8. Catherine Fry, then a doctoral student at the University of Maryland, used topical applications of a developmental hormone called “juvenile hormone” to perturb the growth of male eyestalks. This hormone is known to regulate growth of a number of insect structures, including the distorted heads and weapons of soldier castes in termites and ants. When she painted synthetic juvenile hormone onto developing male larvae, they emerged as adults with disproportionately long eyestalks—she perturbed the relative size of the male weapon. But these males also had drastically reduced testes and, when these males later mated, they were able to transfer only two-thirds as many sperm as males not exposed to the hormone. C. Fry, “Juvenile Hormone Mediates a Trade-Off Between Primary and Secondary Sexual Traits in Stalk-Eyed Flies,” Evolution and Development 8 (2006): 191–201. For her doctoral dissertation, Catherine Fry used two related species of stalk-eyed flies that differ in the relative sizes of their eyestalks to investigate whether eye-span exaggeration results in trade-offs with other body parts. In one species, Cyrtodiopsis dalmanni, males have exaggerated eye spans that are much longer than those of females. In the other, C. quinqueguttata, both sexes have approximately equal eyestalks, which are relatively unexaggerated in length. She used a variety of experimental approaches (including artificial selection, application of exogenous juvenile hormone, and diet manipulation) to perturb the relative length of the eye stalks. She showed that exaggerated eye span in male C. dalmanni is accompanied by a decrease in two other features of head morphology, eye bulb size and eye stalk width, as well as compromised testis growth and sperm production.
9. The Australian sweat bee Lasioglossum hemichalceum produces males with robust, expanded heads and jaws that dwarf the remainders of their tiny bodies (think lentils glued to the tips of rice grains, and you get the general idea). These top-heavy fighters have puny little wings and almost no wing muscles, and they cannot fly. Instead, they remain in their home nest after they emerge, fighting to the death with their brothers for the opportunity to mate with their newly emerging sisters. This same bee species also has smaller, more “typical” males that lack weapons, and these unarmed males can fly. They disperse from their burrow to seek out neighboring nests and females. After the big-headed males have mated with all of their sisters, they, too, venture out from their nest in search of females. But, unlike their flying counterparts, these males must crawl. Crawling the tens of meters between nests is an exceedingly laborious process for a rice-grain-sized bee with a bloated head, and it is almost always fatal because they’re exposed to predators all along the way. The price of winning fights for the chance to mate with your sisters is an utter inability to make it to neighboring nests. P. F. Kukuk and M. Schwarz, “Macrocephalic Male Bees as Functional Reproductives and Probable Guards,” Pan-Pacific Entomologist 64 (1988): 131–37.
10. Cardiocondyla ants produce two types of male, one type that fights and another that does not. Here, too, males develop either with formidable weapons (enlarged heads and jaws), or with wings and wing musculature, but never both. J. Heinze, B. Hölldobler, and K. Yamauchi, “Male Competition in Cardiocondyla Ants,” Behavioral Ecology and Sociobiology 42 (1998): 239–46; S. Cremer and J. Heinze, “Adaptive Production of Fighter Males: Queens of the Ant Cardiocondyla Adjust the Sex Ratio Under Local Mate Competition,” Proceedings of the Royal Society of London, Series B 269 (2002): 417–22.
11. J. Crane, Fiddler Crabs of the World (Ocypodidae: Genus Uca) (Princeton, NJ: Princeton University Press, 1975).
12. B. J. Allen and J. S. Levinton, “Costs of Bearing a Sexually Selected Ornamental Weapon in a Fiddler Crab,” Functional Ecology 21 (2007): 154–61.
13. Masatoshi Matsumasa and Minoru Murai were able to measure the energetic costs of fiddler crab claws in action by tracking changes in blood glucose (a sugar used to power activity) and blood lactate (a chemical by-product of metabolism and an indication of energy burned) as animals performed various behaviors. By measuring baseline lactate levels in resting animals, and comparing this to the elevated levels they detected during fights, Matsumasa and Murai showed that the energetic cost of waving a claw was substantial. M. Matsumasa and M. Murai, “Changes in Blood Glucose and Lactate Levels of Male Fiddler Crabs: Effects of Aggression and Claw Waving,” Animal Behaviour 69 (2005): 569–77.
14. Allen and Levinton, “Costs of Bearing a Sexually Selected Ornamental Weapon,” 154–61.
15. I. Valiela, D. F. Babiec, W. Atherton, S. Seitzinger, and C. Krebs, “Some Consequences of Sexual Dimorphism: Feeding in Male and Female Fiddler Crabs, Uca pugnax (Smith),” Biological Bulletin 147 (1974): 652–60.
16. H. E. Caravello and G. N. Cameron, “The Effects of Sexual Selection on the Foraging Behaviour of the Gulf Coast Fiddler Crab, Uca panacea,” Animal Behaviour 35 (1987): 1864–74.
17. T. Koga, P. R. Y. Backwell, J. H. Christy, M. Murai, and E. Kasuya, “Male-Biased Predation of a Fiddler Crab,” Animal Behaviour 62 (2007): 201–7.
18. M. E. Cummings, J. M. Jordão, T. W. Cronin, and R. F. Oliveira, “Visual Ecology of the Fiddler Crab, Uca tangeri: Effects of Sex, Viewer and Background on Conspicuousness,” Animal Behaviour 75 (2008): 175–88.
19. J. M. Jordão and R. F. Oliveira, “Sex Differences in Predator Evasion in the Fiddler Crab Uca tangeri (Decapoda: Ocypodidae),” Journal of Crustacean Biology 21 (2001): 948–53.
20. T. Koga et al., “Male-Biased Predation of a Fiddler Crab,” 201–7. Predation isn’t always male biased, however. For example, another study found that ibis preferred female fiddlers over males, perhaps because big claws made males harder to swallow. Keith Bildstein, Susan G. McDowell, and I. Lehr Brisbin, “Consequences of Sexual Dimorphism in Sand Fiddler Crabs, Uca pugilator: Differential Vulnerability to Avian Predation,” Animal Behaviour 37 (1989): 133–39.
21. A. G. McElligott and T. J. Hayden, “Lifetime Mating Success, Sexual Selection and Life History of Fallow Bucks (Dama dama),” Behavioral Ecology and Sociobiology 48 (2000): 203–10.
22. R. Moen, J. Pastor, and Y. Cohen, “A Spatially Explicit Model of Moose Foraging and Energetics,” Ecology 78 (1997): 505–21.
23. R. Moen and J. Pastor, “A Model to Predict Nutritional Requirements for Antler Growth in Moose,” Al
ces 34 (1998): 59–74.
24. A. Bubenik, “Evolution, Taxonomy, and Morphophysiology,” in Ecology and Management of the North American Moose, eds. A. W. Franzmann and C. C. Schwartz (University Press of Colorado, 2007): 77–123.
25. T. H. Clutton-Brock, “The Functions of Antlers,” Behaviour 79 (1982): 108–24.
26. R. Moen, J. Pastor, and Y. Cohen, “Antler Growth and Extinction of Irish Elk,” Evolutionary Ecology Research 1 (1999): 235–49.
8. Reliable Signals
1. All exaggerated “sexually selected” animal structures, including flashy ornaments of male displays and extreme male weapons, delay growth until relatively late in an animal’s development, shooting to full size after most or all of the rest of the body is already in place. For example, rapid claw growth in crabs begins at the final, puberty molt. R. G. Hartnoll, “Variations in Growth Pattern Between Some Secondary Sexual Characters in Crabs (Decapoda, Brachyura),” Crustaceana 27 (1974): 131–36; Pitchaimuthu Mariappan, Chellam Balasundaram, and Barbara Schmitz, “Decapod Crustacean Chelipeds: An Overview,” Journal of Bioscience 25 (2000): 301–13. Antler growth begins at puberty, as does narwhal tusk growth and walrus tusk growth. G. A. Lincoln, “Teeth, Horns and Antlers: The Weapons of Sex,” in Differences Between the Sexes, eds. R. V. Short and E. Balaban (Cambridge: Cambridge University Press, 1994): 131–58; H. B. Silverman and M. J. Dunbar, “Aggressive Tusk Use by the Narwhal (Monodon monoceros L.),” Nature 284 (1980): 57–58; Edward Miller, “Walrus Ethology. I. The Social Role of Tusks and Applications of Multidimensional Scaling,” Canadian Journal of Zoology 53 (1975): 590–613.
2. Although I don’t discuss this further in this book, females in many beetles, some decapods, and many of the armed dinosaurs, fish, and ungulates, also produce weapons. In virtually every case these female weapons are similar to, but smaller than, the corresponding structures of males. In the few studied examples, females use horns in fights with conspecific females, generally over food resources or to protect young. See, for example, N. Knowlton and B. D. Keller, “Symmetric Fights as a Measure of Escalation Potential in a Symbiotic, Territorial Snapping Shrimp,” Behavioral Ecology and Sociobiology 10 (1982): 289–92; J. Berger and C. Cunningham, “Phenotypic Alterations, Evolutionarily Significant Structures, and Rhino Conservation,” Conservation Biology 8 (1994): 833–40; and V. O. Ezenwa and A. E. Jolles, “Horns Honestly Advertise Parasite Infection in Male and Female African Buffalo,” Animal Behaviour 75 (2008): 2013–21. Two comparative studies explicitly tested for a role of sexual selection in the evolution of female weapons, and concluded that these structures most likely had been shaped by natural, rather than sexual selection. T. M. Caro, C. M. Graham, C. J. Stoner, and M. M. Flores, “Correlates of Horn and Antler Shape in Bovids and Cervids,” Behaviorial Ecology and Sociobiology 55 (2003): 32–41; J. Bro-Jørgensen, “The Intensity of Sexual Selection Predicts Weapon Size in Male Bovids,” Evolution 61 (2007) 1316–26. Several reviews have focused on this topic. See, for example, C. Packer, “Sexual Dimorphism: The Horns of African Antelopes,” Science 221 (1983): 1191–93; R. A. Kiltie, “Evolution and Function of Horns and Horn-Like Organs in Female Ungulates,” Biological Journal of the Linnean Society 24 (1985): 299–320; and S. C. Roberts, “The Evolution of Hornedness in Female Ruminants,” Behaviour 133 (1996): 399–442. But a great many taxa with female weapons have yet to be studied, and basic questions still linger. For example, under what circumstances do female weapons evolve? Do weapons arise in both sexes due to natural selection (for example, as a defense against predators) and then subsequently become co-opted as signals in males? Or do these weapons arise initially in males, and only in specific circumstances become co-opted by females?
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