© 2009 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured, or disseminated in any form without express written permission from the publisher. AALCOCK_CH06.inddLCOCK_CH06.indd 118282 11/9/09/9/09 111:11:011:11:01 AAMM 6 Behavioral Adaptations for Survival t is hard to pass on your genes when you are dead. Not sur- prisingly, therefore, most animals do their best to stay I alive long enough to reproduce. But surviving can be a challenge in most environments, which are swarming with deadly predators. You may remember that bats armed with sophisticated sonar systems roam the night sky hunt- ing for moths, katydids, lacewings, and praying mantises. During the day, these same insects are at grave risk of be- ing found, captured, and eaten by keen-eyed birds. Life is short for most moths, lacewings, and the like. Because predators are so good at fi nding food, they place their prey under intense selection pressure, favor- ing those individuals with attributes that postpone death until they have reproduced at least once. The hereditary life-lengthening traits of these survivors can then spread through their populations by natural selection—an out- come that creates reciprocal pressure on predators, favor- ing those individuals who manage to overcome their prey’s improved defenses. For example, the hearing abilities of certain moths and other night-fl ying insects may have led ▲ Canyon treefrogs rely on camoufl age to protect to the evolution of bats with unusually high- themselves from predators, frequency sonar that their prey cannot detect which means they must pick the right rocks to which they as easily.500, 1266 But now some night-fl ying cling tightly wthout moving. Photograph by the author. mantises do hear unusually high-frequency © 2009 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured, or disseminated in any form without express written permission from the publisher. AALCOCK_CH06.inddLCOCK_CH06.indd 118383 11/9/09/9/09 111:11:071:11:07 AAMM 184 CHAPTER 6 sounds, presumably as a counter to the innovative high-frequency sonar used by their hunters.325 The back and forths between predator and prey constitute evolutionary arms races. With this chapter, which looks at the results of this ongoing contest between the hunters and the hunted, the focus of the book shifts from the proximate to the ultimate causes of behavior. The main goals of the chapter are to establish what is meant by an adaptation and to show how one can use a cost–benefi t approach to produce hypotheses on the possible adaptive value of a behav- ioral trait while using the comparative method to test those hypotheses. Mobbing Behavior and the Evolution of Adaptations When I was in New Zealand some years ago, I visited a coastal nature reserve rich in wildlife. As I walked along the shore, I came to a place where hundreds of pairs of silver gulls had built their nests on the stony ground. While I was watching the gulls from a distance, a young researcher came down to the coast carrying a scale for weighing gull chicks and a clipboard for recording data. As she walked toward the colony, the gulls took notice, and soon those closest to her began to fl y up, calling raucously. By the time she came within a few meters of the fi rst nests, the colony was in an uproar, and many of the adult gulls were swooping about, some diving at the intruder, others yapping loudly (Figure 6.1). In gull colonies around the world, whenever a human, hawk, crow, or some other potential consumer of eggs or chicks comes close to nesting birds, the gulls usually react strongly. Among the masses of screaming gulls, some may launch what appear to be kamikaze attacks on the unwanted visitor. No one likes being hit on the head by a gull’s trailing foot as the bird pulls out of a wing-roaring dive; nor do visitors to gull rookeries enjoy being splattered by liquid excrement released by agitated gulls fl ying overhead. FIGURE 6.1 Mobbing behavior of colonial, ground-nesting gulls. Silver gulls reacting to a trespasser in their breeding colony in New Zealand. Photo- graph by the author. © 2009 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured, or disseminated in any form without express written permission from the publisher. AALCOCK_CH06.inddLCOCK_CH06.indd 118484 11/9/09/9/09 111:11:071:11:07 AAMM Behavioral Adaptations for Survival 185 FIGURE 6.2 A nesting colony of black-headed gulls. We can easily guess why the gulls become upset when potential predators get close to their nests. The parents’ assaults probably keep hungry intrud- ers away from their youngsters, helping them survive. If so, then mobbing by gulls could increase their reproductive success, passing on the hereditary basis for joining other gulls in screaming at, defecating on, and hitting those who might eat their eggs and youngsters. Indeed, this hypothesis was the one that quickly came to mind when Hans Kruuk, a student of Niko Tin- bergen, decided to investigate mobbing behavior in the black-headed gull, another ground-nesting, colony-forming species (Figure 6.2) but one that lives in Europe rather than New Zealand.814 Kruuk was interested in studying the evolutionary, ultimate causes of mob- bing, not the proximate ones, which would have required examination of the genetic, developmental, hormonal, and neural bases of the behavior—all inter- esting and valuable subjects but not on Kruuk’s agenda. To get at the evolu- tionary foundation of the behavior, Kruuk employed what is now called the adaptationist approach. In effect, he wanted to know whether the mobbing response of black-headed gulls was an adaptive product of natural selection. His working hypothesis was that mobbing behavior distracted certain preda- tors, reducing the chance that they would fi nd the mobbers’ offspring, which would boost the fi tness of mobbing parent gulls. Kruuk used his hypothesis to make testable predictions about gull mob- bing behavior.814 He knew that natural selection occurs when individuals vary in their hereditary attributes in ways that affect how many surviving offspring they contribute to the next generation (see Chapter 1). Imagine a population of gulls, some of whose members mob nest predators while others do not. This population will surely evolve if the difference between the two types of individuals is hereditary and if one type consistently leaves more surviving progeny than the other. If, for example, the mobbing phenotype out- reproduces the non-mobbing type generation after generation, then mobbing behavior will eventually become the norm, and non-mobbing will disappear (always assuming that the differences between the two types are hereditary). Thereafter, any hereditary change in the nature of the mobbing response that enhances individual success in passing on genes will also spread through the species, given enough time. © 2009 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured, or disseminated in any form without express written permission from the publisher. AALCOCK_CH06.inddLCOCK_CH06.indd 118585 11/9/09/9/09 111:11:121:11:12 AAMM 186 CHAPTER 6 TABLE 6.1 Constraints on adaptive perfection CONSTRAINT 1: Failure of appropriate mutations to occur Evolutionary constraints on adaptive perfection can arise from the failure of appropriate mutations to occur, which will prevent selection from keeping up with environmental change. Thus, maladaptive or nonadaptive traits can persist, especially in environments only recently invaded by a species. So, for example, some arctic moths live in regions where bats are absent, but the moths still cease fl ying in response to an ultrasonic stimulus.1265 Likewise, arctic ground squirrels react defensively upon experimental exposure to snakes, even though there are no snakes living in the Arctic.301 Man-made changes in the environment are especially likely to lead to inappropriate expression of previously adaptive traits.1286 Thus, some moths are so strongly attracted to artifi cial lights that bats visit lights in order to make some easy kills.503 Likewise, male buprestid beetles (see Figure 4.8) may die while persistently attempting to mate with beer bottles,599 while sea turtles sometimes expire after consuming plastic bags that they mistake for edible jellyfi sh.205, 831 The current obesity epidemic in Western societies may well be caused in part by the once adaptive desire of humans to consume calorie-rich foods in an “unnatural” modern environment where it is entirely possible to eat too much of a good thing.1010 CONSTRAINT 2: Pleiotropy Developmental constraints on adaptive perfection can occur as a result of pleiotropy (the multiple developmental effects that most genes have). Not all the effects of a given gene are positive. If the negative consequences of a gene outweigh the positive ones, the gene will be selected against. The converse is that because some gene effects are so valuable, the less signifi cant, mildly negative consequences of an otherwise adaptive proximate mechanism may be maintained in the population by selection. For example, misdirected parental care is not uncommon in nature, a result of the intense drive to care for offspring, which usually is adaptive but in relatively rare instances can lead an adult to provide assistance to a youngster of a genetic stranger (see also Figure 14.5).638 CONSTRAINT 3: Coevolution Coevolution (the kind of evolution that occurs when different species interact in ways that affect the fi tness of each other’s members) means that evolutionary stability may never be reached. Instead, each species changes in response to selection pressure imposed by the other, so fi rst one and then the other species gains the upper hand, as in the coevolutionary arms races between predator and prey.