L20-Alcock_Ch_13 - -a - —.--‘,-1—-,'w Weaver ants...

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Unformatted text preview: -a - —.--‘,-1—-,'w Weaver ants form superbiy cooperative societies based on a sterile worker caste. One of the many products of their altruism is a magnificent leaf nest woven together with silk provided by the coiony’s iarvae. Photograph by the author 1 The Evolution , of 5 acid] BehaviOr on’t reach for the Raid "the next time you find a paper wasp colony under an eave on your house {see Figure 3.10). The wasps will not sting you, provided you approach the nest careful- ly—and l have noticed that most people do not need too much encour— agement to be cautious around wasps. But if you overcome your fear of these insectsl am confident you will be fascinated by their behavior. In this opinion ljoin the great evolutionary biologist W. D. Hamilton, whose work is featured prominently in this chapter. l---~lan‘ti|tr.>n had this to say about paper wasps {503}: Social wasps are among the least loved of ii“:sects Yet, where sta- tistics will not alter a general impression, another approach migl'rt. Every schoolchild, perhaps as part of religious training, oug ht to Sli. watching a Polistes wasp nest forjust an hour I think few wili be unaffected by what, they see. It is a world human in Its seeming motivations and activities far beyond all that seems reasonable to expect. from an insect: constructive activity, duty, rebellion, mother care, violence, cheating, cowardice, unity in the face of a threat—all these are there. The quasi—human melodramas that take place at a paper wasp nest involve a community of females both competing and cooperating as they '3- C} __) {,1- Chapter '13 rear the eggs and grubs that. occupy the cells. of the nest. If I \N’Clic to tell _vou llint only one of the several females at the nest might be the mother of all the egg, and grubs hi’)userl there, and that these }-'oongsters l-‘k‘rttl'tf being regularly to; with food collected by females other than their mother, I hope you i.i,-'oL1ld lt-i at least. mild 1y surprised. Although parental care can evolve by; natural selec-- tion when the benefits of the behavior exceed its costs, as we saw in the prev-j“ ous chapter, it is hard to imagine liOt-‘x-" an a d ult’s fitness could be increased tn;- behaving parentally toward 8011100110.QlSQ’S}.-'(')L11“ig5%t01‘5. Yet helpers at nests a n;- found not just in paper iwasps, but in a host of other insects, as l-‘V’Cll as in some birds and mammals. 'I‘hese self-sacrificing individuals pose a i-i-‘onderful Dar-- Winian puzzle 'W hose solution has engaged some of the best evolutiomlr}: biol- ogists in the world, including W. D. l lamilton and Charles Dari-tin himself. This chapter focuses on how altruism and other helpful acts of social organ - isms can be analwcd from an adaptatii‘mist perspective. But first we must asi. a more basic question: Why do any animals live in groups instead of leading solitary lives? The Costs and Benefits of Social Lfe You may think that the reason so many animals live with others of their species is that social creatures are higher up the evolutionary scale, and so better adapted. than anin’ials that live solitary lives. You might hold this belief beca use you know that humans a re highly social, and you i-vould like to think that we, and perhaps a few other higth social species, represent the crowning achieve ments of the evolutionary process. Bi ll' if you believed these things, you would be mistaken, because natural selection does not aim for preset endpoints (sec Cl'iapter '1). Instead, in each and every species, generation after generation, rel- ativer social and relativer solitary types compete unconsciously with one another in ways that determine who leaves more offspring on. average. In some species, the more social individuals have won out, but in a large I'najority, it is the. solitary types that have consistently left more surviving descendants on a v e ra go. But. hot-v can living alone ever be superior to living together? Under some conditions, the cost—benefit equation for solitary life is better than that for a more social existence (Table '13.'l). For example, in most social species, animals have to expend time and energy jockeying for social status. Those that do not occupy the top positions regularhi have to signal their submissive state to their supe— TABLE 13.1 Some potential costs and benefits ofsociai living Costs ~..—- Greater conspicuousness of clumped individuals to predators Greater transmission Ul: Llif‘iL‘tiSL’ ilIlCl parasites among group members More competition for food among group K. members Time and energy expended by subordinates in dealing with more dominant companions Greater male vulnerability to cuckold r}! _,_, Benefits —v~._-———.‘w~ _——_ .-_ _ ,.. s” ___——— _.. l'Jel-ense against predators via the dilution effect or via mutual defense (see Chapter (ii) Oppm'tunilies to receive assistance from others in dealing i-vi th pathogens lm proved foraging via the information center effect (see Chapter 7) Sobordinal‘es are granted permission to remain safely within the group Opportunity for some nodes to cuckold others Greater female vulnerability to egg tossing, Opportunity to toss the eggs of others, dump eggs in others' nests, and interlere With the reproduction of competitors egg dumping, and other forms of reproductive interference by companions {A} l-lelpers -f "——u‘" ' m. "'_— 'hociai Ci Agonistic behavior ' behaviors l:- SuhmissiVe behavior Direct 1] live cleaning lil'tmcl Cd re T , Cl Substrate cleaning, erritorv . . ‘ , . ' Ci Digging j maintenance LB (1"ch . -, it i riors if thefty are to be. permitted to remain in the group. All the ktm’towing can take up a major share. of a social subordinate’s life (Fig— ure 15H) [H78]. in fact, even small social groups are rife t-vith subtle and not-so-subtle competition, as we shall document in the. pa ges ahead. in an African cichlid fish knots-n for its cooperatix-‘e breeding, helpers live with a breeding pair within the group’s communal territory. In Figu re 13.2, the locations occupied by five of these helpers are sl'iown over a 3-day period; on day 3, the largest helper ( 1) was re— moved by researchers but its territory outline remains in the figure [1271]. l-iow would you interpret these data in light of the possibility that helpers a re competing?r with one another while helpingr a breeding pair? What benefit might helpers derive. from achieving domi» nance over other helpers? Figure 13.2 Effect of removal of the top— ranked subordinate helper in a c00peratively breeding group of cichlid fish {Neoiomproiogus brichordi).The removal occurred on day 3 in an aquarium that housed a breeding pair and five helpers. (The different colored dots represent the different fish and show where these individuals were seen on a given day.) After Werner et al. [1 271}. The Evolution of Social Behavior 439 Figure 13.1 The energy budget of subordinate, nonbreeding "helpers" that associate with breeding pairs in the cichlid fish Neolomprobgus puicher. (A) The largest proportion of the subordinate fish's energy is expended on the performance of submissive behaviors—specifically, a tail—quivering display. Most of the remainder of the subOrdinate fish's energy budget is spent attacking intruders and removing sand and debris from the area defended by the breeding pair and their helpers. {8) A subordinate helper quivers his tail as the dominant fish approaches from be- hind/3i, afterTaborsky and Grantner [i 178]; 8, photograph by MichaelTaborsky. z} ’ « ' .:' 2.4. - I r ' I: _¢" ( i ’/l ,~'/‘,/.~ f... xP. ., ‘3.“113"'( .. '/,“..-'$" #,. ,.- ./ “ 51.j4q, ,A‘ c ‘ (:__rl_',-.fi,_...w. / ‘_.%n t" 'v v? 7,; ‘1'?! 5”? of, . ' I " ' é£.'-:': '- fa ' ' - ' - ‘_ _ ---\ \. ' ' . .-.-i *-.~."-‘~.‘-.. ' \' __ l' V :2": _ .-- x \' x ‘ H \q‘lzgf‘f-f‘} ‘ ' .-t.- kin: <_ “a; "- \\ ' \ . u... .:‘. I - x 'q -" - .I‘. I - . ’ - "-- i ' I“? '1 HJ‘ -' fJH- Um,- ] .VttifiMJHt hurts t iitftriim ._ . .. ’3 .) l , . r 4 ,s -«w ".l . ,_-I-" I A( I __.o"‘ i-P q -: .I I“ Find-"'- d P / \ J _.a-"’" ‘l / r} \ I .. ‘u 0 , \ ~., appr- '-FF .— E/ ’ 0 o a a l <35 c ’3“ ’9 In I V “ha 0 5' /’ ' e a a I _ -.____~ ' / {m u (7 a. _ ‘-¢_‘_ (I. ,1 R“ ' xh. f‘ _9__s .. _ 1L5“ baa“ _9__ w__._4bf L-_— — _ __ ____ _.‘_ _ .-__. F) Dat - 440 Chapter 13 Social groups also offer o}.'i,-;‘iorlLsnities for reproductiye interlerei'ice. Bree: ing males that like in close association with more i-ittractn'e rivals ma y lose thee- mates to these individuals. Breeding females may i-rind lip incubating 0:43;}; dumped in their nest by brood parasites of their own species [Fuss 838]. Sn; h costly reproductive penalties come with social living in the acorn wotidpeclai, a bird that fOi‘ITIS breeding groups containing as many as three females and four males. The several females all la y their eggs in the same tree hole nest, per. haps because any female that tried to keep a nest to herself i-‘VULllCl ha we all her eggs destroyed by her i-‘indictiy e companions [(755]. Even when sew-“eral fen'iales agree to use the same nest, the first eggs laid are almost alt-rays removed by another female member of the group ( Fi gu re 'l3.3) [860]. Exi’entually these "coop— eratively breeding” females all lay eggs on the same day, at which time they finally stop tossing one another ’s eggs out and incubate the clutch. By this time, hOt-VBV’QI‘, more than a third of the eggs laid by the woodpeckers may have been destroyed. Having your eggs tossed is an unad ultera ted cost of social living for females of this species. In addition to these direct r iprod uctive costs, sociality has two other poten- Figure 13.3 Reproductive i nterfer— tial disadvantages. The. first is heightened competition for food, which occurs enCe in a SOCial animal. One member in animals as different as colonial fieldfares (Figure TIC-3.4) [1302] and prides on” Of a breedan group Of 503"” WOOd DQCk' lions, i-ehose females are often pushed from their kills by hungry males ll [loo]. :2: :EyfiiiSSZZSrggcfgfnn;$2133: 12:2? The second is increased vulnerability to parasites and. pathogens, which plague graph courtesy Of Walt Koemg' soc1al species of all sorts [l 6} (but see [1033]). The fact that some. socral animals have evolved special responses to these enemies may enable those animals to reduce the damage they cause, but cannot totally eliminate the burden they impose. 'l'hus, honey bees warm their hives in response to an infestation by a fungal pathogen, which apparently helps kill. the heat-sensitive fungus, but at the price of time and energy expended by the heat—prod ucing workers ll 1 49!. Similarly, termites can reduce the lethal effect of a different fungal im-‘ader in their nest mounds because unexposed colony members can acquire some i mm u— nity to the fungus simply by associating i-vith others of their group that hare already developed an immune response to the pathogen [1210]. Even so, the existence of special responses to fungal infection speaks to the high probabil ity that a colony will become infected, perhaps because it offers such a large tar— get. Moreover, the antifungal mecl'ianisms tl’iemselves do not come for free, but require physiological espenditu res on the part of the termites. If social living carries a heightened risk of infection by parasites or pathogens, then the larger the. group, the greater the risk. This prediction holds for cliff swalloi-rs, which pack their nests side by side in colonies composed of t1I1}-’\-\~’l‘l€l”tt from a handful of birds to several thousand pairs. The more swallows nesting together, the greater the chance that at least one bird will be infested with swal— low bugs, which can then read iiy spread from one nest to another. (f ha rles l "7'3; x 1' {"- (.- liar-Kns W l c? 1 6‘33'W-q.‘ a Q “I E U by 5‘9 h na‘finqh “a Q’ 0 S lth‘ t» 3' ,.. h — — . ' . :f. o " r: Flgure 13.4 Competition for food 30 L is a cost of sociality in the fieldfare, a é ll 1 I songbird that nests in loose colonies in ‘ woodlands.The larger the colony, the , . ' [l-Ti . . Fieldiare lower the survwal rate of nestlings, clue . to increased juvenile mortality caused [i largely by starvation. After Wiklund and ‘ h m ‘4 “l” Andersson [1302]. Colony sine set»; L.‘ 0 r. .Lf- [- its The Evolution of Social Behavior Figure 1.3.5 Effect of parasites on cliff swal- low nestiings. The much larger nestling on the right came from an insecticide—treated nest; the stunted baby of the same age on the left occupied a nest infested with swallow bugs. From lirovvn and Brown [155']. and Mary Brown found that nestlings in large colonies vx-rere heavily assaulted by blood-sucking, growth—stunting swallow bugs [155]. The Browns demon— strated that the bugs were guilty of harming the nestlings by fumigating a sam~ ple of nests in an infested colony while leaving other control nests untreated. The nestlings doused with insecticide weighed much more, and ‘WCI‘Q more likely to survive, than those plagued by parasites (Figure 13.5). The parasites and fungi that make life miserable for swallows and other social creatures demonstrate that if sociality is to evolve, the assorted costs of living together must be outr-veighed by compensatory benefits. Cliff swallows m a): join others to take advantage of the improved foraging that comes from follow— ing companions to good feeding sites (see Chapter 7) ['l 56, 473], i-vhile other a ni— mals, such as egg-b roodin g male emperor penguins, save thermal energy by huddling shot:Icler—to—shoulder cl tiring the brutal Antarctic its-Pinter [25]. Still oth— ers, such as lionesses, join forces to fend off enemies of their own species, includ- ing infanticidal males [l'l52]. The most widespread fitness benefit for social animals, however, probany is improved protection against predators (Figure 13.6) [16]. Many studies have Figure 13.6 Sociat living with defensive benefits? The members of this dense school of small [5 cm long} striped catfish living on a coral reef near Sulawesi have almost certainly joined forces to improve their chances of sur— vival. Schooling in this and other species can enhance the survival of individual fish either by intimidating some preda- tors through the collective size ofthe massed school or by amplifying their defenses, if the fish are protected by spines or chemical repellents. Photograph by Roger Steene. Figure 13.7 Mutual defense in a society of bluegills. Each colonial male defends a territory bordered by the nest sites of other males, while bass (above), bullhead catfish (left), snails,and pump- kinseed sunfish (right foreground) roam the colony in search of eggs. Drawing Courtesy of Mart Gross. shown that animals in groups gain by diluting the risk of being captured, or by Spotting danger sooner, or by ganging up on their enemies (see Chapter (5). Thus, in the ma oinao, a reef fish with a wonderful Latin name (/ll?!liftffifilfriflt'ftiiI!lliriffS), individual males in large nesting groups chase other egg—eating fish only about one~fourth as often as males in small nesting aggregations. And when a nest- defending male. is reintwed from a small group, his eggs are attacked by a pred- ator sooner than the eggs of a male removed from a large group, indicating that maomao males definitely derive mutual antipredator benefits by nesting together ['1 220 I. Males in nesting colonies of the bluegill sunfish also cooperate. in driving egg-ea ti ng bullhea d catfish away from their nests at the bottom of a freshwater lake (Figure 13.7) [485]. lfthe social lK‘l’taVlOT of the bluegill has indeed e\-':.il\-'et.'i in response to predation, then closely related species that nest alone should suf— fer less from predation. As predicted, the solitary pumpkinseed sunfish, a mem— ber of the same genus as the bluegill, has powerful biting jaws and so can repel eggweating enemies on its own, whereas bluegi lls have small, delicate mouths good only for inhaling small, soft-bodied insect larvae [485]. l’l_11npl<in--- seed sunfish are in no way inferior to or less well adapted than bl uegills because they are solitary; they simply gain less through social living, which makes solitary nesting the adaptive tactic for them. The Evolution of Helpful Behavior Animals that live together have the. potential to assist one another, and they often do, as maomao and bluegill males demonstrate. Until the mid—'l 960s, biol— ogists took helpful behavior of this sort more or less for granted because they assumed that animals should help one another for the benefit of the species as a whole. But iii-then George C. Williams pointed out the defects of this assump— tion (see p. 19), helpful actions, especially altruistic ones, suddenly became more interesting to evolutionary biologists. The Evolution of Social Behtniioi 4217-3- TABLE 1 3.2 The direct reproductive success of individuals that engage in different kinds of social interactions Effect on direct reproductive success of —'—'_nI-R—l——— Type of interaction Social donor , Social recipient Mutualism (Cooperalion) + Reciprocity + ldClflfl‘dl 4' Altruism — + Selfish behavior 4- — Spiteful behavior” _ "You should not he surprised that spiteful behavior is almost never observed in nature; you should be surprised that altruism is not uncommrm despite the loss of reproductive success experienced by altruists. There. are a number of ways in which animals can behave toward one another in social interactions, which have. different payoffs for the donor and the recip- ient of the behavior (Table 13.2, Figure 13.8). l-{elping sometimes generates immediate returns for both parties, in which case they are. said to be engaged in a mutualism. When one lioness drives a u-‘ildebeest into a lethal ambush set by her fellow pride members [1145], the cooperative driver will usually get some. meat, even if she did not personally pull the antelope down and strangle it her- self. Likewise, if several male bluegills succeed in fending off a bu llhead catfish that has entered their part of. the nesting colony, the eggs in all. the males” nests are more likely to survive to hatch. When both helper and recipient enjoy repro- ductive gains from their interaction, their mutualism, or cooperation, requires no special evolutionary explanation. This is not to say that mutualism is uninteresting. Consider the coalitions of male lions that form to oust rival males living with a pride of females. When cooperating males are successful, they may gain sexual access to a large group of receptive females. When Craig Packet and his associates analyzed lion coali- Mutualism film red gain of direct fitness Exa m pie: Prey capture by lion pride 3 Reciprocity -<—-- --------- ——— l l]fil._.l’i{l{ —-——--->— Obligate altruism Delayed gain of direct fitness Permanent loss of direct fitness (dependent upon repayment) [with potential for indirect lixample: Vampire bat blood fitness gain} exchanges Example: Honey bee workers foraging for colonv Facultative altruism 'l‘empora rig loss of direct fitness (with potential for indirect fitness gain followed by personal reproduction} lixainple: lilorida scrub jay helping at the nest, then gaining parental territory Figure 13.8 The different categories of helping behavior. Cooperative helpers can be placed into four groups based on the fitness consequences of their actions. Wfimkfl—A..wMWWH‘,MAg-Mm 444 Chapter i3 Number of males Figure 13.9 Cooperation among competitors. Yearling male lazuli buntings range in color from dull brown— ish to bright blue and orange. (Their plumage scores range from less than 16 to more than 32.) Bright yearling males permit dull males, but not males of inter- mediate brightness, to settle on territo- ries neighboring their own. As a result, brownish males often pair off with females in their first year whereas year- ling males of intermediate plumage typi- cally remain unpaired. After Greene et al. [474]; photographs courtesy of Erick Greene. Paired i (i 20 24 2 * s tions, they found that partnerships of two or three males shared access to the females fairly evenly [918]. Even so, some males in these groups do not do as well as others. Why do the disadvantaged males tolerate their situation? Prob-- ably because they could do no better alone. If they went solo, their chance of acquiring and defending a pride would be next to zero because one male has little chance against two or three rivals. Thu s, some males may be forced to coop~ erate with domineering companions if they are to have any chance of ma ting [(553 . Likewise, subordinate yearling male lazuli buntings, which have dull brmvn plumage, engage in an interesting mutualism with brightly colored, dominant yearling males (Figure "13.9). The bright males aggressively drive other males with bright or intermediate plumage away from top-quality territories with good. shrub cover, but they tolerate the presence of dull-pl umaged males. These lm-x-'—ranking individuals are permitted to claim territories in good habitat right next to their brightly colored companions. One hypothesis for the bright ma les’ surprising acceptance of their brownish neighbors is that bright males a re unlikely to lose paternity to such neighbors, which lack the attributes that make females eager to engage in extra~pair copulations. If this hypothesis is true, then brightly colored males should not be cuckolded as often as duller ones. In keep— in g with this prediction, in the nests sampled by Erick Greene and his cowork— ers, bright males lost paternity on average at half the rate of their dull neigh- bors. The more frequently victimized duller buntings usually cared for belt-veen one and tree extra-pair young, which were probably the genetic offspring of their brightly plumaged next-door neighbors [474]. Given the costs of trying to raise a family next to dominant male lazuli buntings, why do dull males accept the offer to live near them? Perhaps because the subordinate buntings at least get to hold high—quality territories, which enables them to acquire a social mate more often than males of intermediate plumage brightness. Those iii—between males are often pushed by dominant .h- . —w-m ' ~m=m~ - ~ humu— «u. «sauna—w“. syn-Au.-. xd-hlwmatwflZMéWHWx-fluanm " ‘ u'L-mh-l-hf-nwoélfit'L-Lu u-Mk-L-BWL- 4s“:—F¢L%MA ‘ an" The liveluiir-n of Social F:eira~..-'irii 5-3-43 rivals into habitat so poor that no fen'i ale will join them. .«fxltl‘iough drab firear— ling males one}! often rear the chicks of other males, they also produce somr- of their own on occasion, achieving a modest amount of reproductive success, unlike most yearlings of intermediate plumage and in-betx-veen social status, which have to wait another full year to breed [474] n I Given the differences in reproductive success for the three categories of male lazuli buntin gs, how cm we account for the evolutionary persistence of males with d Llll and, especially, intermediate plumage? The fact that both dull and bright yearling neigl'ibors gain some fitness from their interaction means that their social arrangement constitutes a miitualism. But i-vhat about the male. coalitions of the longtailed manakin studied by David McDonald, in which only one of two cooperat.i\-'e males appears to reproduce? in this bird, males form pairs and sing loud duets over and over to attract females to a display court [40'l , 8055]. Visiting females land on the pair’s display Perch, often a horizontal section of liana that lies a foot or so above the ground. In r *sponse, the two males dart in and land close to the prospective mate before. performing an astonishing cartw heel display (Figure HMO). After a series of these moves, the males ma y perform the "butterfly flight,” in which they flut- ter slowly back and forth in front of the female, displaying their beautiful plumage and coordinated tli ght ca pacity. Should a female ViSll‘OT start jumping excitedly on the perch in response to these displays, one member of the duo dis— creetly lea ves, while the remaining male stays to copulate with her. The female then flies off, after which the mated male calls for his display partner, who be r— ries back to resume his duties. BY markingT the males at display perches, McDonald and his ma na kin I'V‘cllfll' ers found that each site. has on! one mating male. This alpha manakin may Figure 13.10 Cooperative courtship of the long-tailed manakin. The two males are in the cartwheeling portion of their dual display to a female, who is perched on the vine to the right. lief-fl t". l'. a p 1', er 'I Is "° w r .- -. ' l r' _. - figure tit l Cooperationwrthai eventual payorf. After-the I] death of his alpha male partner, the beta male long tailed rnariakil‘: (now an alpha) copulates about as frequently as his predecessor did, presumably because the females attracted to the duo in the past continue to visit the display arena when receptive. After McDonald u. I53 - and Ports [808']. :5 E; c are E ‘ e E [U35 3 t) “g? 9 :3 U __L.. -.___|___. —l ...... __ _.5 {it}? [ill] [1.15 LIQI'; Previous alpha male: copulations per hour have several display companions, but not one of them gets to reproduce, not even the alpha’s favorite colleague, a beta male, who in turn is dominant to any other part—time cooperators [808]. How can it be adaptive for the subordinates to work so hard. on behalf of the sexually monopolistic alpha male? By patiently following males }-’eai‘ after year, Mc Donald established that i-vhenever an alpha male disappeared, the beta male took over, after which a lower—ranking indi ridual moved up to become the net-v alpha’s main nonbreeding display part ner, Thertj‘fore, by cooperating with the alpha male, a beta individual esta blishes his claim to be next. in line, keeping other (probably }-’ounger) birds at bay for yous. When a beta ma le becomes an alpha, he usually gets to mate with ma n y of the same females that copula ted lit-“tth the preritms alpha (Figu re 1311 '1) ['Stlb’l. thus, beta males form a mutualism with their exclusionary partners because this is the only way to join a queue to become a reproducing alpha male—«eren tualh'. In set-"eral ant species, tut-o or more unrelated females may join forces to found a colony after they ha re mated. The. females ma y cooperate in digging the nest and prod ucin g the first Lgeneration oft-vorkers, but then the}? start fighting until orin one is left alive [93]. How can it pay to join such an association? ‘Nhat predic— tion can you make about the survival rates and a verage prtiductit-'it}-’ of colonies founded by a single female? Under what conditions W’Otllc‘l it be accurate to call this social system a mutualism? Uta-'elop at least one cost—benefit hypothesis to account for the timing of the switch from cooperation to aggressive behavior. If the beharior of the two queens is the product of natural selection, not group selection, what pre- diction can you ma ke about the interactions between them during the colony estab - lisl'iment phase prior to the fightsto—the-dealh phase? The Reciprocity Hypothesis The stud y of long—tailed manakins shows us that some superficially self—sacri— ficing actions actual I}! a d trance. the reproducti ce chances of helpful individuals. Another possible case of this sort irn'oh-'es the meerka t, a small African mam— mal that forages in groups. From time to time, one meerkat will stop digging for insects in the soil and climb a tree or a termite mound to look around for approacl'iing predators [Figu re '13.'l '2) [226]. Should a goshawk come swooping The Evolution of Social Behavior 44? in, the elevated sentinel is usually the first to give an alarm, which sends all the still—imaging meerkats dashing for cover. One explanation for this behavior is that sentinels help others at personal cost now because they will be repaid later by their team mates when they take their turns at being lookou ts. Bob— "lrivers called this kind of social relationship “recip- rocal altruism” (it is also known as reciprocity) because helped individuals eventually return the fax-tors they receive ['l2'll[. If the initial cost of help- ing is modest, but the benefit from receiving the returned favor is great, then selection can favor mak ing the initial gesture. Imagine, for example, that a meerkat lookout has a 2 percent Chance of being killed for every 100 hours spent scanning for enemies. But imagine that for every hour he spends on his perch, another companion will pay him back. If hav- ing others keep an eye open for danger for '1 00 hours improves the helpful lookou t’s chance of survival by any amount more than 2 percent, then the benefit is greater than the cost, and reciprocity can spread through a population. However, consider an alternative explanation for sentinel behavior. Perhaps the lookouts are sated and ‘ t ' {I J - 5...: "’2 T". f“... " _ "-4,- 41. '.-‘__ .' £1; .,' -'_~ - ‘ . . 'Aifi‘... do not need to forage for food, so they climb a tree in -- - ‘ ~ ' - -- ' - -~ ' ~- order to better spot danger to themselves. Rather than F 13 1 k . I - - - . x - I . eer a offering costlv assistance to others in their band, the gum 2 A m t semme 0” the alert for approaching predators. "sentinels" could be securing personal fitness benefits, especially if an approach— Photograph by Nigel J Dennis ing goshawk is likely tothase one of the lookout’s fleeing companions rather than the alert sentinel. (l\‘ote that this argument requires that the sated meerkats be safer on a lookout perch than in a burroi-v. N’loretnfer, the sentinel must be less li ker to be attacked if its com pan ions are running for cover than if they are not. Finally, this hypothesis also requires that the signaler’s companions gain more by dashing for a burrow than by remaining frozen in place in an effort to avoid detection by the onrushing predator.) How can we test the reciprocity hypothesis against the personal safety alter— native? The reciprocity hypothesis predicts that meerkats should follow a reg— ular rotation of sentinel duty and that sentiriels should run some risk of pre— dation. However, in reality, sentinel duty is established lurphazardly, and lookou ts a re usually closer to an escape burrow than are their fellova, suggest— ing that lookou ts do not put themselves in special danger. The personal safety l‘iypothes‘is also receives support from the finding that solitary meerkats spend about the same proportion of each day in sentinel behavior as do the members of a band. [\xloreover, when meerkats are given supplemental food, which reduces the cost of takii'ig time out to look around for predators, they increase the amount of ti me spent on a lookout perch. Thus, what initially appears to be a rotation of lookouts may actually be the product of individuals spending as much time as possible during the day in a relatively safe position [226]. l l i l l l I .-o.._..' mid—d. _._..‘,..,. l i This is not to say that reciprocity is absent from nature [915, 1304]. In many i . - . . . v . . ’ i primates, for example, individuals spend considerable. tune carefully groom— in g the fur of a companion (Figure '13.]3). The groomer helps the groomee by .AJ'. ,. renuivin g parasites and debris, but gains no immediate benefit from its actions, cashing in only when the animal it helped returns the favor. In bands of baboons, pairs of females do take turns grooming and being groomed, as predicted by the reciprocity hypothesis [1109]. r.“ «IQ-u— ah-d—M—n-N-4m' '. 4-48 Chapter 13 Figure 13.13 Reciprocity in a social primate. A vervet monkey grooms a companionThe groomee will return the favor at a later date. Photograph by Dorothy Cl'ieney. Figure 13.14 Experimental demon- stration of reciprocity in cotton—top tamarins. (A) A double-compartmented cage with a pull tool that one cotton—top subject (the actor, on the right) could use to drag food down the tray toward its companion [on the left, reaching for a food reward). (B) The proportion of trials during which a cotton-top reciprocated by pulling food to a helpful companion [which had been trained to always pull a food item within reach of the other mon— key) and an unhelpful companion {which had been trained never to pull a food item within reach of another individual}. A, photograph courtesy of Marc Hauser; B, after Hauser et al. [522]. The capacity for reciprocity also appears to exist in another primate, the cotton—top tamarin, as Marc Hauser and his fellow researchers demtmstrateti experimentally in the tollot-ving way [522]. They constructed a special cage will 1 separate compartments for each of two monkeys (Figure 1314), one of wl'ioru had access to a pull bar that could be used to d rag food to within reach of either-- the puller or his companion (dependingr on the placement of the food item in; a researcher). The question was, would a cotton—top repay a puller that used thn. - tool to delix-er food to it? Hauser and company conditioned one monkey lll always pull the food within reach of a companion. This invariant puller was then paired with a genetically unrelated individual, which we shall call the actor The actor and the trained altruist were given opportunities to take turns pullin 1e food for each other over 24 test trials. 'l‘he actor repaid the trained—to—pull—every time companion somewhere between a third and a half of the time, much more so than when the actor was paired with a. “detector” mon key that had been trained meter to use the pull tool to deliver food to at ca gemate. in other words, {13) ll] - Cl Helpful companion o [1.8 " Cl Unhelpful companion 3-7:? 3.: llh ,1 1) E >1 : 3 i t: : L].;’]' I g n. '5 oz "4 to Q.) 4.. Session The Evolution of ."_-,:r.,ir;i;-il elm-with" 19-5533: when paired with an a pparentl}.r helpful companion, cotton—tops reciprocated, but when given an opportunity to assist an unhelpful companion, the tam arins withheld their assistance. Although at least some primates appear to have the ca pacitv for reciprocii}.~’, the behavior is not particularly common among animals generally, perl'iaps because a population composed of reciprocal altruists would be vulnerable to invasion by individuals who accept help but then forget about the payback. “Defectors” reduce the fitness of “helpers” in such a system, which ought to make reciprocity less likely to evolve. The problem can be illustrated with a game theory model called the prisoner’s dilemma (Figure 13.15), which is based on a human situation (see also Figure. 6.33). Imagine that a crime has been com- mitted by two persons who agreed not to squeal on each other if caught. The police have brought them in for interrogation and have put them in separate rooms. The cops have enough evidence to convict them both on lesser charges, but need to have the criminals implicate each other in order to jail them for a more serious crime. They therefore offer each suspect freedom ifhe. will squeal on his pal. lf suspect A accepts the. offer (“Defect”) while B maintains their agreed—upon story (“Cooperate”), A gets his freedom (the maximum reward) while 8 gets hit with the maximum punishment—say, '1 0 years in prison (the “sucker’s payoff”). lf together they maintain their agreement ("CoOperate + Cooperate”), then the police will have to settle for com-'iction of both on the lesser charge, leading to, say, a 'l-year prison term for each suspect. And if each one fingers the other, the police will use. this evidence against both and renege on their offer of freedom for the snitch, so that both A and B will be punished quite severely with, say, a 5-year prison sentence each. In a setting in which the payoffs for the. various responses are ranked “Defect while other plaver cooperates" 12> "Both cooperate” 2» “Both defect” r» "Coop— crate while other player detects,” the optimal response for suspect A is always to defect, never to cooperate. Under these circumstances, if suspect l?) maintains their joint innocence, A gets a payoff that exceeds the reward he could achieve by cooperating with a cooperative B; if suspect B squeals on A, defection is still the superior tactic for A, because he suffers less punishment when both players defect than if he cooperates while his companimi squeals on him. By the same token, suspect B will always come out ahead, on average, it he defects and points the finger at his buddy. This model predicts, therefore, that reciprocal cooperation should never evolve. l-low, then, can we account for the cases of reciprocity that have been observed in nature? One ansi-ver comes from examining scenarios in which two players interact repeatedly, not just once. Robert Axelrod and W. D. Hamilton have shown that when this condition applies, individuals that use the simple l‘layer l3 (fooperale Defect Reward for mutual Ull’PL-‘mt" cooperation (only 1 year in prison.) Maximum punishment i (10 years in prsion) ‘ I)lé ".3 I A I . . 1’“ I Figure 13.15 The prisoner’s dilemma. The dia— gram lays out the payoffs for player A that are associat- Punishment for 4... Maximum reward more“ mutual defection ed with cooperating or not cooperating with player B. (freedom) (5 warb- in prism) : Detection is the adaptive choice for player A given the I I . conditions Specified here (ifthe two individuals will i . -.__.._._,_ interact only once). Chapter 13 decision rule. “Do unto indix'idual X as he. did unto you the last time you use. can reap greater t'a'ci'all gains than cheaters n-l‘io accept t‘issistance but do in L returl't the favor [~16]. l’Vhen multiple interactions are possible, the rim-yards ti : hack—and~foi"tl1 cooperation add up, exceeding the short-term payoff from a s“; gle ClCltK‘llOI‘i. in fact, the potential accunnilation of rot-yards can even favor intif. \-’idtIals W ho "forgix-c” a fellow player for an occasional defection because that tactic can encourage maintenance of a long—term relationship with its addition-i pa yoffs | [239 ]. Vampire bats appear to meet the required conditions for adaptiye multipl- play reciprocity. These animals must find scarce vertebrate victims from whit“, to draw the. blood meals that are their only food. After an evening of fora gins;- the ha ts return to a roost where individuals lmown to one another regularia assemble. A bat that has had success on a given evening can collect a larg amount of blood, so much that it can afford to regurgitate a life—sustainin- amount to a companion who has had a run of bad luck. Under these circum- stances, the cost of the gift to the donor is modest, but the potential benefit it.- the recipient is high, since Vampire 'ba ts die if they fail to get food three night:~ in a row. Thus, a cooperatix-e, blood—transferring vampire bat is really bu yir‘r: insurance against starvation dot-en the road. individuals that establish durable “git-c and ta Ice." relationships with one another are better off over the long hats; than those cheaters that accept one blood gift but then l‘enege on repayment. thereby ending a potentially durable cooperative arrangement that COLllf..l im'olx'e many more meal exchanges [1304]. Altruism and Indirect Selection- Reciprocity is really a special kind of mutualisi'n in which the helpful ind ividu-n endures a shortnterm loss until its help is reciproce‘ited, at which time it earns a net increase in fitness. in contrast, there a re some cases in which a donor reall.i does permai‘iet:tly lose opportunities to produce offspring of its own as a resui! of helping another individual. In ca’olutionary biology, this kind of helpful behay ior is called altruism (see "liable “if-i2). Altruistic actions, if they exist, are an espe cially exciting Dan-yinian puzzle for adaptationists because they \‘iolate t'l‘ie. “rule” that traits cannot spread over evolutionary time. if they ion-mar an indiyiclut’il’: reproductive success relative to that of other indiyid uals (see Chapter 'l ). in order to explain how altruism could evolve, W. I). l-lai‘niltoi'i developed a special explanation that did not rest on ftir-the~good--of—the—gniup a rgumentn [502]. Instead, l'latniltoi'i’s theory was based on the piemise that individual:- reproduce. with the unconscious goal of propagating their alleles more success- fully than other individuals. Personal reproduction contributes to this ultimati' goal in a direct. fashion. But helping genetically similar individuals- that is. one’s relatires—«sun!ire to reproduce can prcaiide an indirect route to the \‘erf. same end. :zlkl .' 'ail~fi.-lll:il.l..:1I... ..-_B H .II i To understand ’t’t’liy, the concept oi the coefficient of relatedness comes i. .- handy. This term refers to the probability that an allele in one individual is present in another because both individuals have inherited it from a recent com- mon ancestor. li'nagine, for example, that a parent has the genotype A/ri, and that a is a rare form of the ,4 gene. Any otfspring of this pa rent" will have a 50 per- cent chance of inheriting the a allele because any egg or sperm that. the. parent donates to the pn'iduction of an offspring has one chance in two of bearing ths‘ a allele. The. coefficient of relatedness beti-yeen parent and offspring is there- fore o r 0.5. The coefficient of relatedness varies for differei'tt categories of relatives. For example, an uncle and his sister’s son have one chance in four of sharing an allele by descent because the man and his sister ha ye one chance in titre of bat-'- ing this allele in common, and the sister has one chance in two of passing that . . . _ . _ . ‘ qu—m .‘nhh- am» an. . .hli‘lo-b I“ IJI—L a “A. m Muwaithuh-m“ nus I... 0(- Mthxwflwfiwnmw ohhflmfimmm.m" i r" ", . .- I... €Z‘,.\, :.._" 3&,.,|_....'. __ 4?. " lllfj L_V(_JiL/lll(.f‘.l iif _.-'.;'x lt‘.iir :.-L‘:iri -l[,i ‘1’ l allele on to an y given offspring. 'l'heretore, the coefficient of relatedness for an uncle and his nephew is %x : or 0.25. For tvvo cousins, the r value fai Is to is, or {H25 In contrast, the coefficient of relatedness between an individual and another, unrelated individual is 0. With kncn-vledge of the. coefficient of relatedness between altriiists and the individuals they help, we can determine the fate of a rare "altruistic" allele that is in competition with a common “selfish” allele. The key question is whether the altruistic. allele. becomes more abundant if its carriers forgo reproduction and instead help relatives reproduce. Imagine that an animal could potentially have one. offspring of its own, or alternativer invest its efforts in the offspring of its siblings, thereby helping three nephews or nieces sari-rive. that would have oth— erwise died. A parent shares half its genes with an offspring; the same ind ivid— ual shares one—fourth of its genes with each nephew or niece. Therefore, in this example, personal reproduction yields r x 'l 2: 0.5 x "l r: 0.5 genetic units con-- lributed directly to the next gei'ieration, iii-“hereas altruism directed at relatives yields r x 3 -: 0.25 x 3 = (1.75 genetic units passed on indirectly in the bodies of . relatives. In this example, the altruistic tactic is adaptive because it results in more shared alleles being transmitted to the next generation. If an altruistic act increases the genetic success of the altruist, tl'ien in what sense is this kind of altruism actually selfish? In everyday lii'iglish, words like “al- truism” and “selfishness” carry u’ll‘l‘l them an implication about the motivation and intentiims of the helpful individual. Why might everyday usage of these words get us into trouble when we hear them in an evolutionary context? Consider the proxi- mate—ultimate distinction here. If an individual inach’ertently helped another at re- productive cost to itself, could the behavior be called altruistic under the evolution— ary definition? Another way of looking at this matter is to compare the genetic consequences for individuals vvl'io aid others at random versus those who direct their aid to close relatives. Ifaid is delivertxl randon'ilv, then no one form of a gene is |il<el_v '- . :u " vfl. . _-.“- ' to benefit more than any other. But if close relatives aid one another selec~ tivelv, then any rare family alleles they possess may survive better, causing those alleles to increase in frequency compared with other forms of the gene in the population at large. When one tl'iin.l<s in these terms, it becomes clear that a kind of natural selection can occur when geneticallv different individuals differ in their effects on the reproductive success of close rela ti ves. _lerrv Brow n calls this form of selection indirect selection, which he contrasts with direct selection for traits that promote success in personal reproduction (Figure mien) [158]. .l {71.}.-.__ -...__._-__..._ ___- __ _____-- __ ___-g . ' l.l\ll_)l\flt)U;’-\.I_, I’RODULTES t)l-'FE»‘I’RI.N(_; l F'gurfi 1316 . The Comp‘lnems Of ,4, selection and fitness. {A} Direct selec- Direct selection "\:] 51'”le Without Permit?” Cal‘s tion acts on variation in individual repro- , N3 SUI‘WW bGCflU-‘v‘t’ 0* Pflft’nt‘dl Cat‘s _l ductive success. Indirect selection acts on ' INDIVIDUAL Hm’ps RELATW : Kin selection variation in the effects individuals have 3 . . , , on their relatives’ reproductive success. E “"11me seledmn " N3 “ll-WW became 0f Imp l (B) Direct fitness is measured in terms of ~— ------ __..--.._ ' personal reproductive output; indirect fit-- :03) —l ness is measured in terms of genetic 3g ‘ _ _ fl gains derived by helping relatives repro— Direci fitness -. (N, x r) i (N; X r} F Indmi H H ' duce. inclusive fitness is the sum ofthe indirect “mess N“ X r l— ‘ we 1 new . two measures and represents the total '4 . ~‘ -' j generic contribution ofan individual to __ _ _____ _ _ _ ______ ___,._.__J the next generation. After Brovvn llS8]. i ' h‘u'o' 452' Chapter 'I 3 A brief digression is necessary here to deal with yet ai‘iother term, kin seleic tion, wl'iicl‘i vvas originally defined by John M avi'ia rd Smith to embrace the evolutionary effects of both parental aid given to descendant kin {offspring} r5735; altruism directed to nondescendant kin {relatives other than (inlfsipringl biolo— gists l‘tft‘v’t? long recognized that pa rents can improve the survival chances of their offspring, and that parental care spieads when the resulting increase in the sur- vival of the aided offspring more than compensates a parent for the loss of oppor- tunities to produce additional offspring in the future (see Chapter 12). in genetir terms, parents can gain via parental im-‘estment ltiecause they share 50 percent of their genes with each offspring. it}! the same token, hot-vexer, individuals can promote the survival of certain of their genes by helping relatives other than offspring. Altruism can be favored hv the component of kin selection that Bros-vii calls indirect selection, and the use of this term keeps the. focus clearly on the dis— tinction between parental effects on offspring and an aid—giver’s effects on non- descendant kin [l 58]. The term ltfii selection is, l't()1~\-'(‘\='t-?l', *widely used by evolu» tionary biologists as a synonym for indirect selection, and readers should be LIW'ai‘e that when they see the term, odds are that it is being used to refer to selection for altruism supplied to relatives other than offspring. indirect Selection and the Alarm Call of Beldi'ng’s Ground Squirrel Having laid the necessary theoretical groundwork, let’s use it in analyzing an alarm-calling behavior that might be an altruistic act, but keeping in mind that what looks like altruism might actually be a case of m utualism or reciproc— ity with direct fitness benefits for the helpful individual [480]. You will recall that African meerka ts stand on guard to warn of approaching predators, but that their behavior appears to improve their own survival more than that of the other meerkats they alert to danger. Does the same. story apply to Belding’s ground squirrel? ".l'his North American rodent produces a staccato alarm whis— tle (.Fi gu r i "I 3.'l 7) when a coyote or badger approaches, which sends other nearby ground squirrels rushing for safety. l’a ul Sherman collected the evidence needed to evaluate alternative l'iypothe— ses on the adaptive value of the ground squirrels alarm call [1094-]. l le found that alarmacalling squirrels are tracked down and killed by weasels, badgers, and coyotes at a higher rate. than noncallers, a discrnrery that eliminates the pos- silgiilitv that alarm calling confers direct fitness on the signa ler by confusing or deterring predators. lVlorem-er, the possibility that alarm calling evolved as a form of reciprocity is also unlikely, because the probability that an individual will give an alarm call is not correlated with familiarity or length of associa tion between the caller and the animals that benefit from its signal ['ltJ‘JS]. Remember that reciprocity is more likely to evolve when reciprorators form long~lerm associations. Sherman’s observa‘itit'n‘i that adult female. squirrels with relatives nearby are more than twice as iil<ely as males to give costly alarm calls is consistent with both a parental care hvpotl’iesis (based on direct. selection) and an altruism l1}-'pothesis (based on indirect selection). You may recall that female Belding’s ground squirrels tend to settle near their n'iothers, whereas males disperse some distance away from their natal burrow (see Figure 8.] 0). If the parental care hypothesis is correct, we would expect females to give more alarm calls than males because only feinale squirrels live near their offspring. lf th .‘ altruism l'iypotl'iesis is correct, we. can also predict a female bias in alarm calling because females not only live near their genetic offspring, but are also surrounded bv other fernale relatives, such as sisters, aunts, and female cousins. When self—sac-d Figure 13.17 A Beiding’s ground squirrel gives an alarm call after sp0t~~ ting a terrestrial predator. Photograph by George Lepp, courtesy of Paul Sherman. The [.1VC3lLlilOn of Social Behavior #3..“ rificing females warn their nondescendant kin, they could be compensated for the personal risks they take by an increased probability that kin other lliu‘ii off- spring will survive to pass on shared genes, resulting in indirect fitness gains for the allruists. Females with offspring living nearby as well as females i-vith only nondescendant l<in as neighbors are in fact more, likely to call upon detect-- ing a predator than are females who lack relatives in their neighborhood. These findings suggest that both direct and indirect selection contribute to the mainv tcnance of alarm calling behavior in this species [1094]. The Concept of Inclusive Fitness Because fitness gained through personal reproduction (direct fitness) and fit— ness achieved by helping nondescendant kin survive (indirect fitness) can both be expressed in identical genetic units, we can sum up an individual’s total con— tribution of genes to the next generation, creating a quantitative measure that can be called inclusive fitness (Figure 13.168). Note that an individual’s inclu— sive fitness is not calculated by adding up that animal’s genetic representation in its offspring plus that in all of its other relatives. instead, what counts is an individual’s own effects on gene prepagation (1) directly in the bodies of its sur— viving offspring Hmt oree their existence to the parent ’s actions, not to the efforts of others, and (2) indirectly via nondescendant kin that would not have existed tirt‘rptfor l'flt’ individuals assistance. For example, if the. animal we mentioned ear- lier successfully reared one of its own offspring and also adopted three of its sibling’s progeny, then its direct fitness would be 1. x 0.5 = 0.5, and its indirect fitness would be 3 x 0.25 : 0.75; the. union of these two figures provides a meas— ure of the animal’s inclusive fitness (0.5 + 0.75 = 1.25). The concept of inclusive fitness, however, is not used to secure absolute meas— ures of the lifetime genetic contribution of individuals, but rather to help us compa re the e\-'olutionary (genetic) consequences of two alternative hereditary traits [990]. In other words, inclusive fitness becomes important as a means to determine the relative genetic. success of two or more competing beha-avioral strategies. If, for example, Wt"? wish to know whether an altruistic strategy is superior to one that pron'iotes personal reproduction, we can compare the inclu— sive fitness consequences of the two traits. In order for an altruistic trait to be adaptive, the inclusive fitness of a ltruistic individuals has to be greater than it would have been if those individuals had tried to reproduce personally. In other words, a rare allele “for” altruism will become more common only if the indi— rect fitness gained by the altruist is greater than the direct fitness it loses as a result of its sel f—sacrificin g behavior. This statement is often presented as Hamil~ ton’s rule: a gene for altruism will spread only if rats} 2:» if. Spelling this out, we calculate the indirect fitness gained by multiplying the extra number of relatives that exist thanks to the altruist’s actions (B) by the mean coefficient of relatedness between the altruist and those extra individuals (iii); we calculate the. direct fitness lost by multiplying the. number of offspring not produced by the altruist (C) by the coefficient of relatedness betx-vetm parent. and offspring (rt). For example, .if the genetic cost of an altruistic act wer‘r the loss of one off— spring (‘l x rt. : l x 0.5 t 0.5 genetic. units), but that altruistic act led to the sur— vival of three nephews that would have others-vise perished (3 x rt} 2 3 x 0.25 '— 0375 Genetic units), the altruist would experience a net gain in inclusive fitness, thereby increasing the frequency of any distinctive allele associated with its altruistic behavior. .'.i‘.i-m..1....m‘- " fiuJA-D‘M' ‘.:;.-’°“ '=‘ ' 'mfi-) ML’.‘{_.‘-&.;:' kg“. 4.1.“: . “L‘A&~m .‘ .‘ Jami-A .0... q.» ;,' .' . - 3n H—m—‘mnnA-KA-m-M.a—. hm“... _....n-dp- ass-Qua..-” .M ‘ua.'4_:.e.-_..uv_‘:..-.u.~.. ' --v 4-bit (Q 52a pter l let’s say that in calculating the inclusive fitness of a male. in a coalition of %; ons, you measured his direct fitness by m Lllthl‘g-‘ll'lg by (1.5 the number of ol'l’sprins. produced by the male, and then added as his indirect fitness the total Inn'nber ol offspring produced by the other n'iembers of his coalition times the mean value of ,. between those offspring and the male in question. Your calculation of his inclush ~- fitness would be challenged on what grounds? Inclusive Fitness and the Pied Kingfisher The ralue of Hamilton’s rule can be illustrated by Uli Reyer’s stud y of the pie: : kingfis net ['1 0'13). 'l'hese attractive .African birds nest colonially in turmels is. ha n ks by large lakes. Some yearaold males are unable to find a mate, and insteaai become prewar}; helpers that bring fish to their mother and her nestlings n-‘liil: attacking predatory snakes and mongooses that threaten the nest. Are thest males propagating their genes as effectively as possible by helping to raise thei: siblings? They do have other options: they could help unrelated nesting pair.» in the manner of secondary helpers, or they could simply sit out the breeding sea son, waiting for next year in the. manner of drawers. To learn why primary helpers help, we need to know the costs and benefits of their actions. Primary helpers work harder than delayers and the more laid- hack secondary helpers (Figure '13.] 8). The greater sacrifices of primary helpers translate into a lower prol Ability of their surviving to return to the breeding grounds the next year ( just percent return) compared with second a rjr helpers (74 percent return) or delayers (70 percent return). Furthermore, only two in three surx-ix'ing primary helpers find a ma te in their second year and reproduce personally; whereas 91 percent of returning secondary helpers succeed in breed ing. Ma n}: one—time secondary helpers breed with the female they helped the preceding year (l (l of 27 in Reyer’s san'iple), suggesting that improved access to a potential mate is the ultimate pa yoff for their initial altruism. These data enable us to calculate the direct fitness cost to the altruistic pri— mary helpers in terms of reduced personal reproduction in their second yea r oI' life. lior siinplicity’s sake, we shall restrict our comparison to solo prirnart‘ helpers l:hat help their parents rear siblings in the first year and then breed ow their oxen in the second yer-u; it they survive and find a ma te, versus second - Htl I‘ .g I. C, hi] ‘ ' § 3 ll} '- f i E .r} 2 ;~J ; 53 E .5 5 7., ~') - E .5 All a ‘-1- I Figure “£3.18 Altruism and relatedness in pied kingfish’ers. . Primary helpers deliver more calories per day in fish to a nesting u --— x - I“ I ------P I —L- . -~ female and her offspring than do secondary helpers, which are not " M" t m“ L “malt Jl-Hmdd'} 1 related to the breeders they assist. After Reyer [l 013]. Breeders I'lclpers The Evolution becial Behavior TABLE 1 3.3 Calculations of inclusive fitness for male pied kingfishers First year Second year Behavioral tactic y r f] o r s m f2 Primary helper 1.8 x 0.32 : 0.58 2.3 x 0.50 x 0.54 x 0.60 2 fig—ll Secondary helper 1.3 x 0.00 = 0.00 2.5 x 0.50 x 0.74 x 0.9] 2 0.84 Delayer 0.0 x 0.00 2 0.00 '25 x 0.50 x 0.70 x 0.33 = 0.29 Source: Reyer l 0113] Sywnbois: i; -"'- extra young produced by helped pa rents; o :..~. offspring produced by breeding L’s-- helpers and cielayers; ." coefficient of relatedness belt-teen the male and if, and between the male and 0;}, -.-.r fitness in first year (indirect fitness for the primary helperlgfg 2 direct fitness in second year, s :2 ].')I'(}L‘.al.')ilil'}’ of surviving into the St‘CtHlLl year; or : probability of finding a mate in the second year. a ry helpers that help nonrelatives with no other helpers present in the first year and then reproduce on their own in the second year, if they survive and find a mate. Primary helpers throw themselves into helping their parents produce off- spring at the cost affirming less chance of reproducing persona/1,1,! in the next year. Although primary helpers do better than delayers in the second year (0.4] versus 02.9 units of direct fitness), secondary helpers do better still (0.84 units of direct fitness) because they hay-e a higher survival rate and a greater proba- bility of securing a partner (Table. 13.3). But is the cost to primary helpers of 0.43 lost units of direct fitness (0.84 — (Hi. 2 0.43) in the second year offset by a gain in indirect fitness during the first year? To the extent that these males increase their parents’ reproductive success, they create siblings that would not othen-vise exist, indirectly propagating their genes in this fashion. In Reyer’s study, the parents of a primary helper gained an extra l .8 offspring, on average, when their son was present. Some primary helpers assisted their genetic. mother and father, in u-rhich case the extra '1 .8 siblings were full brothers and sisters, with a coefficient of relatedness of 0.5. But in other . cases, one parent had died and the. other had remated, so that the offspring pro— duced were only half—siblings (r : 0.25). The a Mirage coefficient of relatedness for sons helping a breeding pair was thus between one-fourth and one—half r = 0.32). Therefore, the average gain for primary helper sons was 1 .8 extra sibs >< 0.32 = 0.58 units of indirect fitness, a figure higher than the mean direct fit~ ness loss experienced in their second year of life. Reyer used Hamilton’s rule to establish that primary helpers sacrifice future personal reproduction in year 2 in exchange for iricrn'rseri numbers of nonde— scendant kin in year 'I [1013]. Because these added siblings carry some of the helpers’ alleles, they provide indirect fitness gains that more than offset the loss in direct fitness that primary helpers experience in their second year relative to secondary helpers. '-'~’ -'a-'-?u'.w\..2v;.;m.x_‘u.-m,&.:;;.;aa.g._' ,.~,'.,,- - - VF“;‘:‘.: Iu-‘J—‘t. -'_ ML..JnI'E..Jha-_x.' . Given the results of our calculations of inclusive. fitness for male pied king— fishers, why are there ever any delayers? is it maladaptive to be a dela yer? (fan you use conditional strategy theory to analyze this case? Another lion problem: Let’s say that a lion pride typically consists of 10 re— prod ucti yer mature females. imagine that a male working by himself has a 30 per- cent chance. of acquiring and defending a pride for 1 year. l'iowever, a pair of males has a 80 percent chance of holding a pride for this same period. ('1) Assuming that all the females mate with the male or males that con'trtfl their pride and produce one ‘ halt-outing“... -uh—‘_._ a...—. .n...‘ ._,..z.._. ‘ Mwlnnw m-WWA_M ,,_. v_ I .~_ “In 1; . . 4 is if: Ch Chapter 13 youngster apiece during the year, and that both males in a two-male pride sire .. equal number of young, should two unrelated males get together to secure thin harem of females? {2) What it the males are cousins? (3') Now imagine that tin males a re halt-brotl'iers, but the dominant male manages to get 80 percent oi ; 2‘: matings, and so 80 percent of the offspring are his. Should the subordinate join -. coalition t-t’il‘l‘t his dominant haltlbrother? in all you r calculations of inclusit'e t}. ness, identity the direct. and indirect fitness components. (i his question is courte: ‘ of Mike Beecher, to whom any complaints should be directed.) inclusive Fitness and Helpers at the Nest In the pied kingfisher, primary helpers raise their fitness indirectly tl'irough thei. increased production of nondeseend ant kin, it'hereas secot'idar}? l‘ielpers this their fitness directly by increasing their future chances of reproducing person ally. Primary helpers demonstrate that altruism can be adaptive; second a r t hetpers show that helping need not be attruistic, but instead may generate diret t fitness benefits to helpers. Thus, this one species offers support for tuft": very d it terent adaptationist hypotheses on the evolution of helping behavior. These hypotheses can be tested for other tases of helpers at the. nest, i-rhich are found in a variety at other birds, as well as fishes, mammals, and insects [158, 229, 9942, ll 77]. Each case of helpers at the nest presents a separate puzzle that deserves be analyzed in light of a full range of l‘iypotheses, including the possibility that caring for another’s offspring is a iioimdnptiee side effect of other adaptive traits. As [an lamieson has pointed out, helping may have originated in some bird species as a n incidental by—p rod act of genetic or ecological changes that made it adaptive for young adults to delay their dispersal from their natal territory [581} 588]. Jf these stay—at—home birds were exposed to the nestlings being cared lo: by their parents, the begging behavior of the baby birds might have activated Par mtal behavior in the young l’tonbreed in}? ad tilts. This behavior could then be maintained over evolutionary" time as a by—product of tin-’0 a daptive traits, s- delatw’ed dispersal and the tendency to care for one's ot-t'n ot'l'ispring, even it: feed-- ing someone else’s young reduced the fitness of nonhreeding helpers. ’l'his nonadaptire b},-‘—product l‘iypothesis assumes that selection could not eliminate the helper’s tendency to iced its {Starents’ offspring tit-’iljhout also destroflng the capacity of the Bit‘t}:’-at-l“lt}ITtC bird to invest in its ow n nestlings at a later date. This pmposition is testable. One of its key predictions is that the. underlying mechanisms of parental care. should be no different in species with helpers than in species without helpers. The group of birds known a»- iays provides the necessary con‘iparative test. In the Mexican jay (Aplicleomm ultnnmiriim) and Florida scrub ja {zip/it’l’tit‘ttilit? cueruiescms), some nonbreed ing birds help their parents rear additional siblings (Figure iii/l9). The nest ern scrub iat-r (/lplirlerrmm t‘iililiiriii'ea) is a member ol' the same genus, but lacks helpers at the nest. in this s}..‘iecies, only breeding individuals have. high pro-- t'dllh-amu-a-‘uu'n—fi" dibnihfi-.m' U.M‘I.\‘chm 'u. A“ 3.0".‘HK: ,_'; . lactin levels, wl'iile nont’ireeders have lot-r levels of this hormone, which appears to regulate parental care in many birds. In contrast, non breeding helpers in the Mexican jay and Florida scrub jay have prolactin levels that match those ol their breeding parents 11072, 1237]. N'iOI'CO‘x’UT, the prolactin in non breeding Mex-- ican jays rises to pea k let-’els tum there are young to Iced in the nest (Figure 13.20), suggesting that selection has fat-'ored nonbreeding individuals of this species that a re capable of becom ing l‘iornionall}r primed to rear their sil'ilingw [1237]. These results are at odds with the nonadaptive byproduct explanation for helping. But it helping is adaptive, do helpers derive. inclusive fitness Oains \‘ia the . \' direct or indirect route, or both? In the Mexican in}: and Florida scrub jay, some The Evolution of Social Behavior 45-}? Figure 13.19 Cooperation among a direct scrub jay relatives. Helpers at the nest in the Florida scrub jay provide food for the young, defense for the territory, and E: stay-a t—home helpers inherit their natal territories from their parents ' fitness benefit. Furthermore, parents t-vith helpers rear more offspring than pa r— ents without helpers, which generates a n indirect fitness benefit for the helpers C protection against predators. Based on a as well ("fable 13.4) [l58, 1338]. However, the apparent increase in the number drawing by Sarah Landry, from Wilson of offspring fledged by pairs with l'rellpers might arise strictly because helpers [1315]- live with parents that ha ve better territories, Twhich provide more food or supe- rior nesting sites. The hypothesis that territon quality, not helpers at the nest, is responsible for differences among breeding pairs in the number of fledglings produced was tested by Ronald Mumme. He. captured and removed the non~ breeding:J helpers from some randome selected breeding pairs of Florida scrub jays, while lea vine; other helpers untouched. The experimental removal of (A) Breeders Nestlinits {Bl Ntllll‘l't‘(?tit‘1”5 NilSlll’lgi‘ hatch hatch . . . I . lager; \t‘sllmgs luggs = Nestlmgs laid fledged laid fled ged l i l l If I I I ‘— r .' I l’ I l ‘ I I I I i 1 Females la 1 i I I I I I ' l 3 i I w Males I 0 a; ; __ Fill. i log i ,fi 30- .49 i6 0: .z . I a I —- I I | _: :o i GiggloO: i. “N.- 1. Q I KM“ I .z ' CL I a I I CC db“ .- g I a C '0 .l 9 C o I’ 9"! g I o j ‘ : : : ‘«—r F) | . I a I .5 «U . . .°. .45 a“ ‘ e r : «If. . - I I : f“ I G J 'F" . : r I F! I. I a I ‘l ‘ 75 i i i "f ' ; ’ o: .3 I: l I I 0 I I O O I" I n ' ' H ' Q I i m o I I i ° 1 . l a i i i 9 a I I I I O I l a 3 I I I I I I o I J I ‘ I I I ’ o ‘ z a 6 I I I (3 -.._._l—L__1 _ *L- _ .l_l_l_l___ - ____s._l ll t_;._°_gut_-'_LHI-.__LI_LH_.__J ---'l2.‘§ —'l[}{l ~75 ----5tl "25 [l 25 50 ‘75 Hill 125 4125 --ll}tl 47:3 "fill “25 [1 2'3 5t} '75 Hill 125 Days relative to own clutch l'Jajt-s relative to first clutch in group Figure 13.20 Seasonal changes in prolactin concentrations in breeders and non~ breeding helpers at the nest in the Mexican jay. Nonbreeding birds in a group exhibit the same pattern of inCreased prolactin production prior to the hatching of eggs as do breeding adults. After Brown and Vleck [160] v 45% Cha pier 'i 3 TABLE 1 3.4 Effect of Florida scrub jay helpers at the nest on the reproducti , success of their parents and on their own inclusive fitness Parents without Parents with breeding experience” breeding experience Average n umber of {leclglings I {H l (32 p roduced with no helpers AVOI‘agt.‘ number of fledglings 2.06 2.20 produced with helpers Increased reproductive success 1.03 0.58 due to help Avemge number of helpers 'l .70 lfiil} indirect fitness gained per helper 0th [1.30 ' Source: tzl'nlen I365] “includes pairs in which one parent has reproduced, which is vile; some pairs in this category acquire a heiper at the nest. helpers reduced the reproductive success of the experimental pairs by aboui s”- percent, as measured by the number of offspring knot-en to be alive (ill days aiie‘ hatching (Figure 13.21 ). l--lelpers apparenthi really do help in this species [85" i. In fact, helper scrub jay-1s also improve the chances that their parents will iii to breed again another year, as do helpers in the pied kingfisher. improve: parental survival means that the helpers are. responsible for still more. SlbllL-l in the. future; these extra siblings yield an ax-ierage of about 0.30 additional iii-.2: rect fitness units for helpers [861]. Thus, the total indirect fitness gains in helping at the nest can potentially exceed its Costs in terms of lost direct fitnes- -. especially if the young birds have. almost no chance of reproducing perso :~ all}: When very few openings are ax-u-iilable for dispersing young adults, 1m - ing is more. likely to be the adaptive option for ii'idi\.-'icluals that have the putt . tial to be either altruistic or to reproduce on their oi-vn. lndi\.-'idi.lals of this s: «2 can be said to be. lacultative altruists (see. Figure. 13.8) because they are. “.ol' loclw - into the helper role. W’hetl'ier saturated nesting habitats con tribute. to the main tenance oi liei; : ing at the nest is also testable. if young birds remain on their natal terriiors: :. because they cannot find suitable nesting habitat, then }.ieai‘li1‘igs gi\-'en an oppi tunity to claim good open territories should pi’OI]’iptl}-’ become breeders. _I.".: Korndeu r did the necessa r}: espcriment with the Sc}.~’chelles warbler, a eh: little brown bird that has played a big role in testing en’olutionary hypothes’ 31} :— iF l::l Experimental q u; Cl Control us .; 'i #— Niean number of oftsprin . Figure “I 3.21 Helpers at the nest help parents raise more siblings in the Florida scrub jay. The graph shows numbers of offspring alive after 60 days in experimental nests that lost their helpers and in unmanipulated control nests during a 2—year experiment. After Mumme [859]. lite. Evolution of Social iflt-iisavior 41>??? about helping at the nest. When Komdeur transplanted 58 birds from one island (Cousin) to ti-vo other nearby islands with no t-X’DI‘blthS, he created vacant terri— tories on Cousin, and helpers at the nest. there immediater stopped helping in order to move into open spots and begin breeding. Since the islands that: receit'ed the transplants initially had many more suitable territorial sites than warblers, Komd eu r expected that the offspring of the transplanted adults would also leave home promptly in order to breed elset-yhere on their own. They did, providing further evidence that young birds help only when they ha re little chance of ma king direct fitness gains by dispersing 1658]. lX/loreover, the sophisticated conditional strategy that controls the dispersal decisions made by young Seychelles Warblers is sensitive to the quality of their natal territory. Breeding birds occupy sites that vary in size, vegetational cover, and insect supplies. By using these variables to divide warbler territories into categories of low, medium, and high quality, Komdeur showed that young helpers on good territories were likely to su.i'\-'iye there i-vhile also increasing the odds that their parents would reproduce successfully. ‘r’oun g birds whose pa r- ents had prime sites often stayed put, securing both direct and indirect fitness gains in the process. in contrast, young birds on poor natal territories had little chance of ma king it to the next year, nor could they have a positive effect on the reproductive success of their parents. They left home and tried to find a breed— ing opportunity of their own [657}. l-lelpers at the nest have been found in only about 3 percent of all birds [Sill Oiie attribute of this small minority of birds that has often been linked to the evolu- tion of helpers is the delayed dispersal of juveniles, as we have just illustrated for Florida scrub jays and Seychelles warblers. But another factor that might haye pro- moted the evolution of helping is a very low adult mortality rate. These two ideas have sometimes been prosen ted as competing h }-*ptitlit.‘st-_rs, but how might they both reflect the same ecological pressure that makes helping at the nest an adaptive mal — ing—the-best—tif—a-bad-job option for young birds? v. --.-:.:.m.,i' ..'u.....;_.'z " ' ‘ ‘ :11, '%..—I 'l he flexibility of behavior exhibited by Seychelles warblers is not unique to that species. Consider how young fem ale. t-yl'iite~fronted bee—eaters make adap— tive conditional decisions about reproducing (Figure 1.3.22). 'i‘his African bird nests in loose colonies in clay banks. Like male pied kingfishers, young female white-fronted bee-eaters can choose to breed, or to help a breeding pair at their nest burrow, or to sit out the breeding season altogether. if an unpaired, domi— na nt, older male courts her, a young female almost alt-vays leaves her family and natal territory to nest in a different part of the colony, particularly if her mate has a. group of helpers to assist in feed in g the offspring they will prod uce. Her choice usually results in high direct fitness payoffs. But ifyoung, subordinate males are the. only potential mates available to her, the young female will usually refuse to set up housekeeping. Young males come with fer-v or no helpers, and. when they try to breed, they are often harassed by their fathers, who may force their sons to abandon their mates and return home to help rear their siblings. A female that opts not to pair off under un fa vorable conditions may choose i to slip an egg into someone else’s nest, or to become a helper at the nest in her natal territory-----provided that the breeding pair there are her parents, to iii-"horn she is closely related. If one or both of her pa rents have. died or moved away, she. is unlikely to help rear the chicks there, which are at best half—siblings, and instead will simply wait, conserving her energy for a better time in t-vhich to reproduce [3641‘ Thus, although daughter bee-eaters have the potential to become helpers at the nest, they choose this option only when the indirect fit— ness benefits of helping are likely to be substantial. \ II ,L‘n"..a(,t,‘ -.. u-u. ~---:- ~— - a-nv-—O':-m__.L-u-_.... a... “A '0“. .h‘_._..n_-._._._n.__~y_\__‘_.a .. .. Figure 1.3.22 Conditional repro- ductive tactics of female white-front— ed bee—eaters. Females of this species have many options, of which helping at the nest is only one. Females select a given Option depending on their special circumstances. After Emlen et at. [3641- I Breeder up! ionj -_. -.__ ____..a n.--——-— l’airs and nests Lays eggs in other pairs" nests [Parasite optionJ [Nonparticipant option—l l.-.‘-_,. . _.._-. “a. ._-_—_.-_ _u_4 Sits out breed ing season (“it ("V (“K i \ ,1 \ t \\ t ) ' ,. t i \‘p C L ‘\ kW (“t P _\ ,5) ' a I. l i i \ .I i "1,5 It \R liem ale leaves natal site i F0111 a le Stilt-’8 wi th parents c\ l t3 L5 5- Helps (turf lays t3 Ci “ t ' t O Hits out breeding season egg in host nest .— __ ! Nonparticipant option - . —.—n..r—— Insect Helpers at the Nest Although some birds provid e impressive examples of adaptive helping at the nest, the phenomenon also occurs in highly sophisticated forms in certain insects, includingr the paper wasps mentioned at the beginning of this chapter. Paper its-“asp colonies usually consist of one or more reproductix-‘ely active females and a number of helpers at the nest, or workers, which are always females, never males. In order to generate a set of female helpers early in the nesting cycle, egplaying temalc wasps fertilize. some. eggs by releasing sperm from a sperm storage organ as the eggs pass down the oi-‘iduct. These diploid eggs will develop into females, whereas to produce a son, a. queen need only lay an unfertilized (haploid) e. jg. All the l-lymenoptera (the t-i-'asps, bees, and ants) can use this haplodiploid system of sex determination to produce daugh~ ters and sons at the appri'j)priate times during the breeding cycle ( Figu re 13.23). The degree to which hymenopteran queens can control the. fertilization ot' their eggs has been measured in the. honey bee. in this species, worker (female) I l'lelper at the nest option f [l lelper and parasite option ._‘ . . " .' :§~I'r:‘... ‘ l .. ...
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