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7KH(YROXWLRQRI*HQHURVLW\+RZ1DWXUDO6HOHFWLRQ %XLOGV'HYLFHVIRU%HQHILW'HOLYHU\ 0LFKDHO(0F&XOORXJK(ULF-3HGHUVHQ Social Research: An International Quarterly, Volume 80, Number 2, Summer 2013, pp. 387-410 (Article) 3XEOLVKHGE\7KH-RKQV+RSNLQV8QLYHUVLW\3UHVV DOI: 10.1353/sor.2013.0021 For additional information about this article http://muse.jhu.edu/journals/sor/summary/v080/80.2.mccullough.html Access provided by University of Miami (3 Sep 2015 19:25 GMT) Michael E. McCullough and Eric J. Pedersen The Evolution of Generosity: How Natural Selection Builds Devices for Benefit Delivery W H Y DO W E CE L E B RA T E D A R W I N DAY B U T NOT A R I S T O T L E DAY OR Newton Day or Descartes Day? The reason Charles Darwin is special enough to deserve a toast every Februaiy 12, quite simply, is because he cam e up w ith what philosopher Daniel D ennett has called “the single best idea anyone has ever had” (1995: 21): a purely naturalistic means o f explaining why living things bear features th at m ake them appear as i f they had been designed (West, Griffin, and Gardner 2007). Darwin’s fundam ental contribution to science was to identify a mindless, physi cal process th at could produce com plex, functional design, w hich he called natural selection. To understand natu ral selection, it is useful to th in k o f genes as replicating en tities that, through repeated generational cycles o f replication, m utation, and selection for variants that confer beneficial fitness effects on th eir bearers, com e to build “devices” around them selves. These phenotypic design features, w hich are “devices” in the sense o f having a com plex ordering o f interrelated and hierarchically organized parts th at cooperate to efficiently and elegantly accomplish some task, are how genes “take action” in the world, w hich eventuates in their increased reproductive success. And, it is through the increased social research Vol. 8 0 : No. 2 : Sum m er 2013 387 reproductive success o f the genes th a t produce these design features th at those features becom e species-typical (West, Griffin, and Gardner 2007; Dennett 1995; Dawkins 1976). The reality o f n atu ral selection as a biological process m eans th at genes (or com binations o f genes) th a t cause organism s to build traits that increase those genes’ rates o f replication— so-called adapta tions (W illiams 1966)— them selves w ill becom e increasingly com m on in any population o f genes. Consequently, organisms will, through the process o f natural selection, com e to bear traits that appear as i f they were designed to increase the organism ’s reproductive success. NATURAL SELECTION A N D THE EVO LUTIO N O F BENEFITDELIVERY DEVICES One o f the perennial sources o f fascination for evolutionary biologists is the realization that even though genes are “selfish” (in the sense that natural selection causes them to com e to encode recipes for traits that cause the organisms in w hich they reside to act in ways that benefit the genes’ own replication), the traits they create need n ot be (Dawkins, 1976): natural selection ’s action on genes can cause the evolution o f traits that cause organisms to interact w ith other organisms in coopera tive, generous, and even self-sacrificial ways. This is because there are many ways th a t delivering ben efits to oth er individuals in th e world ultim ately boost the rep lication rates o f the genes th at create these forms o f generosity. Here we use the term benefit-delivery devices to refer to the class o f biological systems th at evolved through natural selec tion, at least in part, because o f the benefits they caused organisms to deliver to other organisms. W H Y BENEFIT DELIVERY IS AN E VO LU TIO NA RY PROBLEM Ben efit-d eliv ery devices pose a p ro b lem for ev olu tion ary th eory because organism s th a t possess such devices should, all else being equal, experience less reproductive success than an organism th at does n ot possess such devices. This is because delivering benefits to oth er individuals prevents the b en efit deliverer from using those resources 388 social research to advance its own reproductive efforts. Consequently, it should be im possible for m utan t genes th a t cause organism s to deliver benefits to others to overtake a population o f genes th at do n ot create such benefit-delivery devices; fu rth erm o re, even i f a species did acquire a gene th a t caused it to deliver b en efits to others, th a t gene would easily be overtaken by a new m utant gene th at prohibited its bearer from doing so. Nevertheless, it is self-evident th at m any organism s (including humans) do possess devices for benefit delivery (including the cognitive ones th at m otivate us to care about other individuals), so a cardinal task for evolutionary science, at least as far as cooperation is concerned, is “exp lain in g how th e a ctu al is p o ssib le” (Rosenberg 1992, 19). Evolutionary scientists who study cooperation try to determ ine how natural selection builds benefit-delivery devices, w hich usually involves tiying to identify the routes by w hich the genes th at give rise to those benefit-delivery devices are “rewarded” through enhanced reproduc tive fitness. In general, evolutionary biologists divide the fitness bene fits that enable m echanism s for cooperation to evolve through natural selection into two broad types: direct fitness benefits (that is, the organ ism enjoys b etter reproductive success because o f an allele [variant o f a gene] that causes it to deliver benefits to others), and indirect fitness benefits (that is, the organism ’s direct reproductive success is reduced by possessing an allele th at causes it to deliver benefits to others, but the reproductive success o f other individuals who also share the same allele increases, thus prom oting the replication o f the allele overall). The sum o f direct and indirect fitness benefits is referred to as inclusive fitness (Hamilton 1964). In the rem ainder o f this article we will describe first some o f the direct fitness benefits, and then the indirect ones, that can lead to the natural selection o f benefit-delivery devices. We also describe what is currently know n (or conjectured) about the circu it logic governing the operation o f naturally selected cognitive m echa nism s that regulate benefit deliver. We close w ith a b rief treatm ent o f the concept o f group selection and its value for social research on the evolution o f benefit-delivery devices in humans. The E vo lu tio n o f G e n ero sity 3 89 NATURAL SELECTION O F BENEFIT-DELIVERY DEVICES THROUGH DIRECT FITNESS BENEFITS In evolutionary biology, a behavior is “social” w hen the m echanism s th at m otivate it evolved in part because o f the effects o f its behavioral outputs on oth er organism s. W hen genes give rise to benefit-delivery systems th a t m otivate generosity because those systems boosted the replication rates o f the ancestral copies o f the genes that govern their assem bly and operation, evolutionary biologists talk about mutually beneficial cooperative traits. Mutually beneficial traits evolve by natural selection because the beneficial effects o f those traits on other individu als in turn cause (by virtue o f second-order effects) an increase in the reproductive success o f the genes th at build the trait w ithin actors. It is worthwhile here to distinguish betw een systems that evolved for the function o f delivering benefits to others (that is, systems whose func tion is to increase others’ reproductive fitness) and systems that evolved for other functions, but w hich cause benefits to flow to other individu als incidentally in the course o f executing their evolved functions. For exam ple, elephants m ake available to dung beetles a substance th at dung beetles recognize as a benefit— elephant dung—but it would be silly to conclude from this observation that elephants defecate for the purpose o f delivering b en efits to dung beetles. Instead, the b en efit is a b en efit only because dung b eetle’s evolved to m ake the m ost o f elephants’ waste products (West, Griffin, and Gardner 2007). Thus, it is wise to restrict our d efin ition o f benefit-delivery devices to those th at have been designed via natural selection specifi cally fo r th e b en eficial effects they deliver to others (West, Griffin, and Gardner 2007). That is, some behaviors th at are often m istaken as exam ples o f “cooperation” or “generosity” or “altruism ” in hum an behavior m ight m erely reflect (a) actors’ pursuit o f th eir own direct fitness interests w ithout regard to their effects on others’ fitness, and (b) others’ opportunism in reaping fitness benefits for themselves from the actors’ behavioral by-products. Following someone hom e w hen you have becom e disoriented is a costless enterprise for the person whom you follow back to camp, for instance. She pursues her own self-inter 390 social research est by getting h erself back to camp—w ithout regard to your w elfare— w hile you pursue yours by following the path she takes. Thus, readers will do well to stay m indful o f the fact th at some apparent exam ples o f benefit delivery are not produced by benefit-delivery devices at all. Here, we hold such by-product exam ples o f “benefit delivery” aside and focus instead on some o f th e ways in w hich benefit-delivery devices can be explained in term s o f the direct fitness benefits they secure for th e genes responsible for building them . These include reciprocity, the extensions to reciprocity th at m ight have emerged from hum ans’ specialization in the cognitive niche, and group augmentation. Reciprocity The m ost com m only studied route by w hich benefit-delivery devices could have evolved in hum ans via n atu ral selection is recip rocity (Trivers 1971). The P riso n er’s D ilem m a, in w h ich two players are presented w ith a ch oice to cooperate w ith, or d efect against, each other, nicely illustrates how reciprocity can generate benefits. I f both players cooperate, they each receive a m oderate payoff; i f b oth defect, they each receive a sm all payoff; if one player defects and the oth er cooperates, th e d efector receives a large payoff and th e cooperator receives the sm allest possible payoff (the “su cker’s p ayoff”). Due to th is payoff stru ctu re, d efectio n always yields th e h igh est average payoff in a one-shot in teractio n (that is, an in teraction th at w ill not be repeated). However, i f th e gam e consists o f m ultiple rounds o f iter ated play, m utual cooperation can lead to higher average payoffs than m utual or alternating d efection (Axelrod and H am ilton 1981; Trivers 1971). W h en one thinks about these payoffs in the currency o f “life tim e reproductive success,” we can see how the prison er’s dilem m a also illustrates how reciprocity m ight cause the evolution o f benefitdelivery devices via natural selection. Axelrod and Hamilton (1981) demonstrated that the iterated pris on er’s dilem m a provides a gam e-theoretic m odel for the evolution o f direct reciprocity. M echanisms th at deliver benefits to others via direct reciprocity (as modeled in the iterated prisoner’s dilemma) can evolve The E vo lu tio n o f G enerosity 391 by natural selection w hen the probability o f a successive round o f inter action betw een two individuals (that is, the probability that two indi viduals will interact again in th e future) exceeds the ratio o f the lifetim e fitness cost o f the benefit delivery to the donor divided by its lifetim e fitness value to the recipient. Results from m ore recen t models suggest th a t a bias to cooperate, even w hen one faces cues o f an in teraction being one-shot, should be expected to co-evolve w ith reciprocity. This is because m istaking a one-shot interaction for a repeated interaction is a less costly error than the reverse—th a t is, it is m uch m ore costly to m iss out on th e long-term benefits th a t can be obtained through repeated gains in trade than it is to be exploited in a single interaction (Delton et al. 2011). W ith a few p ossib le ex cep tio n s, recip ro city appears rela tively unim portan t for understanding cooperation in m ost non h u m an anim als (Clutton-Brock 2009; W est, Griffin, and Gardner 2007). However, reciprocity is arguably very im portant for understanding the evolution o f hum an cooperation because m uch o f hum an social inter action involves long-term relationships am ong nonrelatives (such as in the contexts o f hunting, foraging, territory defense, dwelling construc tion, food preparation, and child care). For exam ple, pooling risk and effort for hunting by sharing the spoils w ith others, on the condition th at recipients o f benefits at one point in tim e reciprocate in the future, is m uch m ore efficient than solitary hunting to provision only oneself and one’s close kin. This is because hunting is a relatively high-variance m ethod o f food acquisition: am ong ex tan t hunter-gatherer groups, individual probabilities o f failed hunts on any given day range from 40 percent to 96 percent (Gurven et al. 2012). Reciprocal cooperation in such circum stances can reduce or elim inate the variance in individ ual food availability, leading to direct benefits for recipients (through im m ediate acquisition o f food) and benefactors (by motivating recipro cal help at a later date). Although reciprocity can provide m utual direct benefits through gains in trade, it also exposes cooperators to the possibility o f exploi tation—that is, to interacting w ith individuals who will take benefits 3 92 social research w ithout reciprocating them at a later tim e (Cosmides 1989; Trivers 1971). The dangers o f exploitation m aybe particularly acute in humans, for hum ans possess zoologically unusual cognitive capabilities such as language, m ental tim e travel, the ability to infer oth ers’ goals and psychological states, and th e ability to in fer the social consequences o f their (and oth ers’) actions. These cognitive capacities m ight m ake it easier for humans to evolve m echanism s for exploiting other individu als’ cooperative dispositions. W ere such exploitive abilities to evolve, they would set the stage for evolutionary arm s races in w hich natural selection m ight conse quently favor the evolution o f m echanism s th at im p lem en t defen sive tactics for resisting or deterring exploitation. To the exten t th at n atu ral selection has indeed produced adaptations for exploitation and counter-exploitation in reciprocal interaction, all neurologically in tact hum ans can be expected to possess the full suite o f exploitive and counter-exploitive m echanism s. Such subsidiary cognitive m ech anism s m ight include perceptual systems th at identify likely reciprocators (for exam ple, kin detection; Lieberm an, Tooby, and Cosmides 2007) th a t in h ib it individuals from helping likely nonreciprocators (Cosmides 1989), and that m otivate the punishm ent or term ination o f interactions w ith nonreciprocators (West, Griffin, and Gardner 2007). Additional m echanism s m ight include capacities for rem em bering the outcom es o f cooperative in teraction s (for exam ple, classifying those actions with respect to w hether they violated social contracts), as well as m otivational systems for im pelling cooperation, reciprocal return o f benefits, and the punishm ent o f cheaters (Trivers 1971). It is worth keeping in m ind that the prospect th at a given bene fit-delivery system evolved via reciprocity (that is, by virtue o f the fact that benefit/cost ratio exceeded the probability o f repeat encoun ters betw een the actors in th e environm ent in w hich the m echanism evolved) tells us nothing, in and o f itself, about how th e resultan t cognitive m echanism s im plem ent their functions. A reciprocity-based benefit-delivery system could (theoretically) simply entail, for instance, a cognitive system th a t com pares on e’s own language or accen t to The E vo lu tio n o f G e n ero sity 393 the language or accent o f a potential reciprocity partner— since facil ity w ith the sam e language was likely very highly correlated w ith geographic locale, and thus, the likelihood o f m eeting again (Pagel and Mace 2004)— and th at m otivates benefit-delivery toward individuals whom one determ ines to speak in a language or w ith an accent th at is suitably sim ilar to one’s own (Nettle and Dunbar 1997). It is the jo b o f evolutionary behavioral scientists to em pirically determ ine the circuit logic that governs the operations o f these systems; the theories o f social evolution do not them selves prescribe how they should be cognitively or neurally instantiated (Scott-Philips 2007). OCCUPYING THE C O G N ITIVE NICHE FAVORS THE EVO LUTIO N OF INDIRECT RECIPROCITY Tooby and DeVore (1987) proposed th at hum ans evolved to exploit a “cognitive n ic h e ”— th at is, a way o f life for w hich natural selection resulted in problem -solving m echanism s th at enable organism s to form ulate in real tim e (rather than over evolutionary time) novel strate gies for surm ounting the fixed defenses o f other organisms (for exam ple, the toxins in otherw ise edible plants or the defensive weaponry o f potentially edible animals), and in so doing, extract resources from them . Pinker (2010), in particular, proposed th at hum ans succeed in exploiting the cognitive niche due to a suite o f zoologically exceptional cognitive adaptations that include technological problem-solving and gram m atical language. W ith these adaptations in place, new adaptive space opens up in w hich new variations on reciprocity can plausibly evolve. For exam ple, once language has evolved, in form atio n about third parties’ previous cooperative behaviors can be efficiently trans m itted orally from someone who has acquired direct (or even indirect) knowledge bearing on this issue (“Maggie is ju st so stingy . . . ”) to third parties who lack such knowledge. If people subsequently were to come to possess, via natural selection, psychological m echanism s that m oti vated them to adjust th eir cooperative behavior on the basis o f such reputational inform ation, they could avoid the costs associated w ith 394 social research providing benefits to nonreciprocators. Indeed, people do use thirdperson inform ation to preferentially cooperate w ith those who have cooperated w ith others, but only w hen they lack first-person experi ence (once first-person experience is acquired, third-party inform ation becom es irrelevant; Krasnow et al. 2012). This sets the stage for the evolution o f so-called indirect reciprocity (Nowalc and Sigmund 1998), w hich results in individuals who appear as if they are m otivated to reward individuals for their previous cooperative behavior toward other b eneficiaries—w hen w hat they are really doing is stream lining their own efforts to b en efit from reciprocal in teraction by directing ben e fits toward individuals who have proven them selves to be trustworthy reciprocators. GROUP AUGMENTATION In som e anim al species, m em bers o f stable social groups provide care (that is, deliver benefits) to offspring th at are n eith er th eir own offspring nor th e offspring o f close genetic relatives (Clutton-Brock 2002). Although such behavior at first seem s puzzling, a closer look at the consequences o f reproductive support reveal several routes by w hich the genes th at build the m echanism s th at m otivate such behav iors could be favored by natural selection. First, providing reproductive support can increase helpers’ direct fitness by increasing their chances o f survival (Grinnell, Packer, and Pusey 1995) or yielding allies if they m igrate from their natal groups to begin th eir reproductive careers else w here (Clutton-Brock 2002). Second, by contributing to group survival, nonreproductive m em bers can increase the likelihood th at helpers will be available to aid th eir own reproductive efforts if they should ever becom e one o f the group’s reproductive m em bers (Clutton-Brock 2002). H um ans are n o t coop erativ e breed ers, o f cou rse; an cestral hum an societies are n ot characterized by castes o f nonreproductive helpers. Even so, group size its e lf m ight nevertheless have b een an im p o rtan t source o f d irect fitn ess b en efits for an cestral hum ans. For exam ple, studies w ith non h um an anim als suggest increases in group size can in crease th e fitn ess o f all group m em bers because The E vo lu tio n o f G enerosity 395 larger groups can be b etter at obtaining (and retaining) food (CluttonBrock 2002), spotting and defending against predators (Clutton-Brock 2002), defending breeding sites against takeovers (Port, Kappeler, and Joh n ston e 2011), and rearing offspring. Because o f the direct benefits to individuals in the group th a t m ight accrue simply by virtue o f the group’s expanding, it can b e b en eficia l for helpers to provide care for unrelated offspring in order to help in increasing the size o f the group. In addition to direct benefits from so-called group augm enta tion, provisioning b en efits to young can also be repaid via “delayed reciprocity,” or benefits provided to the helper by offspring who have reached adulthood. Although th e im portance o f group augm entation as an evolutionary route to th e evolution o f h u m an s’ cooperative instincts is currently unknow n, it has received less atten tion th an it m erits (Port, Kappeler, and Joh n ston e 2011). NATURAL SELECTION O F BENEFIT-DELIVERY DEVICES THROUGH INDIRECT FITNESS BENEFITS The classical Darwinian notion o f natural selection has seen only one m ajor th eoretical refinem en t. This refinem en t resulted from efforts by biologists to understand how traits that reduce their bearers’ direct reproductive success can evolve. The existence o f sterile worker castes, for exam ple, along w ith less extrem e instances o f organisms that pay fitness costs in order to provide fitness benefits to others, caused evolu tionists to eventually realize that the scope o f natural selection was broader than they had originally realized: natural selection’s partiality for a gene is determ ined n o t only by how that gene affects the repro ductive success o f the individual organism in w hich it resides, but also by how it affects the reproductive success o f replicas o f itse lf that are locked inside other organism s— namely, genetic relatives o f the donor individual. Decades later, Hamilton (1964) showed m athem atically that natural selection builds com plex functional design by favoring m utant genes that cause traits th at boost those genes’ inclusive fitness, w hich is the sum o f direct fitness (a genetic variant’s success in creating replicas o f itself) and indirect fitness (its success in assisting other copies o f itse lf— 396 social research located inside offspring and siblings and cousins and other relatives— to replicate). H am ilton ’s m a jo r in sig h t— la ter dubbed H am ilton’s rule— was th a t a new genetic m utant th a t reduces its b earers’ direct reproduc tive success can evolve by natural selection if the lifetim e reproductive b en efit b it confers to all recipients, discounted by the average degree o f relatedness r betw een th e actor and all recipients (which is really shorthand for “the probability that the recipients o f the benefit share the new genetic variant that is responsible for causing the benefit-delive iy ”), exceeds the lifetim e reproductive cost c that the trait imposes upon the actor— th a t is, w hen rb - c > 0. Traits th at evolve by adher ing to Ham ilton’s rule can be said to have evolved through “kin selec tion ,” as com m on ancestry (kinship) is the m ost com m on reason why two individuals share a genetic variant. Because they evolve through the accum ulation o f genes th a t cause organisms to provide benefits for other individuals th at the donors could otherwise use to pursue their own reproductive agendas (with benefits and costs referring to lifetime fitness consequences), kin-selected traits can rightly be said to evolve through an “altruistic” pathway o f natural selection (West, Griffin, and Gardner 2007). Adaptations for Parental Care as Altruism Devices Some o f the clearest illustrations o f altruistically designed biological devices are adaptations for parental care (Dawkins 1979, 1976), and here we dwell on them in some detail. “Parental care” refers to the full suite o f anatom ical, physiological, and behavioral adaptations whose function is to cause parents to invest in the fitness o f th eir offspring (Clutton-Brock 1991). For m any biologists who study parental care, it seem s intuitively wrong to th in k o f adaptations for parental care as “altruistic.” They often argue that w hen an organism provides parental care it is simply pursuing th e m axim ization o f its own direct fitness, w ith d irect fitn ess being defined as th e num ber o f the organism ’s offspring that reach reproductive maturity. Nevertheless, evolutionary geneticists have good reasons to think th at the production o f zygotes The E vo lu tio n o f G enerosity 397 (the cell th a t results from th e u nion o f egg and sperm) is a b etter measure o f an individual’s fitness than is the num ber o f their offspring th a t m ake it to m aturity (Hunt and Hodgson 2010). As a side benefit, we find it is clarifying to count fitness in zygotes rather than in sexu ally m ature adults because it is a less parento-centric view o f sexual reproduction. Most organism s do n ot provide any parental care, and relatively few provide m ore than hum ans do. Consequently, one should not be surprised if adaptations for parental care require a special kind o f biological explanation. W e th in k th at explanation is the altruistic route to com plex functional design. In this way o f thinking, m am m alian lactation is an iconic exam ple o f an altruistically designed benefit-delivery device (Oftedal 2012). Human m others, for instance, whose infants (in traditional societies and, one presumes, ancestral societies) feed exclusively on breast m ilk, m ust increase th eir caloric intake by 670 kilocalories per day because o f the high m etabolic costs o f m ilk production (Dewey 1997). In addi tion, there are opportunity costs: breastfeeding stimulates the produc tion o f prolactin, a horm one that both stim ulates m ilk production and prevents the release o f the horm ones (called gonadotropins) th at cause w om en’s m enstrual cycles to resume. Thus, while hum an infants are nutritionally dependent on th eir m o th er’s m ilk (a period th at lasts betw een 2 and 3 years am ong w om en from nonindustrial societies; Sellen 2001), wom en are typically not ovulating, w hich is to say, they are delaying the pursuit o f increasing th eir direct reproductive success. Moreover, it is insufficient m erely to produce m ilk: m am m alian m others also m ust have a behavioral repertoire that makes them both able and w illing to tran sfer th at m ilk to th eir offspring. There is an im portant but often underappreciated behavioral com ponent to success in breastfeeding, which includes learning to read infants’ signals that they are ready to eat, specialized learning systems that stim ulate m ilk let-down in response to in fan ts’ cries, developing skill with stim ulating babies who are too sleepy to eat and soothing babies who are too fussy to eat, and others (Mulford 1992). And ideally, all o f this learning should happen very soon after the in fan t is born. For this reason, natural selec 398 social research tion, through the altruistic design route, plausibly led to the evolution o f specialized learning m echanism s, physically instantiated through a com plex netw ork o f neural and endocrine pathways, whose function is to enable m others to becom e proficient at breastfeeding quickly. Milk delivery is only one elem ent o f parents’ food provisions for their offspring (in modern and traditional societies alike, parents subsi dize th eir offspring’s caloric intake throughout adolescence; Kaplan et al. 2000), and food provision itse lf is m erely the tip o f the parental care iceberg. For exam ple, the anthropologist Melvin Konner (2010) has enum erated many additional evolved functions o f hum an motherhood. These include tem perature hom eostasis; protection from predators, enem ies, and organisms such as insects, scorpions, and snakes; transfer o f specific im m unity; and th e nongenetic transm ission o f behavioral and psychological dispositions. Parents also invest in th eir children’s reproductive success by helping them to acquire the hum an capital— specialized storehouses o f know ledge, skill, or expertise— th at will m ake them valuable to potential m ates, potential friends and allies, and m em bers o f the wider com m unity (Geary 2010). The cognitive m echa nism s th at enable m others (and fathers) to provide these benefits to offspring require natural selection explanations every b it as m uch as adaptations for food delivery do. Kin Discrimination Systems The high degree o f relatedness betw een m others and th eir offspring m eans that it is relatively easy for natural selection to build altruistic adaptations for m aternal care, but another im portant factor is the high availability o f so-called kin discrim ination cues, w hich enable altruistic genes to “know ” (in a purely m etaphorical sense) w here to direct their help. Kin discrim ination— the ability to recognize (nonconsciously, o f course) one’s own relatives and then regulate behavior in response to th at recognition— is a feature o f hum an nature that is so thoroughly taken for granted (because language enables us to label certain individ uals as our fathers, m others, siblings, grandparents, and so forth) that we fail to recognize that altruistically designed systems for caring— in The E vo lu tio n o f G e n ero sity 399 hum ans and m any other species— often rely deeply on a netw ork of kin-discrim ination cues to regulate their operation. By relying on such cues, evolving altruistic systems can reduce the costs o f parental care per unit o f benefit transferred to offspring, which, per H am ilton’s rule, enhances evolvability (West, Griffin, and Gardner 2007). Many cues for offspring recognition are available to m others. As a soon-to-be-born m am m al descends through its m oth er’s b irth canal, for instance, th e stretch o f th e m uscle fibers th at line th e uterin e wall send a volley o f neural signals to the brain th at stim ulate the pituitary gland to release prolactin and oxytocin. These horm ones, in turn, not only stim ulate the further progress o f labor and delivery, but also the activation o f m ilk production and the b ra in ’s behavioral parenting circuits (Russell and Leng 1998). After infants are born, hum an m oth ers alm ost instantaneously appear to begin m aking use o f visual, audi tory, and even olfactory cues to th eir offspring (some o f w hich can be updated as children age and develop) for the purpose o f kin recogni tion (Tal and Lieberm an 2007). It is also likely th at hum ans, like m any oth er m am m als (and birds and fish), com e to recognize offspring on the basis o f co-residence— perhaps m ediated by cognitive system s th at im plem ent the logic “any young in m y nest are m in e” (Penn and From m en 2010, 64). In discussing altru ism thus far, we have focused m ainly on m other-child relation sh ip s, but a ltru istic benefit-delivery systems have very likely also evolved to regulate benefit-deliveiy from fathers, siblings, grandparents, aunts and u ncles, and o th er relatives (Sear and Mace 2008; Gurven et al. 2012). In m ost animals, m others have a distinct advantage over fathers and other relatives in offspring recogni tion because o f their heavy physiological investm ents in the growth and developm ent o f the offspring following egg fertilization. These invest m ents m ake available to m others (but not fathers and other kin) a vari ety o f kin discrim ination cues that m aternal altruistic benefit-deliveiy systems can put to use. Although some evidence suggests that fathers assess kinship by relying on visual or olfactory cues o f genetic sim ilar ity (Alvergne, Fauire, and Raymond 2009), it is also possible th at fathers 400 social research possess com putational neurocircuitiy th at solves offspring-recognition problem s in a different way. Holding aside the w onders o f m odern fertility m edicine, m en cannot be the fathers o f the children o f wom en w ith w hom they did not have sex, so a reasonable first step for simplifying the offspring recogni tion problem would be for m en to rule out o f further consideration all w om en w ith w hom they have never had sex. Second, because ances tral m en cannot be fathers o f children who are not also the children o f wom en w ith w hom they had sex, they m ight also observe the relations betw een the wom en with w hom they have had sex and the young chil dren in their midst. Young children who receive m aternal care from a wom an w ith w hom the m an had sex approxim ately 10 m onths prior to the in fan ts’ births are likely (holding aside other considerations such as the w om an’s likelihood o f having had sex w ith oth er m en, w hich m ight also be relevant) to be the m an’s children (Lieberman, Tooby, and Cosmides 2007; Tal and Lieberm an 2007). Sim ilarly, child ren apparently recognize th e ir siblings based largely on environm ental cues acquired during childhood experience, including the num ber o f years o f co-residence and (for older siblings) w atching one’s own m other provide m aternal care to another individ ual (Tal and Lieberm an 2007; Lieberman, Tooby, and Cosmides 2007). DOES GROUP SELECTION EXPLAIN ADAPTATIONS FOR BENEFIT DELIVERY? Group selection is the idea th a t natural selection can w ork by en h an c ing th e fitness o f groups o f individuals rath er th an acting exclusively on individuals. In th e sc ie n tific lite ra tu re, som e sch olars p resen t group selection as an alternative to standard inclusive fitness m axi m ization m odels o f n atu ral selection in order to explain the evolu tion o f m echanism s for hum an b en efit delivery (Fehr and Fischbacher 2 0 0 3 ; Sober and W ilson 2011). C urrent group se lectio n th eo rists recog n ize th a t in clu sive fitn ess m odels are n ecessary in g en eral and th a t th ey ex p lain m an y coop erativ e p h en o m en a, b u t th ese scholars also m ain tain th a t inclusive fitn ess theory can not account The E vo lu tio n o f G e n ero sity 401 fo r all o f th e types o f coop eration found in hum ans. For in stan ce, group se lectio n has b een invoked to exp lain coop eration in oneshot in teraction s (in teraction s th a t w ill n o t be repeated and h en ce can not be reciprocal; Gintis 2000), costly punishm ent in public goods scenarios (Fehr and G achter 2002), costly punishm ent by third-party w itnesses o f unfairness (Fehr and Fischbacher 2004), and even costly punishm ent o f an individual who has directly harm ed the punisher (Fehr and Fischbacher 2003). In all o f these cases, proponents o f group selection models argue that the behaviors in question provide benefits to others (for example, punishm ent deterring a transgressor from harm ing a stranger in the future) at a n et cost to the individual perform ing them (for exam ple, pu n ish m en t is in h eren tly costly to th e pu nisher as it takes tim e, energy, and could incite retaliation) and thus cannot evolve through the standard Darwinian design pathways. Importantly, group selection proponents also tend to be skeptical o f claims that behaviors like these would have been adaptive for individuals under ancestral (though not modern) conditions, or that they would reveal them selves to be adap tive even today if the fitness benefits were reckoned over the course o f a lifetim e (rather than over the course o f a one-hour laboratory session), or th a t th eir salutary effects on others are by-products rath er th an evolved functions (Chudek, Zhao, and Henrich in press). Space lim ita tions prevent form al consideration o f these specific em pirical claim s, so we lim it our attention here to describing the various ways in which group selection is invoked and some o f the lim itations o f these usages. Types o f Group Selection It is im portant to note th a t group selection is n ot a singular, form al theory. Rather, the term has been applied to several different processes th at can usefully be classified as exam ples o f either “old” group selec tion or “new ” group selection (West, El Mouden, and Gardner 2011). Old group selection models propose th at group-level adaptations would result from d ifferen tial survival am ong groups—th a t is, th a t traits would be selected to m axim ize group success (West, El Mouden, and 402 social research Gardner 2011). For exam ple, Wynne-Edwards (1962) argued that groups o f organisms th at sought solely to m axim ize their own individual inter ests would exhaust ecological resources and therefore face extinction, whereas groups o f organisms that exercised restraint in pursuing their individual interests would n ot deplete th eir resources, and thus would be m ore likely to survive. Through a persistent process o f differential group success on th e basis o f individual restrain t, Wynne-Edwards argued, behaviors could evolve th at ben efitted the group as a whole even if costly to the individual. Old group selection models therefore rely on the proposition that groups o f individuals, and not m erely indi viduals, can be the vehicles on which natural selection acts. The theoretical and em pirical w ork th at em erged in the wake o f Wynne-Edwards’s proposal showed th at old group selection, w hile possible in theory, could only w ork under a very narrow range o f condi tions, and thus was veiy likely to be unim portant in explaining adap tation (and basically im possible in hum ans; W illiam s 1966; W est, El Mouden, and Gardner 2011). For exam ple, group-level adaptations can be favored by natural selection w hen all o f the individual organisms w ithin a group are genetic clones, w hich can occur w hen relatedness am ong group m em bers is high (that is, m igration is essentially zero) and there is com plete suppression o f reproductive com petition w ithin groups (West, El Mouden, and Gardner 2011; Gardner and Grafen 2009). Because these conditions are rarely fulfilled in nature— and not at all in the case o f hum ans—group-level adaptation is rarely invoked inten tionally in the contem porary literature, although confusion arising from “new ” group selection models does som etim es result in research ers rehashing some old group selection ideas (West, El Mouden, and Gardner 2011). Unlike old group selection models, “new ” group selection models do n ot focus on group-level adaptations. Rather, new group selection models propose th at natural selection operates at m ultiple levels, and that traits can be selected for if their benefits at the level o f the group (between-group level) outweigh the benefits at the level o f the individ ual (within-group level) (Sober and W ilson 2011, 1998). Some models The E vo lu tio n o f G enerosity 403 also posit that direct com petition betw een groups results in selection for cooperative behaviors, such as w hen groups battle for territories (that is, groups w ith a g reater num ber o f cooperators are expected to outcom pete groups w ith fewer cooperators; W est, El Mouden, and Gardner 2011). O ther m odels th at can be categorized as new group selection models incorporate culture to explain differential success o f groups, w hereby groups th a t express a particular cultural trait outcom pete groups th at do not (Boyd and Richerson 2005; W est, El Mouden, and Gardner 2011). These various new group selection models, collec tively, are featured prom inently in the current literature on the evolu tion o f benefit delivery in humans. Is Group Selection Useful? Group selection m odels can provide a ten able selectio n ist logic by w hich some adaptations for ben efit delivery evolve (Gardner in press). So why do m ost evolutionary biologists resist using group selection m odels? There are four reasons. First, group selection models do not provide any explanatory pow er above and beyond the power th at is already built into standard inclusive fitness theory (that is, accounting for direct and ind irect benefits). More strongly, new group selection models already are incorporated into standard inclusive fitness theory— though th ey rely on d ifferen t m ath em atical expressions o f n atu ral selection, they yield identical predictions (Gardner in press; Gardner and Grafen 2009). Second, despite many claims to the contrary, no one has proposed an em pirical or theoretical exam ple o f a benefit-delivery system that can be shown to evolve by m ulti-level selection and th at cannot also be shown to evolve through standard inclusive fitness considerations (for a list o f examples, see table 5 o f W est, El Mouden, and Gardner 2011). The converse is not true: som e benefit-deliveiy systems th at are explica ble w ith an inclusive fitness m axim ization approach to understanding natural selection cannot be explained using the analytical tools asso ciated w ith m ulti-level selection. Third, the m athem atics required to analyze the evolution o f biological phenom ena w ith group selection 404 social research models tends to be m uch m ore unwieldy than the m ath th at is required to analyze them w ith inclusive fitness models. Fourth, and perhaps m ost im portant, even w hen using group selectionist models to explain the evolution o f benefit-delivery systems, one reaches the conclusion th a t organism s still evolve in such a way as to pursue th eir inclusive fitness interests. That is, even w hen one uses the (often) cum bersom e group selection approach to modeling the selection dynamics th at lead to benefit-deliveiy devices, those devices still reside in individuals who w ill appear as i f they are designed to optimize their inclusive fitness. Group selection may provide an alter native view o f selection, but it does not lead to new understandings o f what results from natural selection. This is one source o f the elegance o f inclusive fitness theory: it seamlessly bridges the process o f natural selection (genes acting in th e world to create phenotypes th at boost th eir own rates o f replication will increase in the population) and the product (individual organism s th a t appear designed to pursue the enhancem ent o f their own inclusive fitness). Group selection views do not unite process and product in such an elegant fashion (Gardner in press). CONCLUSION Human generosity is not an illusion, and m uch o f the generosity that we see betw een individuals and w ithin societies today is motivated by biological systems that plausibly evolved by natural selection through the causal pathways we have outlined here. But is evolution the only gam e in town for explaining hum an generosity? Far from it. Much o f th e generosity we see in th e contem porary world is probably caused not by biological systems designed for generosity acting alone. Instead, these m echanism s often in tera ct w ith unique innovations th at have arisen in the m odern world— for exam ple, laws, charitable organiza tions, taxation, and social insurance—that were intentionally designed to goad humans into greater generosity than could be leveraged on the basis o f naturally selected benefit-delivery devices alone. Some o f these innovations m ight n ot even require the action o f naturally selected The E vo lu tio n o f G enerosity 405 benefit-delivery m echanism s at all. All they m ight require, instead, is for hum ans to apply th eir capacities for abstract reasoning (Singer 1981) and their evolved inclinations to avoid sticks (such as the form al penalties associated w ith tax dodging or failing to return found prop erty; W est 2003; W ebber and Wildavsky 1986), pursue carrots (as soci eties grow larger, and as com m unication goes from oral to w ritten to electronic, the potential reputational benefits o f generosity increase exponentially), and follow fashionable social trends (note the rise o f charitable voluntary associations in V ictorian England; H im m elfarb 1991). A com plete understanding o f hum an generosity in the modern world, therefore, w ill require not only the careful application o f the insights o f evolutionary science, but also a careful inspection o f the insights that can com e from histoiy, political science, econom ics, and the other social sciences. 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