Downloaded by guest on October 1, 2021 www.pnas.org/cgi/doi/10.1073/pnas.1618655114 Chagnon A. Napoleon brothers between mate competition and conflict parent–offspring of evidence Yanomam the among Cross-cousin aetofpigconflict parent–offspring marriage cross-cousin prescriptions. marriage cross-cousin mate of controls origins who the over and how conflicts choice of underlie importance reciprocity evolutionary and the kinship into This insights rules. provides marriage cross-cousin study bilateral drive gen- may subsequent to they forward erations, carried are relationships sib- these opposite-sex If lings. between mates, alliances over forging compete simultaneously who while same-sex esca- between may com- conflict late mate over control local parental that with strate- combined posit norms petition mating cultural We by marriage. optimal reinforced cross-cousin is over prescribing marriages of siblings These control Parental among do. parents gies. and siblings between offspring conflicts same-sex suggest and or outcomes suffer parents, fitness but their asymmetric relatives they, marry their when siblings when costs opposite-sex or not when benefit children to but their seem individuals relatives Therefore, do. marry siblings same-sex siblings opposite-sex their (iv (iii and depression; grandchildren; inbreeding from that suffer find spring we fit- kin, the close Yanomam marry the (i analyze individuals When among we Amazon. relatives the Here marrying from exchanges. of unclear consequences these is ness it from —but benefits opposite-sex parent’s who a cross-cousins—marriage of involve child the often with most insti- of exchanges the groups Fox) Such among Robin concerns and kin. partners Chapais often reproductive Bernard of societies by exchange reviewed traditional 2016; tutionalized 10, many November review in for Marriage (sent 2016 21, December Chagnon, A. Napoleon by Contributed 68588-0368 a rd’ aiya rd rc) n mrig ycpue in capture” by “marriage Yanomam and the price), a like to bride societies a egalitarian the as by called family rendered service—sometimes bride’s service (bride measured the service as service—is males bride groom than prices, value bride higher value have of by exchange to properties high likely mar- basic have are spouses The the [females the (10). over (i) daughters are influence marriages and strong arranged For sons a soci- their (9). have gathering of offspring parents and riages their that hunting of found of survey eties choices cross-cultural mate consider- a exert the example, often over parents control because able unique is mating Human Parent–Offspring Generates Conflict Choice Mate of Control Parental eventu- are transactions these 8). that (7, ensure reciprocated to ally way a rel- be accord close may In with atives 6). offspring recipro- (5, exchanging spouses characterizations, to these future family with or support receiving political the through offering obligates cate whereby marriage parties viewed in between have arrangement someone others access reciprocal whereas a sexual (2–4) as for coalitions it competition male anthropolo- by a females as notable to marriage Several depicted built. which have are gists upon structures foundation social families—the human form relationships these B eateto nhoooy nvriyo isui ouba O62114;and 65211-1440; MO Columbia, Missouri, of University Anthropology, of Department ohhsad n ie aesihl oe etlt;(ii fertility; lower slightly have wives and husbands both ) xeddknadnni h eoei-as() Together (1). in-laws become both who between nonkin ties and kin establish extended partners married between onds | inbreeding ilns seilybohr,bnfi when benefit brothers, especially siblings, ) | Yanomam a,1,2 oetF Lynch F. 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Reviewers: and the researched paper M.V.F. the and R.H. researched and M.K.S. study; paper; the the wrote and data, analyzed itbtenteitrsso aet n fsrn.Trivers’ offspring. and parents of interests the between flict (9). norm character or moral rule cultural a a social achieve become to mere they ultimately siblings as and before out opposite-sex regularities start and spouse’s] may patterns one’s practices These [or outgrowth children. own natural exchange the one’s is using marriage mar- Cross-cousin of prescriptive mar- 14). 13, anthropologists—cross-cousin common (5, by and riage described widespread practice most riage the would we at siblings, same-sex arrive between taboos exchanges and exclude rules cultural to mate If began over (9). control to reciprocity contingent parental likely and of is choice combination system a This from service.) politi- emerged bride for have or offspring transac- price, of marriages bride reciprocal exchanges support, often arranged always cal are of and not offspring structures of are tions basic “exchanges” most (Marriage the (5). of reci- one on forms based (12). marriages spouses the of of history families An the long between 11). a mitochon- procity 9, suggests using practices (1, DNA marriage drial (8)] hunter-gatherer altruism con- of by reciprocal driven analysis [i.e., often in- are and become reciprocity that spouse power; ties tingent and long-lasting sibling) political maintain or who and parent and laws (e.g., older social arranger usually more the are being (iv) have arrangers are the marriages typically (iii) whose therefore kin; those close and are arranging arranged the doing uals uhrcnrbtos ...cletdtedt;RFL eindadpromdresearch, performed and designed R.F.L. data; the collected N.A.C. contributions: Author owo orsodnesol eadesd mi:[email protected]. Email: addressed. be should correspondence whom To work. this to equally contributed R.F.L. and N.A.C. rlo araeadcmeiinbtensm-e siblings. same-sex between competition and con- marriage parental owe of through trol cousins conflict parent–offspring parallel to marrying origin their against taboos pre- and lower marriage scriptions have cross-cousin that unions suggest these findings These by fitness. produced offspring the and and Meanwhile, children individuals. spouses related respective closely more their marry when sisters achieve outcomes brothers and fitness parents higher fitness that Amazon—shows Yanomam the the the of in in ety analysis marriages An of resolved. pre- consequences been marriage this not of have function scription adaptive and origin the preferred investi- gation, intense common Despite cultures. most a across arrangement the of marriage offspring is the sibling) with opposite-sex parent’s marriage (i.e., marriage Cross-cousin Significance aetliflec vrmrig sepce ognrt con- generate to expected is marriage over influence Parental groups kin daughters—by children—especially of Exchanges b eateto nhoooy nvriyo ersa icl,NE Lincoln, Nebraska, of University Anthropology, of Department b n akV Flinn V. 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ANTHROPOLOGY PNAS PLUS theory of parent–offspring conflict (15) provides a framework (11). During the period of N.A.C.’s data collection (1964–1988) for understanding these tensions. Because mate preferences of the Yanomamo¨ relied on gardens where they grew plantains, offspring may not maximize the fitness of their parents, con- bananas, and manioc (26) and also on hunting (27). It is esti- flict is expected. For example, children are more likely to value mated that the Yanomamo¨ numbered approximately 25,000 peo- signs of genetic quality of a potential spouse, whereas parents ple across 250 villages during this period (11). The Yanomamo¨ are more likely to value the family background of a poten- are in many ways an ideal society for answering questions about tial in-law (16). Parents are also expected to be more toler- human evolution because they share many traits that were likely ant of inbreeding (Inbreeding) than their offspring. These dis- to have been common in ancestral human populations, includ- agreements are the outcome of inclusive fitness (7) differences ing (28), agnatic descent groups (14), patrilocality (29), between parents and offspring and parents are expected to (14) [in the standard cross-cultural sample (SCCS), benefit more when their offspring marry relatives (to whom the a widely used worldwide cross-cultural sample, 17% of societies parents are more closely related). These asymmetric fitness inter- are matrilineal compared with 41% that were classified as patri- ests are also expected to generate conflict between siblings. This lineal], lineage (14), and prescriptive bilateral cross- is because parents are equally related to all of their offspring (30, 31) arranged by older male kin (10). (For and are therefore expected to value and hence invest in them primary source ethnographies on Yanomamo¨ economic, social all equally, whereas offspring are fully related to themselves but and political life see refs. 2 and 32–35. For additional details only related by a half, or a quarter, to their full and half siblings, on Yanomamo¨ social organization see Inbreeding, Yanomamo¨ respectively (15). Kinship and Politics.) The Yanomamo¨ practice prescriptive bilateral cross-cousin Mate Competition Between Siblings. Local mate competition marriage. This means that males are expected to marry their (Inbreeding Local Mate Competition) between siblings is com- female cross-cousins (i.e., the daughters of their parent’s mon in a variety of taxa (17), and fights to the death over mating opposite-sex siblings). This practice is so embedded in the can occur between same-sex siblings (18, 19). In many species of Yanomamo¨ culture that the words for female cross-cousin and insect these conflicts are resolved by the production of female- wife are both suaboya¨ and, reciprocally, the words for male cross- biased sex ratios (17, 20). In mammals, local mate competition cousin and husband are both hearoya (36). If a cross-cousin is may result in sex-biased dispersal—one sex remains in its natal not available, an individual is still required to marry someone territory and the other disperses (Inbreeding Sex-Biased Disper- outside of his or her patrilineage. These rules are often manipu- sal) (21–23). Sex-biased dispersal provides a way to balance the lated when it is difficult to find a wife, however, which sometimes costs of inbreeding load (24) and local mate competition with the leads to conflict. Because prescriptive marriage rules among the cooperative activities among siblings that lead to local resource Yanomamo¨ require that marriages are between individuals in enhancement (25). the same generation, it is common for a father to attempt to Once parental control over mating evolved in humans, how- manipulate genealogical relationships such as by reclassifying a ever, conflicts and cooperation among siblings could also be “niece” as a “sister” so that his sons may now marry her daugh- generated through parent–offspring conflict. This is because ters (37). The Yanomamo¨ are normatively patrilocal (the men marriage exchanges that are under the control of parents are stay in their natal village and the women move to the village of likely to produce uneven fitness benefits across offspring. These their husbands), but men who have been promised a wife may unequal outcomes are, in turn, expected to induce sibling com- have an obligation to perform for their father-in- petition over spouses. In polygynous and patrilocal societies like law although the obligation is less for older males who become the Yanomamo,¨ brothers in particular are expected to vie for polygynous. This bride service, which may last for several years, wives. At the same time, marriage exchanges may produce bene- consists primarily of hunting and providing meat to the house- fits for opposite-sex siblings (e.g., a brother receives a wife that is hold of his father-in-law (36). exchanged for his sister). Overall, parental control over marriage Yanomamo¨ marriages are typically arranged either by parents generates parent–offspring conflict over mating that can lead to or by the eldest adult male members of local patrilineal descent asymmetric fitness consequences for offspring. These discordant groups (36). Fathers and brothers exert the most control over outcomes can in turn produce antagonistic interests between the marriages of their respective daughters and sisters whom same-sex siblings while providing opportunities for opposite-sex they attempt to exchange for female cross-cousins (38). Girls are siblings to build cooperative alliances. first promised in marriage at a very young age—occasionally at birth—and may be pledged to multiple individuals (2). Young Predictions. In this study, we used genealogical data from the girls marry and begin living with their husbands before or soon Yanomamo,¨ a traditional society of South American horticul- after reaching puberty. Members of allied villages are usually turalists, to analyze the effect that spousal relatedness has on reluctant to cede women to their partner villages due to concerns the reproductive success of offspring, spouses, parents, and sib- that the latter might not reciprocate as promised (6). “Recipro- lings. We test the following predictions (P): P1, offspring of cal” marriage exchanges are therefore fraught with nervousness more related parents will have fewer children due to inbreeding on both sides and the parties usually enter into these agreements depression; P2, spouses who are more closely related will have with caution (37). The marriage patterns observed in Yanomamo¨ fewer children due to mechanisms to avoid incest; P3, parents villages appear to be the outcomes of strategies that seek to will have more grandchildren when their children marry close rel- ensure that men will receive brides back in return for the daugh- atives because close kin are expected to be more likely to recip- ters and sisters that they give away. For additional details on rocate promised spousal exchanges and engage in other forms Yanomamo¨ marriage see Inbreeding, Yanomamo¨ Marriages. of cooperation; and P4, siblings will have more children when their opposite-sex siblings marry relatives and fewer children Results when their same-sex siblings do. This is because siblings of the We measured fitness as (i) the total number of children ever born same sex, especially brothers, will compete over marriage part- (Table 1 and Tables S1 and S2), (ii) grandchildren (Table 1), ners whereas opposite-sex siblings, especially sisters, will increase (iii) number of children who survived to age 15 y (Table S1), opportunities to marry relatives. and (iv) number of spouses (Table S2). Table 1 and Table S1 show the impact of spousal relatedness (three groups bracketed The Yanomamo.¨ At the time these data were collected (Methods, by their coefficient of relatedness; Methods)(Fig. S1) on the Data Collection), the Yanomamo¨ were a sovereign, indigenous fitness outcomes of males and females for each of the follow- tribal population living in the northern Amazon along the bor- ing relationships: (i) parent’s relatedness on offspring reproduc- der between Brazil and Venezuela. Until the 1950s there is no tion, (ii) spousal relatedness on the reproduction of their respec- record of any sustained contact with a modern western society tive husbands or wives, (iii) offspring relatedness on parental

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Parent’s nificantly Their on either Relatedness of Offspring P3: offspring the of have survival not ( did wives the and or on analyzed husbands the also effect of was survival detectable y the 15 any on age relatives to marrying children of couple’s groups impact most-related The detectable wives. and no of were intermediate- hus- there have the their Meanwhile between they to 2). differences Fig. related that and most 1 show were (Table who did bands women those but than from children related differ more significantly intermediately not were did least who repro- husbands were her their who on women to effect that related revealed significant contrasts overall to Pairwise an relatedness duction. had wife’s but A also wives 2). husband Fig. their her and and 1 intermediate- to (Table the groups related between most-related difference most significant and no showed those intermediately than offspring were fewer significantly who had wives least their were to who husbands related that between revealed close reproduction contrasts sig- Pairwise in marry wife groups. differences his who to overall relatedness wives predicted husband’s nificantly and A ambiguous. husbands more are of kin Wives. outcomes and Husbands fitness of The Reproduction the on Relatedness Spousal P2: S2 (Fig. y 15 sig- age had to also S1 survived related Table who closely offspring more fewer were The nificantly 1). who Fig. parents and of 1 the children (Table most- between groups difference most-related and significant and intermediate-related no intermediate- showed the but sur- groups both more related significantly than had offspring the parents that viving least-related signif- showed the had contrasts of related Pairwise children offspring. closely total more fewer were icantly who parents of Reproduction. daughters Offspring on Relatedness Parental P1: brothers their of reproduction sisters. the and on relatedness produced), sibling (iv) grandchildren and of number in (measured reproduction hgo tal. et Chagnon ). Overall high to Medium high to Low o omedium to Low Sisters Parents generations three across relatives marriage marrying of of Consanguinity outcomes Fitness 1. Table Overall medium to Low eimt high to Medium high to Low o ohigh to Low medium to Low o ohigh to Low medium to Low Spouses Overall high to Medium Brothers Offspring high to Medium Overall high to Medium high to Low medium to Low Overall al S1 Table d ¯ stema ifrnebtentegroups, the between difference mean the is and i.S3). Fig. ANOVA ANOVA ANOVA ANOVA ANOVA d d d d d d d d d d d d d d d ¯ ¯ ¯ ¯ ¯ ¯ ¯ ¯ ¯ ¯ ¯ ¯ ¯ ¯ ¯ .2(0.28), 1.12 = (0.28), 1.1 = = .0(0.23), 0.30 = = = .5(2.1), 3.05 = = = .1(2.0), 8.61 = (0.21), =−1.3 (0.36), =−1.19 1(0.38), =−0.11 = = 2, = −0.02(032),t −0.02(023),t=12, −1.35(028),t=48, 4, = −0.76(034),t (0.41), −1. 0.33(044), 6(2.1), 5.56 ae aesig- have Males ohsn and sons Both 2,1049 2,988 2,1461 2,569 2,767 ahrsgrandchildren Father’s ubn’ offspring Husband’s aereproduction Male rte’ offspring Brother’s rte’ offspring Brother’s o’ offspring Son’s F F 4.71,P = F F F = = t t t = = t t t t = = = t t 15.3, 10.21, = t = = 21.6, = 12.0, t t =−6.1, = and sthe is 4.0, 1.4, 4.2, −4.4, =−3.4, =−0.3, 2.66, 4.0, −0.1, −2.2, 0.74, −2.7, P .0*ANOVA 0.009* = P P P P P P t P < < = < < P < P P ttsi,*P statistic, < P P P P P < ar oecoeyrltdrltvs(i.3 u emt bene- P to (ANOVA seem relatives marry but daughters 18.2, 3) their (Fig. when relatives more fit related children closely their when more grandchildren marry more have also (F Females tives. sons (ANOVA their depend daughters or to seem their not differences do whether benefits the fitness on These 3). but not Fig. high- and were 1 groups significant (Table and high-relatedness and both low- intermediate- low- the were between the the groups and between relatedness groups contrasts intermediate-relatedness Pairwise and relatives. related closely ewe n’ aet.Errbr:9%cndneitra (CI). interval confidence y). 95% bars: 15 Error age parents. one’s to between survival for residuals are shows parents whose those related. than offspring less fewer have parents more-related of 1. Fig. P 0* ANOVA 0.001** = P P < < 0.14 0.001** 0.001** 0* ANOVA 0.001** = 0* ANOVA 0.001** < = = 0* ANOVA 0.001** = < = 0.001** < = 0.008* 0.001** 0.001** 0.46 0.001** 0.96 0.02 0.007* 0.91 .0)( 0.001) 0.76 0.001** P < h feto nreigo oa etlt.Bt osaddaughters and sons Both fertility. total on inbreeding of effect The < .0)ta hntersn o(ANOVA do sons their when than 0.001) y 1 **P 0.01, i.S4B). Fig. i.S2 (Fig. children of number total for (Methods) residuals axis: d d d d d d d d d d d d d d d ¯ ¯ ¯ ¯ ¯ ¯ ¯ ¯ ¯ ¯ ¯ ¯ ¯ ¯ ¯ = = (0.20), 0.29 = .5(0.22), 0.35 = .2(0.20), 0.62 = .7(0.23), 0.27 = = = = 06 (1.2), 10.64 = (1.3), 4.27 = .7(1.5), 6.37 = 5(0.27), =−0.75 6(0.15), =−1.06 (0.29), =−0.3 2,340 5, = −0.59(025),t = −0.31(024),t 7(0.23), −0.37 8, = −0.64(018),t 4, = −0.27(024),t < ohrsgrandchildren Mother’s 4.36, = 2,712 2,754 2,1186 2,683 2,841 eaereproduction Female agtrsoffspring Daughter’s 0.001. itrsoffspring Sister’s itrsoffspring Sister’s iesoffspring Wife’s F F F F F = = = = t t = t t t t t = = t P 1.96, 4.67, 42.4, 6.81, = = = = = 25.0, t t t =−1.0, 4.3, 3.3, ar rela- marry A) S4 (Fig. 0.014) = =−2.8, =−6.9, = 1.3, 1.6, 3.0, 1.2, 9.2, −2.9, −1.3, −3.6, −1.1, −1.6, P P P P P P P P P P P P = = < = x < = < P P P P P = = = = < xs ofceto relatedness of coefficient axis: 0.13 0.01* 0.001* 0.001** P P P 0.001** 0.001** 0.001** = 2 = = < = 0.18 0.12 0.002* 0.23 0.001** ,445 = < = 0.30 0.03 0.2 0.24 NSEryEdition Early PNAS 0.001** 0.006* 0.001** 0.10 F 4.48, = 2,413 P F 0.012) = 2,525 9.88, = | f8 of 3 F =

ANTHROPOLOGY PNAS PLUS ric fitness costs and benefits of marrying relatives among the Yanomamo¨ support this prediction and suggest that parents should prefer that their offspring marry more closely related kin than the spouses themselves or the offspring would pre- fer. But how exactly are parents benefiting? Because of high male reproductive skew among the Yanomamo,¨ it is possible that fathers might actively desire to exchange their daughters for wives for themselves—a particular risk in polygynous societies. However, the Yanomamo¨ have a generational rule that forbids males from marrying females in the descending generation (36). Although such marriages may occasionally occur, our results do not indicate that individuals obtain more spouses when either their daughters (Fig. S5A) or sons (Fig. S5B) marry relatives. If fathers were preferentially exchanging daughters with relatives to obtain additional spouses for themselves, we would expect to see a positive association between their numbers of wives and the relatedness of their daughters to their sons in-law. Instead, par- ents appear to be exchanging their daughters for daughters in- Fig. 2. The effect of marrying a relative on total fertility. Relatedness to law. In other words, exchanging daughters with relatives enables one’s wife or husband slightly reduces one’s total number of children, espe- parents to obtain more brides for their sons, which in turn seems cially for females. y axis: residuals (Methods) for total number of children to generate more grandchildren. (Fig. S2 shows residual for offspring survival to age 15 y). x axis: mean relat- edness to one’s spouse. Error bars: 95% CI. The Origins of Cross-Cousin Marriage. Preferentially exchanging spouses with close relatives may be driven by contingent reci- procity. One of the biggest problems that individuals face when P4: Sibling Relatedness on the Fitness Outcomes of Brothers engaged in high-stakes exchanges, which are often separated by and Sisters. Brothers. Male reproduction is significantly lower extended time lags, is how to accurately assess the risk of defec- when their brothers marry relatives (Table 1 and Fig. 4A). tion by the other party (8). This is particularly important when Pairwise contrasts between the low- and intermediate-relatedness giving a daughter away in exchange for the mere promise of a groups and the low- and high-relatedness groups were both sig- future bride who is either not yet born or very young. Therefore, nificant but the differences between the intermediate- and high- parents may attempt to hedge the risk of the other party defect- relatedness groups were not. In contrast, males have signifi- ing by preferentially arranging marriage exchanges with close rel- cantly higher reproduction when their sisters marry relatives atives (7). From the parents’ point of view, kin marriages have (Table 1 and Fig. 4B). A pairwise contrast between the low- the additional benefit of strengthening kin networks (e.g., kin and intermediate-relatedness groups was not significant but dif- marriages increase overall within-family relatedness) (15, 36). ferences between the low- and high-relatedness groups and the Although these benefits may help to explain the frequency of intermediate- and high-relatedness groups were. consanguineous marriages, they do not account for why cross- Sisters. The fitness of females increases slightly when their broth- cousin marriage (marriage between the offspring of opposite-sex ers marry relatives (Table 1 and Fig. 4A). Pairwise contrasts siblings), in particular, is so much more common than parallel- between the low- and intermediate-relatedness groups and the cousin marriage (marriage between the offspring of same-sex sib- intermediate- and high-relateness groups were not significant but lings) across cultures (14, 30). the difference between the low- and high-relatedness groups was. Traditionally, hypotheses for cross-cousin marriage prescrip- Meanwhile, females are largely unaffected by the relatedness of tions have fallen into two basic camps—inbreeding avoidance their sisters to their spouses (Table 1 and Fig. 4B). Pairwise con- and mate exchange. Alexander (39) was the first to suggest that trasts between the low- and intermediate-relatedness groups and parallel-cousin marriages were often prohibited because of the the low- and high-relatedness groups were not significant, but possibility that same-sex siblings might share (sexually) each the difference between the intermediate- and high-relatedness groups was.

Discussion To better understand the fitness consequences of consan- guineous marriage, we examined the effects of marrying rela- tives on the reproduction of members of the nuclear family: offspring, spouses, parents, and siblings. We found that (i) chil- dren suffer from inbreeding depression when their parents are closely related, (ii) the reproduction of wives is slightly lower whereas the effects on husbands are equivocal when they marry close kin, (iii) parents have more grandchildren when their chil- dren marry relatives, and (iv) brothers have more children when their sisters marry relatives and fewer children when their broth- ers do whereas sisters benefit slightly when their brothers marry kin and are unaffected when their sisters do. These results sug- gest that parents benefit from exchanging their daughters with close relatives. Overall, the asymmetric fitness costs and bene- fits reported here provide evidence of an evolutionary conflict over mate choice between parents and their offspring and among brothers. Fig. 3. The effect of one’s offspring marrying relatives on number of grand- children produced. Both sexes have more grandchildren when their chil- Parent–Offspring Conflict over Marriage. Differences in optimal dren marry relatives (Fig. S5 A and B separates this relationship by sons and fitness outcomes between parents and offspring are expected daughters). y axis: residuals (Methods) for total number of grandchildren. x to cause conflict over marriage preferences (15). The asymmet- axis: mean relatedness of all offspring to their spouses. Error bars: 95% CI.

4 of 8 | www.pnas.org/cgi/doi/10.1073/pnas.1618655114 Chagnon et al. Downloaded by guest on October 1, 2021 Downloaded by guest on October 1, 2021 hgo tal. et Chagnon way other the than rather around. marriage cross-cousin exogamy lineage promoted was that it that suggests and invokes constraints Whereas hypothesis” evolutionary explanation phylogenetic (9). “the functional exchange marriage, a cross-cousin sister provides for hypothesis or exchange daughter con- mate and parental the children, exogamy, the patrilocality, of in bonding, trol emerge pair naturally to of expected presence hypothe- struc- is this a marriage to cross-cousin created According sis, cross-cousins. exogamy marrying of for practice bias which tural the with in phylo- combined hypothesis persal) (Inbreeding, a exchange dispersal female proposed mate and philopatry the (9) male of Chapais explanation however, genetic recently, groups More descent between lineage (40). alliances build promotes to functions marriage and cross-cousin exogamy between that exchange argue alliances “mate this hypothesis” of lineages form Proponents an different patrilines). from or to that usually matrilines (e.g., are is argued cross-cousins that marriage have and groups of others function and inbreeding. important (5) of risks Levi-Strauss parallel- the lower interpretation Meanwhile, to this function In taboos parallel marriage siblings. putative cousin half that actually risk are the cousins increases which spouse(s), other’s CI. 95% bars: Error spouses. their to paternal) children. and of (maternal number marry. total sisters for their females and whom ods) relatives by fertil- marry total unaffected sisters on largely their relatives are when marrying children sisters more one’s have of Males effect ity. Error The spouses. (B) their CI. rela- to 95% paternal) marry bars: and (maternal brothers brothers one’s their of when relatedness children more relatives slightly tives. marry have brothers their females when and children fewer significantly have Males 4. Fig. y o oa ubro children. of number total for (Methods) residuals axis: h feto n’ rtesmryn eaie nttlfertility. total on relatives marrying brothers one’s of effect The (A) x xs enrltdeso n’ sisters one’s of relatedness mean axis: y xs eiul (Meth- residuals axis: e-isdDis- Sex-Biased x xs mean axis: atrlsshsbe ena motn ntefrainand formation Bedouin the among in herds important of as seen defense been the mate has reduces and pastoralists that raiding general camel exam- For in ple, brothers. between herding) alliances cultivates goat and competition (e.g., also societies pastoral- may or There ist environments daughters. desert challenging their about exchange something to be them enough allow enabling between to thereby trust bonds competition, strengthen how- mate reduce to Perhaps, and serve (40). brothers impor- rules families inheritance the within these and ever, property societies retaining these of in His- tance resources focused (46). have inheriting uncles arrangement males paternal of on type their mari- (30, this of possess for East daughters explanations to Middle torically, the presumed the over are near rights instance, or tal for in men, occur Bedouin these of 45). of exchanges most are and mar- parallel-cousin riage) record patrilateral (i.e., cross-cultural brothers between the parallel-cousin offspring all in competi- Almost noted low. mate is marriages when to siblings same-sex often expect of between more origin should tion marriages the we in parallel-cousin then role see prescriptions, important marriage an plays cross-cousin siblings between tition marriage cross-cousin drives prescriptions. suggests competition hypothesis” that competition opposite—sibling mate is the “local sib- The results the between whereas different. competition our lings, mate is generates of causation phyloge- marriage interpretation cross-cousin the the with constraints although consistent phylogenetic (9) also of are noted hypothesis offspring be patterns netic the should same It only the marry. these time that to in that permitted over prescribing codified are can norms siblings become opposite-sex ultimately social regularities, and as social patterns, status marriage culture these mere formal the that as a governing argued acquire begin has eventu- rules often (9) and the which Chapais generation in system. next embedded exchange the become cooperative into and ally bleed competitive can these same-sex children, females relationships their their of whereas of consanguinity fitness marriages 4 the reduced (Fig. by endure siblings unaffected hand, largely other are Males, kin. the close marry on siblings opposite-sex their when children (Inbreed- ing, patrilocality of independently biases marriage strong cross-cousin generate for could brothers that between suggest do competition they mate brothers, necessary between the competition mate are of prescriptions result marriage cross-cousin not that do results mean daugh- these this Although of siblings). and exchange opposite-sex factor, the between ters critical (i.e., bond the marriage the is cross-cousin spouses generate exchange), can the sister of parents of the parents instead between over by exchange control arranged daughter are parental marriages (e.g., of when absence However, the choice. mate in develop could between suggest conflicts brothers to and siblings seem opposite-sex observations between sis- brothers alliances these that or interactions Interestingly, and mixed-sex aggressive (44). with 43) dyads more compared ter behaviors, in (42, affiliative engage sexes fewer to and both observed of been have contain siblings often polyg- mature beringei) or of beringei sexually sisters groups (Gorilla social gorillas between mountain example, be alliances ynous For may favoring (41). alliances siblings those opposite-sex con- male–male than the of there- common that formation and less such can the adults polygyny mates favoring as Meanwhile, for ditions resources. competition together over same-sex live compete exacerbate not not do do adult- fore usually in who and together brothers between sisters reside relationships beneficial often mutually and who hood com- brothers mar- mate between cross-cousin foster of can petition Patrilocality frequency an cross-culturally. and play systems origin riage may the siblings in among role that important cooperation suggest also and they competition explanation, mate phylogenetic a and exchange ftelclmt optto yohssi readcompe- and true is hypothesis competition mate local the If Yanomam the Among mate both with consistent broadly are results our Although n ieg exogamy. lineage and Dispersal) Sex-Biased A and .Bcueprnscniflec the influence can parents Because B). ,bt ae n eae aemore have females and males both o, ¨ NSEryEdition Early PNAS | f8 of 5

ANTHROPOLOGY PNAS PLUS preservation of alliances and central to the preservation of the dependent variables showed signs of overdispersion and an excess of zeroes culture of these kin-based societies (47). The need to defend so a zero-inflated negative binomial (ZINBI) generalized linear regression and tend to herds can increase the benefits of cooperation model was used. between males. It is important to note, however, that a reduc- The sample was first divided into dead (N = 743) and living (N = 856) tion in the intensity of mate competition between brothers in individuals over the ages of 17 y and 13 y for males and females, respec- parallel-cousin marriage systems does not address causation and tively. For individuals who were alive at the time of the last interview the is compatible with both the “phylogenetic constraints” and local residuals for males and for females were obtained separately. This was done mate competition hypotheses. Which sex disperses (Inbreed- because of the high reproductive skew and different life history patterns of ing, Sex-Biased Dispersal) is also likely to affect mate com- Yanomamo¨ men and women: Male variance in reproduction σ = 10.34 (N = σ petition and resource competition among siblings (48), so we 2,268) is higher than female variance = 6.0 (N = 1,890). The age of the oldest female to give birth was 52 y but 99.5% of all female births were should expect to see more competition between maternal kin to mothers who were 45 y old or younger. Therefore, all females over 45 y and less conflict between paternal kin (49) in matrilocal soci- old were given the truncated age of 45 y so that all females in our sample eties. Female philopatry and high male reproductive skew (e.g., had adjusted ages that were between 14 y and 45 y old. The oldest male polygyny) are expected to expected to impact mate competition to father a child was 81 y but 99.5% of births were to fathers who were among siblings oppositely, however, so these interactions can be 72 y of age or younger. Therefore, all males over the age of 72 y were given complicated. the truncated age of 72 y so that all males in or sample had adjusted ages between 17 y and 72 y old. Conclusion Using these adjusted ages, we then used a retrospective technique to esti- In summary, marriages between close kin (i) significantly reduce mate the completion of these key fitness traits had these males and females the reproductive success of offspring that result from these lived to senescence (52). Year of birth, age, and age squared were all found unions, (ii) impose a slightly negative effect on the reproduc- to have strong effects on fitness consequences so we entered these three tive success of husbands and wives, and (iii) provide a substan- variables into our model. Age squared was included to account for quadratic tial reproductive benefit to both parents and opposite-sex siblings. relationships (e.g., fitness returns may decline beyond a certain age). Year of birth was used to control for cohort effects (i.e., certain generations or Together, these results suggest an important role of both parent– time periods when individuals reproduced more) and because it provided offspring conflict and sibling competition over mate choice among an estimate of the maximum amount of time that any additional data (e.g., the Yanomamo.¨ These results have broad implications for under- children, grandchildren, spouses, mean relatedness to spouses) could have standing the prevalence and origins of marriage systems across been collected on any particular individual. For example, an individual born cultures. Our findings may also reveal new ways to understand in 1950 and censused in 1974 may have been 24 y old the last time N.A.C. within-family conflicts over mate choice. Overall, the impor- actually saw and recorded data on him but life history or spousal related- tant role that Yanomamo¨ parents play in the marriages of their ness information on this individual may have been updated up until the last children, combined with asymmetric fitness outcomes between census in 1988. parents and children, suggests that individual mate preferences For males the model revealed a strong and positive impact of all (especially those of daughters) may be less important than those covariates—age, age squared, and year of birth—on an individual’s total of parents (2, 10, 50) in generating marriage prescriptions. In fertility (McFadden’s pseudo-R2 = 0.49, N = 403), offspring who survived to the Yanomamo,¨ at least, cross-cousin marriage may be a partial age 15 y (McFadden’s pseudo-R2 = 0.49, N = 403), number of grandchildren resolution to mate competition between coresident brothers. (McFadden’s pseudo-R2 = 0.69, N = 403), and number of spouses (McFadden’s pseudo-R2 = 0.27, N = 403). For females the model also showed a strong and Methods positive impact of age, age squared, and year of birth on an individual’s total fertility (McFadden’s pseudo-R2 = 0.50, N = 453), offspring who survived to Data Collection. This study is based on data collected by Napoleon A. age 15 y (McFadden’s pseudo-R2 = 0.49, N = 453), number of grandchildren Chagnon (N.A.C.) between 1964 and 1988, ranging over a period of 50 non- (McFadden’s pseudo-R2 = 0.70, N = 453), and spouses (McFadden’s pseudo-R2 = consecutive months from interviews of almost 2,000 individuals in 60 vil- 0.14, N = 453) for all individuals who were still alive at the time of the last lages. Information was obtained for 4,158 individuals and 1,507 marriages. census. Using these three covariates also produced the lowest adjusted and The genealogical data used in this study include data on all marriages, unadjusted Akaike’s information criterion scores for both males and females. including information on the spouses, their children, their siblings, and their Therefore, a ZINBI generalized linear model was used to regress year of birth, parents (2). There were approximately 25,000 Yanomamo¨ living in this area age, and age squared on each of the dependent variables and these resid- at the time these data were collected (11). The ways in which spouses were uals were saved and used to estimate fitness for all individuals who were related could often be traced through multiple common ancestors and these alive at the time of the last interview for all subsequent analyses. Dead sub- complex relationships were determined using the KINDEMCOM program. jects were presumed to have complete life histories, so their fitness (i.e., The relatedness values between the spouses are coefficients of relatedness total number of children, children surviving to age 15 y, grandchildren, and (r) (the probability that any two individuals share two alleles that are iden- spouses) was fitted to a model in which year of birth was entered as a pre- tical by descent from a common ancestor) (51) and were derived from the dictor to correct for birth cohort effects on fitness residuals. These residuals genealogy. for living and dead individuals were saved and were used as our estimate of The Yanomamo¨ do not have a written language, so the genealogi- fitness. cal data are reliant upon information gathered through oral interviews. Finally, individuals were categorized into three groups based on their mean The genealogies range from a depth of 1 to as many as 10 generations. coefficient of relatedness to their spouse(s)—[Low] = 0–0.031, [Medium] = The accuracy of the estimates of relatedness between spouses depends 0.032–0.062, and [High] = 0.063–1. These categories are meaningful as on the number of generations ancestral to the couple that are known, composite categories of cousin relatedness in a society with high repro- whereas the completeness of reproductive histories depends on the age of ductive skew and where half-cousin marriages are much more common the individuals at the time of the census. To improve the accuracy of the than full-cousin marriages. These categories roughly equate to third and analysis, we excluded individuals if either of their parents was not known fourth cousins [Low], second cousins and half-first cousins [Medium], and and because the youngest male to reproduce was 17 y old and the youngest full first cousins [High] and have enough individuals in each group so that female was 14 y old, we excluded all males and females younger than these meaningful statistical comparisons between all categories can be made ages. In the end there were 1,599 individuals (770 males and 829 females) (Fig. S1). for which there was enough information to obtain reliable measures of spousal relatedness and estimates of fitness. This project was approved on Data Archival. The data used in all these analyses can be found in Dataset S1. April 28, 2016, by the University of Missouri Institutional Review Board For queries on any of these results or analyses please contact Robert Lynch (project no. 2001639). at robertfl[email protected].

Analysis. We used R version 3.2.2 for all analyses. The dependent variables ACKNOWLEDGMENTS. We thank Robin Fox and Bernard Chapais for their used in this study were age and year of birth adjusted estimates of an indi- useful comments on this article. N.A.C. was supported by National Science vidual’s (i) number of children, (ii) number of grandchildren, (iii) number of Foundation (NSF) Grant BCS-1461532 and R.H. was supported by NSF Grant children who survived to age 15 y, and (iv) number of spouses. All of the BCS-1461504.

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