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Home , Cousin marriage, Exogamy, Inbreeding, Patrilineality, Polyandry, Polygyny

Cross- among the Yanomamo¨ shows evidence of –offspring conflict and mate competition between

Napoleon A. Chagnona,1,2, Robert F. Lyncha,1, Mary K. Shenka, Raymond Hamesb, and Mark V. Flinna

aDepartment of , University of Missouri, Columbia, MO 65211-1440; and bDepartment of Anthropology, University of Nebraska, Lincoln, NE 68588-0368

Contributed by Napoleon A. Chagnon, December 21, 2016 (sent for review November 10, 2016; reviewed by Bernard Chapais and Robin Fox) Marriage in many traditional societies often concerns the insti- uals doing the arranging and those whose are being tutionalized exchange of reproductive partners among groups of arranged are close kin; (iii) the arrangers are usually older and kin. Such exchanges most often involve cross-—marriage therefore typically have more social and political power; and with the of a parent’s opposite- —but it is unclear (iv) the arranger (e.g., parent or sibling) and become in- who benefits from these exchanges. Here we analyze the fit- laws who maintain long-lasting ties that are often driven by con- ness consequences of marrying relatives among the Yanomamo¨ tingent reciprocity [i.e., reciprocal altruism (8)] (1, 9, 11). An from the Amazon. When individuals marry close kin, we find that analysis of hunter-gatherer marriage practices using mitochon- (i) both and have slightly lower ; (ii) off- drial DNA suggests a long history of marriages based on reci- spring suffer from depression; (iii) have more procity between the of the (12). grandchildren; and (iv) , especially brothers, benefit when Exchanges of children—especially —by kin groups their opposite-sex siblings marry relatives but not when their forms one of the most basic structures of arranged marriages same-sex siblings do. Therefore, individuals seem to benefit when (5). (Marriage “exchanges” are not always reciprocal transac- their children or opposite-sex siblings marry relatives but suffer tions of offspring and are often exchanges of offspring for politi- costs when they, their parents, or same-sex siblings do. These cal support, , or .) This system is likely to asymmetric fitness outcomes suggest conflicts between parents have emerged from a combination of parental control over mate and offspring and among siblings over optimal strate- choice and contingent reciprocity (9). If cultural rules and gies. Parental control of marriages is reinforced by cultural norms began to exclude exchanges between same-sex siblings, we would prescribing cross-. We posit that local mate com- arrive at the most widespread and common prescriptive mar- petition combined with parental control over marriages may esca- riage practice described by anthropologists—cross-cousin mar- late conflict between same-sex siblings who compete over mates, riage (5, 13, 14). Cross-cousin marriage is the natural outgrowth while simultaneously forging alliances between opposite-sex sib- of using one’s own [or one’s spouse’s] opposite-sex siblings to lings. If these relationships are carried forward to subsequent gen- exchange children. These practices may start out as mere social erations, they may drive bilateral cross-cousin marriage rules. This patterns and regularities before they achieve a moral character study provides insights into the evolutionary importance of how and ultimately become a cultural rule or norm (9). and reciprocity underlie conflicts over who controls mate Parental influence over marriage is expected to generate con- choice and the origins of cross-cousin marriage prescriptions. flict between the interests of parents and offspring. Trivers’

cross-cousin marriage | inbreeding | local mate competition | Significance parent–offspring conflict | Yanomamo¨ Cross-cousin marriage (i.e., marriage with the offspring of a onds between married partners establish ties between both parent’s opposite-sex sibling) is the most common preferred Bextended kin and nonkin who become in-laws (1). Together marriage arrangement across cultures. Despite intense investi- these relationships form families—the foundation upon which gation, the origin and adaptive function of this marriage pre- human social structures are built. Several notable anthropolo- scription have not been resolved. An analysis of the fitness gists have depicted marriage as a competition for sexual access consequences of marriages in the Yanomamo—a¨ tribal soci- to females by male coalitions (2–4) whereas others have viewed ety in the Amazon—shows that parents and brothers achieve it as a reciprocal arrangement between parties whereby offering higher fitness outcomes when their respective children and someone in marriage obligates the receiving to recipro- marry more closely related individuals. Meanwhile, the cate through political support or future spouses (5, 6). In accord with these characterizations, exchanging offspring with close rel- spouses and offspring produced by these unions have lower atives may be a way to ensure that these transactions are eventu- fitness. These findings suggest that cross-cousin marriage pre- ally reciprocated (7, 8). scriptions and taboos against marrying parallel cousins owe their origin to parent–offspring conflict through parental con- Parental Control of Mate Choice Generates Parent–Offspring trol of marriage and competition between same-sex siblings. Conflict Author contributions: N.A.C. collected the data; R.F.L. designed and performed research, Human mating is unique because parents often exert consider- analyzed data, and wrote the paper; M.K.S. researched the paper and helped to design able control over the mate choices of their offspring (9). For the study; and R.H. and M.V.F. researched the paper. example, a cross-cultural survey of hunting and gathering soci- Reviewers: B.C., University of Montreal; and R.F., Rutgers, The State University of eties found that parents have a strong influence over the mar- New Jersey. riages of their and daughters (10). The basic properties of The authors declare no conflict of interest. arranged marriages are (i) the spouses have high exchange value [females are likely to have higher value than males as measured Freely available online through the PNAS open access option. by bride prices, bride service (bride service—sometimes called 1N.A.C. and R.F.L. contributed equally to this work. groom service—is the service rendered by the to a 2To whom correspondence should be addressed. Email: [email protected]. bride’s family as a bride price), and “marriage by capture” in This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. egalitarian societies like the Yanomamo]¨ (6); (ii) the individ- 1073/pnas.1618655114/-/DCSupplemental.

E2590–E2597 | PNAS | Published online March 13, 2017 www.pnas.org/cgi/doi/10.1073/pnas.1618655114 Downloaded by guest on September 30, 2021 Downloaded by guest on September 30, 2021 hgo tal. et Chagnon eodo n utie otc ihamdr etr society western modern no a is with there contact 1950s sustained the bor- any Until the of Venezuela. along record and Amazon northern between the der in living Yanomam tribal the Collection), Data Yanomam The relatives. part- marry increase the to marriage will opportunities sisters, of over especially siblings compete siblings, opposite-sex will because whereas children ners brothers, is fewer especially This sex, do. when and same siblings children relatives same-sex more marry their have when siblings forms will other siblings opposite-sex in P4, their recip- engage and to likely and cooperation; more exchanges of be spousal to expected promised parents are rocate P3, kin rel- close ; close because marry avoid children atives have their to when will grandchildren mechanisms more related have of to will closely due offspring more inbreeding children are P1, to fewer who due (P): spouses children P2, fewer predictions have depression; following will parents on the sib- related has and more test parents, relatedness We spouses, spousal offspring, lings. that of success effect reproductive the the analyze to turalists, Yanomam Predictions. between alliances. cooperative interests opposite-sex build for antagonistic to opportunities siblings providing produce while turn siblings same-sex in can discordant These to outcomes offspring. lead for can consequences that fitness mating asymmetric over marriage conflict over is parent–offspring control that parental generates Overall, a ). receives his for a bene- exchanged (e.g., produce siblings may opposite-sex exchanges for marriage fits time, same the At wives. like societies com- patrilocal sibling Yanomam and induce the polygynous to In are expected spouses. over turn, These parents petition in offspring. of across are, control benefits outcomes because fitness unequal the uneven be is under produce to also are This likely that could conflict. exchanges siblings parent–offspring marriage among through cooperation generated and conflicts ever, resource local to lead (25). that enhancement the siblings with the competition among mate balance activities local to cooperative and (24) way load a inbreeding Disper- of provides costs Sex-Biased dispersal natal (Inbreeding Sex-biased its disperses (21–23). in sal) other competition remains the mate sex and dispersal—one local territory sex-biased , female- in In of result 20). production may (17, the ratios by of sex resolved mating biased are many over In conflicts death 19). the these (18, to insect siblings com- fights same-sex and is between (17), occur taxa siblings can of variety between a Competition) in mon Siblings. Mate Local Between (Inbreeding Competition siblings, Mate half and full their to quarter, them a but in (15). or themselves respectively half, invest to offspring a related hence by their fully related and of are only value offspring all whereas to to equally, expected all related therefore equally are This are and siblings. parents between conflict because generate to is to expected expected the also inter- fitness whom are are asymmetric ests (to These related). relatives parents closely marry more are offspring and parents their differences when offspring toler- more (7) more and benefit fitness poten- be inclusive parents a of to between outcome of expected the background are also (Inbreeding agreements family are inbreeding the of Parents parents ant value (16). whereas spouse, in-law to potential tial value likely con- a to more of parents, likely quality more are their are genetic of children of example, fitness signs For the expected. of is maximize flict preferences not framework mate may a Because offspring tensions. provides these (15) understanding conflict for parent–offspring of theory neprna oto vrmtn vle nhmn,how- humans, in evolved mating over control parental Once ,ataiinlsceyo ot mrcnhorticul- American South of society traditional a o, ¨ nti td,w sdgnaoia aafo the from data genealogical used we study, this In o. ¨ ,bohr npriua r xetdt i for vie to expected are particular in brothers o, ¨ ttetm hs aawr olce (Methods, collected were data these time the At hnterofpig hs dis- These offspring. their than ) eeasvrin indigenous sovereign, a were o ¨ oa aecompetition mate Local fsrn eaens nparental on relatedness offspring (iii) wives, respec- or their follow- of husbands reproduction the the tive of on reproduc- relatedness each offspring spousal on (ii ) for relatedness tion, females parent’s (i) and relationships: males ing of relatedness; outcomes and of S1), bracketed fitness 1 groups coefficient (Table (three Table y their relatedness S2). spousal 15 by (Table of age impact spouses to the of show survived number who (iv) children and of number born (iii) ever and children of 1 number total (Table the (i) as fitness measured We on details additional Results For away. to give seek they daugh- that the that for Yanomam strategies return sisters in of back and brides outcomes ters receive the will men be that ensure to Yanomam appear in agreements observed villages patterns these marriage into The enter (37). usually caution parties with nervousness the with and “Recipro- sides fraught (6). both therefore on promised are as exchanges reciprocate marriage usually not concerns cal” might to are due latter villages villages the partner soon their allied that to or women of before cede to Members husbands reluctant Young their puberty. (2). with reaching living individuals after begin multiple at and age—occasionally to marry young pledged very be a whom may at are birth—and sisters marriage Girls in (38). and cross-cousins promised over female daughters first control for respective exchange most to their attempt the they of exert descent brothers patrilineal marriages local and the of members (36). male adult groups eldest the by or house- the to meat (36). -in-law providing years, his and several of become hold hunting for who last of males may primarily older which consists father-in- service, for their bride less may for This is wife polygynous. service obligation a bride the of promised perform although village been law to the have to obligation move who an women men have the but and husbands), daugh- village her their natal marry their now to in may Yanomam stay attempt sons The his to that (37). a father so ters reclassifying “sister” a a by for as as “niece” common such relationships is genealogical it manipulate generation, same the the among rules sometimes marriage which prescriptive Yanomam however, Because wife, conflict. a manipu- someone find to often to leads are marry difficult rules is to These it patrilineage. required when lated her still or his is of individual outside an both available, are not and cousin poiesxsbig) hspatc ss meddi the in parent’s embedded their so of both is are wife daughters their practice marry This the Yanomam to siblings). expected (i.e., are opposite-sex cross-cousins males that female means This marriage. details additional For 32–35. Politics.) and and 2 Kinship refs. Yanomam see (For on (10). life kin Yanomam political male on and older cross- ethnographies by bilateral source arranged prescriptive primary 31) (30, and patri- marriage (14), as cousin classified were that societies 41% lineal], of with 17% compared sample, matrilineal cross-cultural are worldwide used (SCCS), sample widely cross-cultural a standard (29), includ- the patrilocality [in (14), , (14) groups human descent agnatic ancestral (28), in likely common ing were that been about traits questions have many answering to share for Yanomam they society because The ideal (11). esti- an human period ways is this many It in during are (27). villages 250 hunting across on ple also Yanomam and the that (26) mated manioc and (1964–1988) bananas, collection data Yanomam N.A.C.’s of the period the During (11). Yanomam h Yanomam The araesee marriage o in individuals between are marriages that require o utr httewrsfrfml rs-osnand cross-cousin female for words the that culture o ¨ ¨ ¨ arae r yial ragdete yparents by either arranged typically are marriages o ¨ suab oilognzto see organization social o ¨ alsS1 Tables eido adn hr hyge plantains, grew they where gardens on relied o ¨ oya ¨ rciepecitv iaea cross-cousin bilateral prescriptive practice o ¨ n,rcpoal,tewrsfrml cross- male for words the reciprocally, and, PNAS and ubrdapoiaey2,0 peo- 25,000 approximately numbered o ¨ r omtvl arlcl(h men (the patrilocal normatively are o ¨ Inbreeding, | rncide Tbe1), (Table grandchildren (ii) S2), ulse nieMrh1,2017 13, March online Published hearoya nthe on S1) (Fig. Methods) Yanomam 3) facoscui is cross-cousin a If (36). Inbreeding, cnmc social economic, o ¨ Marriages. o ¨ Yanomam al S1 Table | E2591 o o ¨ ¨ o ¨

ANTHROPOLOGY PNAS PLUS Table 1. outcomes of marrying relatives across three generations of marriage Male reproduction Female reproduction Parents ’s offspring ’s offspring ¯ ¯ Low to medium d =−1.19 (0.36), t =−3.4, P < 0.001** d =−0.75 (0.27), t =−2.8, P = 0.006* ¯ ¯ Low to high d =−1.3 (0.21), t =−6.1, P < 0.001** d =−1.06 (0.15), t =−6.9, P < 0.001** ¯ ¯ Medium to high d =−0.11 (0.38), t =−0.3, P = 0.76 d =−0.3 (0.29), t =−1.0, P = 0.30 Overall ANOVA2,1461 F = 21.6, P < 0.001** ANOVA2,1186 F = 25.0, P < 0.001** Spouses Husband’s offspring Wife’s offspring ¯ ¯ Low to medium d = −1.1 (0.41), t = −2.7, P = 0.007* d = −0.37 (0.23), t = −1.6, P = 0.10 ¯ ¯ Low to high d = −0.76(0.34),t = −2.2, P = 0.02 d = −0.64(0.18),t = −3.6, P < 0.001** ¯ ¯ Medium to high d = 0.33(0.44), t = 0.74, P = 0.46 d = −0.27(0.24),t = −1.1, P = 0.24 Overall ANOVA2,767 F = 4.71,P = 0.009* ANOVA2,841 F = 6.81, P = 0.001* Offspring Father’s grandchildren ’s grandchildren Low to medium d¯ = 5.56 (2.1), t = 2.66, P = 0.008* d¯ = 4.27 (1.3), t = 3.3, P = 0.001** Low to high d¯ = 8.61 (2.0), t = 4.2, P < 0.001** d¯ = 10.64 (1.2), t = 9.2, P < 0.001** Medium to high d¯ = 3.05 (2.1), t = 1.4, P = 0.14 d¯ = 6.37 (1.5), t = 4.3, P < 0.001**

Overall ANOVA2,569 F = 10.21, P < 0.001** ANOVA2,683 F = 42.4, P < 0.001** Brothers Brother’s offspring Sister’s offspring ¯ ¯ Low to medium d = 0.30 (0.23), t = −4.4, P < 0.001** d = 0.27 (0.23), t = 1.2, P = 0.23 ¯ ¯ Low to high d = −1.35(0.28),t=−4.8, P < 0.001** d = 0.62 (0.20), t = 3.0, P = 0.002* ¯ ¯ Medium to high d = −0.02(0.23),t=−0.12, P = 0.91 d = 0.35 (0.22), t = 1.6, P = 0.12 Overall ANOVA2,988 F = 15.3, P < 0.001** ANOVA2,754 F = 4.67, P = 0.01* Sisters Brother’s offspring Sister’s offspring ¯ ¯ Low to medium d = −0.02(0.32),t = −0.1, P = 0.96 d = 0.29 (0.20), t = 1.3, P = 0.18 ¯ ¯ Low to high d = 1.1 (0.28), t = 4.0, P < 0.001** d = −0.31(0.24),t = −1.3, P = 0.2 ¯ ¯ Medium to high d = 1.12 (0.28), t = 4.0, P < 0.001** d = −0.59(0.25),t = −2.9, P = 0.03 Overall ANOVA2,1049 F = 12.0, P < 0.001** ANOVA2,712 F = 1.96, P = 0.13

d¯ is the mean difference between the groups, t is the t statistic, *P < 0.01, **P < 0.001.

reproduction (measured in number of grandchildren produced), closely related relatives. Pairwise contrasts between the low- and (iv) sibling relatedness on the reproduction of their brothers and intermediate-relatedness groups and the low- and high- and sisters. relatedness groups were both significant but the differences between the intermediate- and high-relatedness groups were not P1: Parental Relatedness on Offspring Reproduction. Both sons and (Table 1 and Fig. 3). These fitness benefits do not seem to depend daughters of parents who were more closely related had signif- on whether their daughters (ANOVA2,445 F = 4.48, P = 0.012) icantly fewer total offspring. Pairwise contrasts showed that the or their sons (F2,340 = 4.36, P = 0.014) (Fig. S4A) marry rela- children of the least-related parents had significantly more sur- tives. Females also have more grandchildren when their children viving offspring than both the intermediate-related and most- marry more closely related relatives (Fig. 3) but seem to bene- related groups but showed no significant difference between the fit more when their daughters marry relatives (ANOVA2,525 F = intermediate- and most-related groups (Table 1 and Fig. 1). The 18.2, P < 0.001) than when their sons do (ANOVA2,413 F = 9.88, children of parents who were more closely related also had sig- P < 0.001) (Fig. S4B). nificantly fewer offspring who survived to age 15 y (Fig. S2 and Table S1).

P2: Spousal Relatedness on the Reproduction of Husbands and Wives. The fitness outcomes of husbands and wives who marry close kin are more ambiguous. A husband’s relatedness to his wife sig- nificantly predicted overall differences in reproduction between groups. Pairwise contrasts revealed that husbands who were least related to their wives had significantly fewer offspring than those who were intermediately and most related to their wives but showed no significant difference between the intermediate- and most-related groups (Table 1 and Fig. 2). A wife’s relatedness to her husband also had an overall significant effect on her repro- duction. Pairwise contrasts revealed that women who were least related to their husbands did not significantly differ from those who were intermediately related but did show that they have more children than women who were most related to their hus- bands (Table 1 and Fig. 2). Meanwhile there were no detectable differences between the intermediate- and most-related groups of wives. The impact of marrying relatives on the survival of the couple’s children to age 15 y was also analyzed and did not have any detectable effect on the survival of the offspring of either Fig. 1. The effect of inbreeding on total fertility. Both sons and daughters husbands or wives (Table S1 and Fig. S3). of more-related parents have fewer offspring than those whose parents are less related. y axis: residuals (Methods) for total number of children (Fig. S2 P3: Offspring Relatedness on Their Parent’s Fitness. Males have sig- shows residuals for survival to age 15 y). x axis: coefficient of relatedness nificantly more grandchildren when their children marry more between one’s parents. Error bars: 95% confidence interval (CI).

E2592 | www.pnas.org/cgi/doi/10.1073/pnas.1618655114 Chagnon et al. Downloaded by guest on September 30, 2021 Downloaded by guest on September 30, 2021 ocuecnitoe araepeeecs(5.Teasymmet- expected The (15). are preferences offspring marriage over and conflict parents cause to between outcomes Marriage. fitness over Conflict Parent–Offspring conflict among and evolutionary offspring their an and brothers. parents of bene- between and evidence choice mate costs provide over with fitness here daughters asymmetric reported their the fits sug- exchanging Overall, results from These relatives. do. benefit close sisters parents their marry that when brothers gest unaffected their are when slightly and benefit broth- kin their sisters when whereas children do when fewer ers children and more relatives have marry chil- brothers sisters their their (iv) when and grandchildren lower relatives, marry more marry slightly they have dren when parents is equivocal (iii) wives are kin, husbands close of on are reproduction effects parents the the family: whereas their (ii) when chil- nuclear related, depression (i) the that closely inbreeding found of from We consan- suffer members siblings. rela- dren and of of marrying parents, of reproduction spouses, consequences offspring, effects the the fitness on examined tives the we marriage, understand guineous better To Discussion high-relatedness but and significant, intermediate- not was. the groups were between groups difference high-relatedness the and con- and low- Pairwise groups 4B). intermediate-relatedness the Fig. and low- and the 1 between (Table of trasts spouses relatedness their the to by sisters unaffected their largely are was. groups females high-relatedness Meanwhile, contrasts and low- the Pairwise the between but difference significant 4A). and the not were groups Fig. groups high-relateness intermediate-relatedness and and and intermediate- 1 low- the (Table between relatives marry ers the low- and Sisters. were. the groups groups high-relatedness high-relatedness between and and intermediate- contrast dif- low- but the pairwise significant between relatives A not ferences was marry signifi- 4B). groups sisters have Fig. intermediate-relatedness and their and males 1 when contrast, (Table reproduction In higher not. high- cantly were and 4A). sig- intermediate- groups both the Fig. between relatedness were differences groups and the high-relatedness but 1 and Brothers nificant low- (Table the of and relatives intermediate-relatedness groups and Outcomes low- marry the between contrasts Fitness brothers Pairwise the their when on Sisters. Relatedness and Sibling P4: CI. 95% y). bars: 15 Error age spouse. to one’s survival to offspring edness for residual shows espe- S2 children, (Fig. of number females. total for one’s reduces cially slightly husband or wife one’s 2. Fig. hgo tal. et Chagnon h feto arigarltv nttlfriiy eaens to Relatedness fertility. total on relative a marrying of effect The h teso eae nrae lgtywe hi broth- their when slightly increases females of fitness The Brothers. y xs eiul ( residuals axis: aerpouto ssgicnl lower significantly is reproduction Male o oa ubro children of number total for Methods) ifrne noptimal in Differences x xs enrelat- mean axis: ie o hmevsapriua iki oyyossocieties. polygynous in Yanomam risk the for particular However, high daughters themselves—a their of exchange for to Yanomam pre- Because wives desire actively the would benefiting? might among fathers offspring parents that skew are the related reproductive exactly or closely male how themselves more But spouses marry fer. the the offspring than among their kin relatives that marrying prefer of should benefits and Yanomam costs fitness ric osblt htsm-e ilnsmgtsae(euly each (sexually) share might siblings the of same-sex that because suggest that prohibited to possibility often first avoidance the were was camps—inbreeding marriages (39) parallel-cousin basic Alexander two exchange. mate into and fallen have tions 30). parallel- (14, sib- than cultures same-sex across common of lings) offspring more the between much (marriage so marriage cousin is cross- particular, opposite-sex why of of in for frequency offspring siblings), the account the between not (marriage explain marriage do cousin to they help 36). marriages, may kin (15, consanguineous benefits (e.g., relatedness) these networks have within-family Although kin marriages overall kin strengthening increase view, of marriages of benefit point additional parents’ the the defect- From party rel- other close (7). with the atives exchanges of a marriage Therefore, arranging risk of preferentially young. the by very promise hedge ing or to mere born attempt yet the may when not for parents either important exchange is particularly who in bride is away future This defec- daughter of (8). risk a party the giving other assess the accurately to by by how tion separated is often when lags, reci- are face time which contingent individuals extended exchanges, that by high-stakes problems in driven biggest engaged be the of may One relatives procity. close Marriage. with Cross-Cousin spouses of Origins The seems turn in which grandchildren. sons, more their generate for to in- enables brides relatives more daughters with obtain for to daughters parents exchanging daughters words, their par- other exchanging In Instead, law. be in-law. sons to their appear to ents the daughters and wives their to of of expect numbers relatedness their would between we association positive themselves, a for relatives see If spouses with relatives. additional daughters marry obtain exchanging either S5B) to ( Fig. preferentially when sons were spouses or fathers more S5A) (Fig. obtain daughters do individuals their results that our indicate occur, occasionally (36). not may generation marriages descending such the in Although females marrying from males xs enrltdeso l fsrn otersoss ro as 5 CI. 95% bars: Error spouses. their to offspring all of relatedness mean chil- axis: their when grandchildren daughters). S5 more (Fig. relatives have marry dren Both produced. children 3. Fig. rdtoal,hptee o rs-osnmrig prescrip- marriage cross-cousin for hypotheses Traditionally, h feto n’ fsrn arigrltvso ubro grand- of number on relatives marrying offspring one’s of effect The y upr hspeito n ugs htparents that suggest and prediction this support o ¨ o oa ubro grandchildren. of number total for (Methods) residuals axis: PNAS A aeagnrtoa ueta forbids that rule generational a have o ¨ and | B ulse nieMrh1,2017 13, March online Published eaae hsrltosi ysn and sons by relationship this separates rfrnilyexchanging Preferentially ,i spossible is it o, ¨ | E2593 x

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

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(iii) these the these opposite-sex Together, and and parents on both from wives, to effect benefit and reproductive result tial negative husbands of that slightly success a offspring tive impose of (ii) success unions, reduce significantly reproductive (i) kin the close between marriages summary, In Conclusion be can interactions these competition complicated. so mate however, impact soci- oppositely, to (e.g., siblings matrilocal expected among skew to in reproductive expected male (49) are kin high polygyny) kin and maternal paternal philopatry between Female we between competition eties. so conflict more (48), less see siblings and to among expect competition (Inbreed- should resource disperses and sex petition Which local hypotheses. ing, and constraints” competition in “phylogenetic brothers the mate both between cooperation and with reduc- causation competition compatible address of a is mate not that does benefits of systems however, marriage intensity the note, parallel-cousin the to defend increase in important to can is tion need It herds The males. to (47). between societies tend kin-based and these of culture preservation tepoaiiyta n w niiul hr w lee htaeiden- are that two share individuals two any that probability (the ) h Yanomam The sas ieyt fetmt com- mate affect to likely also is Dispersal) Sex-Biased i ubro hlrn (ii children, of number ) eue eso .. o l nlss h eedn variables dependent The analyses. all for 3.2.2 version R used We falacsadcnrlt h rsraino the of preservation the to central and alliances of .Teerslshv ra mlctosfrunder- for implications broad have results These o. ¨ ,a es,coscui araemyb partial a be may marriage cross-cousin least, at o, ¨ hssuyi ae ndt olce yNplo A. Napoleon by collected data on based is study This onthv rte agae otegenealogi- the so language, written a have not do o ¨ aet lyi h arae ftheir of marriages the in play parents o ¨ ubro rncide,(iii grandchildren, of number ) ubro pue.Alo the of All spouses. of number ) iigi hsarea this in living o ¨ ubrof number ) ,6)i ihrta eaevariance female than higher of is patterns 2,268) history life the different interview and respec- skew done last Yanomam females, was reproductive the This high and separately. of the obtained males of time were for because females the for y at and 13 males alive for and were residuals y who 17 individuals For of tively. ages the over individuals regression linear generalized (ZINBI) used. binomial was model negative zeroes of zero-inflated excess an a and so overdispersion of signs showed variables dependent onain(S)GatBS1652adRH a upre yNFGrant NSF by Science supported National was by R.H. supported and BCS-1461504. was BCS-1461532 N.A.C. Grant (NSF) article. Foundation this on comments useful Lynch ACKNOWLEDGMENTS. Robert contact please analyses or results these robertfl[email protected]. at of any on queries For made Archival. be Data can that categories so all group each between S1). in (Fig. individuals and comparisons enough [Medium], statistical have cousins and and meaningful half-first [High] third and cousins common to first cousins more equate full second much roughly [Low], repro- categories cousins are high These fourth marriages with as marriages. half-cousin society meaningful full-cousin a where are than in and categories relatedness skew These cousin ductive of 0.063–1. = categories = [Medium] composite 0–0.031, [High] = and spouse(s)—[Low] their 0.032–0.062, to relatedness of coefficient of estimate our as used were pre- residuals and a saved These as fitness. were residuals. entered individuals fitness was dead on and birth effects living of cohort for year birth which for (i.e., correct in and fitness to model grandchildren, dictor their y, a 15 to so age fitted histories, to was surviving spouses) life children sub- complete children, were Dead of have analyses. who number subsequent total to individuals all presumed for all interview for were last fitness resid- the jects of these estimate time and to the variables at used dependent alive and the saved of were each on uals birth, squared of year age regress and to used age, was model linear generalized females. ZINBI and and a males adjusted Therefore, both lowest for the scores criterion produced information Akaike’s also unadjusted covariates three these Using census. 0.14, pseudo-R (McFadden’s pseudo-R (McFadden’s y 15 total age individual’s an on birth pseudo-R of (McFadden’s year fertility and squared, age age, of impact positive pseudo-R pseudo-R (McFadden’s total pseudo- (McFadden’s individual’s y an 15 birth—on age of pseudo-R year (McFadden’s and fertility squared, age covariates—age, last related- the spousal N.A.C. until up or time updated history last 1988. been life the in have census may old but individual y him this 24 on on information been data ness have recorded may and 1974 saw in born actually individual censused an and example, 1950 For have individual. in could particular spouses) any (e.g., on to data collected relatedness additional been any mean provided that spouses, time it or grandchildren, of because amount generations children, maximum and certain the more) (i.e., of effects estimate reproduced an cohort individuals Year for when age). control periods certain to time a used beyond was decline birth three may of these quadratic returns for entered fitness account to we (e.g., included so was relationships squared consequences found Age all model. fitness our were into on squared variables effects age and strong age, females have birth, and of to males Year these (52). had senescence traits to fitness lived key ages these of adjusted completion had the sample mate or were in old. males who given y all were fathers 72 y that and to 72 so y of were y 17 age male births 72 between the oldest over of of males age The 99.5% all truncated old. Therefore, but younger. the y y or sample 45 age our 81 of and in was y y females 72 child all 14 a that between y were father so were 45 births y to over that 45 female females ages of all all adjusted age Therefore, of truncated had younger. 99.5% the or given old but were y y old 45 52 were was who birth to give to female oldest h apewsfis iie noda (N dead into divided first was sample The ial,idvdaswr aeoie notregop ae ntermean their on based groups three into categorized were individuals Finally, all of impact positive and strong a revealed model the males For esti- to technique retrospective a used then we ages, adjusted these Using N 5)fralidvdaswowr tl lv ttetm ftelast the of time the at alive still were who individuals all for 453) = 2 e n oe:Ml ainei reproduction in variance Male women: and men o ¨ 0.27, = h aaue nalteeaaye a efudin found be can analyses these all in used data The N 0) o eae h oe losoe togand strong a showed also model the females For 403). = 2 2 0.70, = etakRbnFxadBradCaasfrtheir for Chapais Bernard and Fox Robin thank We 0.69, = PNAS N R 2 2 N 2 2 5) n pue MFde’ pseudo-R (McFadden’s spouses and 453), = 0.50, = 0.49, = 0) n ubro pue (McFadden’s spouses of number and 403), = 0.49, = 0.49, = | Published σ N N N N . 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