R EPORTS

the study period into one “premove” and two “post- 23. T. E. Seeman, B. H. Singer, C. D. Ryff, G. D. Love, L. 34. STATA 8.0, Stata, College Station, TX (2003). move” periods. For Hook’s Group, which was ob- Levy-Storms, Psychosomatic Med. 64, 395 (2002). 35. We thank the Office of the President of Kenya and the served for 9 years before the move and 7 years after 24. W. L. Gardner, S. Gabriel, A. B. Diekman, in Handbook Kenya Wildlife Service for permission to work in Am- the move, we divided the study period into two of Psychophysiology, J. T. Cacioppo, L. G. Tassinary, boseli; the staffs of the National Museums of Kenya, the premove and one postmove periods. We calculated G. G. Berntson, Eds. (Cambridge Univ. Press, New Kenya Wildlife Service, and Amboseli National Park for the value of the composite sociality index for each York, 2000), pp. 643–664. cooperation and assistance; the members of the pasto- female during each time period using the median 25. J. T. Cacioppo et al., Int. J. Psychophysiol. 35, 143 (2000). ralist communities of Amboseli and Longido and the values of the three behavioral measures derived from 26. N. L. Collins, C. Dunkel-Schetter, M. Lobel, S. C. Institute for Primate Research in Nairobi for assistance each time period for each group. We computed the Scrimshaw, J. Pers. Soc. Psychol. 65, 1243 (1993). and local sponsorship; R. Mututua, S. Sayialel, P. Mu- adjusted value of relative infant survival as the dif- 27. T. E. Seeman, B. S. McEwen, Psychosomatic Med. 58, ruthi, and K. Warutere for their assistance with data ference between the proportion of infants born to 459 (1996). collection; and D. Onderdonk for database assistance. female x in group y in period z that survived to 1 year 28. J. A. LeFevre, M. K. McClintock, Physiol. Behav. 52, Supported by grants from the National Geographic of age and the proportion of all infants born to all 603 (1992). Society, the Louis S. B. Leakey Foundation, the UCLA females in group y in period z that survived to 1 year. 29. W. Saltzman, S. P. Mendoza, W. A. Mason, Physiol. Academic Senate, and NSF (to J.B.S.); the Chicago Zoo- For females observed in multiple time periods, we Behav. 50, 271 (1991). logical Society and NSF (to J.A.); and NSF (to S.C.A.). based analyses on the mean of the adjusted values of 30. C. A. Shively, T. B. Clarkson, J. R. Kaplan, Atheroscle- Supporting Online Material the composite sociality index and adjusted relative rosis 77, 69 (1989). www.sciencemag.org/cgi/content/full/302/5648/1231/ infant survival across time periods. This procedure 31. S. Cohen, J. R. Kaplan, J. E. Cunnick, S. B. Manuck, B. S. DC1 ensures that each data point is independent. Analyses Rabin, Psychol. Sci. 3, 301 (1992). Materials and Methods based on the full data set generate very similar results. 32. F. Aureli, D. A. Smucny, in Natural Conflict Resolution, SOM Text 21. J. S. House, K. R. Landis, D. Umberson, Science 241, F. Aureli, F. B. M. de Waal, Eds. (Univ. California Press, References 540 (1988). Berkeley, CA, 2000), pp. 193–224. 22. S. E. Taylor et al., Psychol. Rev. 197, 411 (2000). 33. H. White, Econometrica 48, 817 (1980). 30 June 2003; accepted 29 September 2003

social relations outside the matriline. In con- Hierarchical Classification by trast, occasional between-family rank reversals represent major social upheavals in which all Rank and Kinship in Baboons the members of two or even more matrilines may lose or gain rank (1, 16–18). They there- Thore J. Bergman,1* Jacinta C. Beehner,1 Dorothy L. Cheney,1 fore have the potential to influence the rank Robert M. Seyfarth2 relations of many individuals. Matrilineal kin groups and linear domi- Humans routinely classify others according to both their individual attributes, such nance rank orders are evident not only to as social status or wealth, and membership in higher order groups, such as families human observers but also to the monkeys or castes. They also recognize that people’s individual attributes may be influenced themselves. Both observations and playback and regulated by their group affiliations. It is not known whether such rule- experiments have demonstrated that monkeys governed, hierarchical classifications are specific to humans or might also occur in recognize the matrilineal kin (or close asso- nonlinguistic species. Here we show that baboons recognize that a dominance ciates) of other group members (1, 5–8). Sim- hierarchy can be subdivided into family groups. In playback experiments, baboons ilarly, monkeys appear not only to understand respond more strongly to call sequences mimicking dominance rank reversals who is dominant or subordinate to themselves between families than within families, indicating that they classify others simul- but also to recognize the relative dominance taneously according to both individual rank and kinship. The selective pressures ranks of others (1–4). It remains unclear, imposed by complex societies may therefore have favored cognitive skills that however, whether monkeys are capable of constitute an evolutionary precursor to some components of human cognition. evaluating other individuals simultaneously according to both rank and kinship or wheth- Although nonhuman primates recognize other between families are potentially much more er they can combine their knowledge of rank individuals’ dominance ranks and kin relations destructive than quarrels within families. and kinship to recognize that some rank re- (1–8), it is not known whether they classify Social groups of Old World monkeys such versals have potentially much greater social others according to both criteria simultaneous- as baboons, macaques, and vervets are com- importance than others. ly. Humans make such higher order classifica- posed of a number of different matrilines To investigate this question, we designed a tions routinely, and as a result easily recognize arranged in a stable, linear dominance hier- playback experiment in which free-ranging fe- that not all superficially similar interactions archy in which all female members of one male baboons (Papio hamadryas ursinus) were have equal importance. For example, in Shake- matriline outrank or are outranked by all played a sequence of calls mimicking a fight speare’s Romeo and Juliet, we discount Mercu- female members of another (9–13). Threats between two other females (19). Call sequences tio’s teasing of Romeo as trivial because both and supplants (interactions in which one an- consisted of a series of threat-grunts by one Mercutio and Romeo are allied with the house imal retreats from the approach of another) individual played in conjunction with the of Montague. When Mercutio aims his taunts at are almost without exception directed by screams of another. Threat-grunts are tonal, Tybalt, however, we regard his behavior as higher ranking individuals toward lower multisyllable, staccato calls that are produced more ominous because Tybalt is a Capulet. Our ranking individuals, and alliances usually tar- only when female baboons are threatening in- responses are guided in part by our tendency to get subordinate opponents (14, 15). Affinitive dividuals who are subordinate to themselves, organize social relations into a hierarchical social behavior such as grooming is directed whereas screams are given only by animals structure, such as familial affiliation, that is preferentially toward close matrilineal kin. who are being threatened by a more dominant governed by a functional set of rules: Quarrels Members of the same matrilineal kin group individual. Numerous experiments and acousti- occupy adjacent ranks and usually retain the cal analyses have indicated that monkey vocal- same relative ranks throughout their lives. izations are individually distinctive and that 1Department of Biology, 2Department of Psychology, University of Pennsylvania, Philadelphia, PA 19104, Both within- and between-family rank rever- subjects discriminate among the voices of ma- USA. sals are rare. When within-family rank rever- trilineal kin (7, 20). *To whom correspondence should be addressed. E- sals do occur, however, they typically involve Subjects were 19 adult female baboons mail: [email protected] only two individuals and have little effect on (Ͼ 6 years old) living in the Okavango Delta

1234 14 NOVEMBER 2003 VOL 302 SCIENCE www.sciencemag.org R EPORTS in Botswana. Matrilineal kinship for all natal versals involved signalers who were adja- different matrilines. However, females animals was known. A matriline included all cent in rank; that is, the lowest ranking were more likely to have non-kin than kin individuals to the level of first cousin. When female in one matriline and the highest as nearest neighbors (21). Finally, subjects’ constructing within-family rank reversal se- ranking female in the next. responses were not affected by the relative quences, however, we chose signalers who Overall, there was a significant differ- frequency of fights among kin as opposed were more closely related to each other (ei- ence in the duration of subjects’ responses to non-kin. Among kin dyads, aggressive ther sisters, mothers and daughters, or nieces to the three call sequences (Fig. 1). Sub- interactions that included threat-grunts and and aunts). The experiments used a within- jects looked toward the speaker for signif- screams occurred at an average rate of 5.4 subject design. On separate days, the same icantly longer durations when hearing se- times per 1000 hours of observation, com- subject heard one of three different call se- quences that mimicked a between-family pared with 6.5 times for non-kin dyads. In quences: (i) an anomalous threat-grunt- rank reversal than when hearing both within- no case did these aggressive interactions scream sequence mimicking a within-family family rank reversal sequences and no- involve threats or screams that violated the rank reversal (e.g., in a group where family A reversal control sequences. In contrast, al- dominance hierarchy. outranks family B, B outranks C, and so on, though subjects on average looked longer at One explanation for subjects’ relatively the subordinate female B3 threat-grunts and within-family rank reversal sequences than weak responses to within-family rank re- the dominant B1 screams), (ii) an anomalous at control sequences, this difference was versals is that they treated all members of sequence mimicking a between-family rank not significant (Fig. 1). Among control se- the same matriline as effectively equivalent reversal (e.g., C1 threat-grunts and B3 quences, subjects looked as long at se- and therefore failed to distinguish among screams), and (iii) a no-reversal control se- quences that mimicked a within-family their ranks. According to this argument, kin quence consistent with the female dominance dispute as at those that mimicked a be- were grouped into the same “equivalence hierarchy. In some control sequences, the tween-family dispute (mean duration of class” as a result of their high rate of signalers were related to each other (e.g., looking, within-family controls: x ϭ 1.4 s, association, becoming both interchangeable ϭ ϭ B1 threat-grunts and B3 screams); in others, SD 1.7; between-family controls: x and mutually substitutable (22). This argu- ϭ they were unrelated (e.g., B3 threat-grunts 1.3 s, SD 1.6; Mann-Whitney U test, ment has some validity. Indeed, the hypoth- ϭ ϭ ϭ Ͼ and C1 screams). Sequences were con- N1 6, N2 13, U 36.5, P 0.25). esis that monkeys perceive within-family structed from the vocalizations of 19 dif- Subjects’ responses to apparent rank re- rank reversals as less important than ferent females. All signalers were unrelated versals were unrelated to the rank distance between-family rank reversals assumes that (i.e., from a different matriline) to the sub- separating the two signalers. In both members of the same matriline are classi- ject who heard their calls. within- and between-family rank reversal fied into the same subgroup. This does not Previous experiments had shown that sub- sequences, subjects looked for equally long imply, however, that monkeys do not rec- jects respond more strongly (by looking to- durations at apparent reversals involving ognize the relative ranks of matrilineal kin. ward the speaker for longer durations) to closely ranked opponents as at those in- During this study, as in most other studies playback sequences that mimic interactions volving more distantly ranked opponents of Old World monkeys (1, 13, 16, 23), rates inconsistent with the current dominance hier- (Fig. 2). Another alternative explanation of aggression among members of the same archy than to those consistent with it (2). We for the animals’ responses might be the matriline were similar to those among un- therefore predicted that subjects would re- possible novelty of proximity between the related females, and their relative ranks spond more strongly to both of the rank were as stable as those of non-kin. Indeed, reversal sequences than to the control se- during the 10 years preceding these experi- quences. We further predicted that, if ba- ments, there were no changes in the adult fe- boons were simultaneously sensitive to both male dominance hierarchy other than those rank and kin relations, they should respond caused by recruitment and mortality. There was more strongly to sequences that simulated a therefore as much opportunity for baboons to between-family rank reversal than to se- learn the ranks of kin as of non-kin. quences that mimicked a within-family rank reversal. A between-family rank reversal is potentiallymuchmoreimportantthanawithin- family rank reversal because it signals a pos- sible change in the dominance relations of two entire matrilines. It therefore has the potential to affect the relative ranks of many individuals rather than just two. Fig. 1. The mean duration that subjects orient- One possible confounder arose because ed toward the loudspeaker following playback members of the same matriline occupy ad- of each sequence type. Overall, there was a jacent ranks, whereas members of different significant difference in the duration of sub- matrilines are often more widely separated jects’ responses to the three call sequences (Friedman two-way analysis of variance, df ϭ in rank. As a result, subjects might respond 2 ϭ Ͻ 2, Xr 12.00, P 0.01). Subjects responded more strongly to a between-family rank for significantly longer durations to between- Fig. 2. The correlation between the strength of reversal sequence simply because the rever- family rank reversal (BFRR) sequences than to subjects’ responses and the disparity in rank sal involved individuals of more disparate both within-family rank reversal (WFRR) se- between the two signalers involved in the ap- ranks. We controlled for rank distance by quences (Wilcoxon matched-pairs signed-rank parent rank reversal. Subjects did not respond test, N ϭ 18, 2 ties, T ϭ 22.5, P Ͻ 0.01) and for longer durations to sequences involving dis- ensuring that a proportion of the within- ϭ ϭ Ͻ family rank reversals involved signalers control sequences (N 19, 2 ties, T 20, P tantly ranked, as opposed to closely ranked, 0.01). There was no significant difference be- opponents (between-family rank reversal: from large matrilines who were separated ϭ ϭ tween the duration of subjects’ responses to Spearman rank correlation, N 19, rs 0.225, by as many as seven ranks. Similarly, a WFRR and control sequences (N ϭ 18, 3 ties, P Ͼ 0.25; within-family rank reversal: N ϭ 18, ϭ Ͼ ϭ Ͼ proportion of the between-family rank re- T 47, P 0.25). rs –0.016, P 0.25).

www.sciencemag.org SCIENCE VOL 302 14 NOVEMBER 2003 1235 R EPORTS

These experiments provide evidence that lective pressures imposed by life in complex 16. A. Samuels, J. Silk, J. Altmann, Anim. Behav. 35, 785 monkeys classify others simultaneously ac- social groups may therefore have favored (1987). cording to both their individual attributes and cognitive skills that constitute an evolution- 17. B. Chapais, Behaviour 104, 41 (1988). 18. C. Ehardt, I. Bernstein, Int. J. Primatol. 7, 157 (1986). their membership in higher order groups, and ary precursor to at least some components of 19. Materials and methods are available as supporting that they do so in the absence of human human behavior. material on Science Online. training. Baboons appear to understand that 20. R. M. Seyfarth, D. L. Cheney, Ann. Rev. Psych. 54, 145 (2003). their group’s female dominance hierarchy References and Notes 21. T. J. Bergman, J. C. Beehner, unpublished data. can be subdivided into matrilines. As a result, 1. D. L. Cheney, R. M. Seyfarth, How Monkeys See the World: Inside the Mind of Another Species (Chicago 22. R. J. Schusterman, D. A. Kastak, Anim. Behav. 55, 1087 they may recognize that, although predictable Univ. Press, Chicago, 1990). (1988). rank relations are maintained both within and 2. D. L. Cheney, R. M. Seyfarth, J. B. Silk, J. Comp. Psych. 23. I. S. Bernstein, in Kin Recognition, P. G. Hepper, Ed. between matrilines, the latter are qualitatively 109, 134 (1995). (Cambridge Univ. Press, Cambridge, 1991), pp. 6–29. 3. A. Sinha, Phil. Trans. Roy. Soc. Lond. B 353, 619 (1998). 24. S. Pinker, The Language Instinct (Harper, New York, different from the former. 4. J. B. Silk, R. M. Seyfarth, D. L. Cheney, Behaviour 136, 1995). These results may also be relevant to the- 679 (1999). 25. R. Jackendoff, Foundations of Language: Brain, Meaning, ories concerned with the evolution of human 5. V. Dasser, Anim. Behav. 36, 225 (1988). Grammar, Evolution (Oxford Univ. Press, Oxford, 2002). 6. F. Aureli, R. Cozzolino, C. Cordischi, S. Scucchi, Anim. 26. M. D. Hauser, N. Chomsky, W. T. Fitch, Science 298, language. As many authors have noted, hu- Behav. 44, 283 (1992). 1569 (2002). mans deduce the meaning of sentences by 7. D. Rendall, P. S. Rodman, R. E. Emond, Anim. Behav. 27. T. Macuda, W. A. Roberts, J. Exp. Psych. Anim. Behav. arranging words into nested, hierarchical 51, 1007 (1996). Proc. 21, 20 (1995). groups that are defined according to their 8. D. L. Cheney, R. M. Seyfarth, Anim. Behav. 58,67 28. We thank the Office of the President and the Depart- (1999). ment of Wildlife and National Parks of the Republic of function as noun phrases, verb phrases, and 9. S. Gouzoules, H. Gouzoules, in Primate Societies,B. Botswana for permission to conduct research in the so on (24, 25). At present, it is not known Smuts, D. Cheney, R. Seyfarth, R. Wrangham, T. Stru- Moremi Game Reserve. We are grateful to M. Mokopi whether the formation of such rule-governed, hsaker, Eds. (Chicago Univ. Press, Chicago, 1987), pp. for invaluable assistance in the field and to J. Silk for 299–305. comments. Research was supported by grants from the hierarchical groups is specific to language or 10. J. R. Walters, R. M. Seyfarth, in Primate Societies,B. University of Pennsylvania, the Leakey Foundation, NIH might have evolved to serve other, nonlin- Smuts, D. Cheney, R. Seyfarth, R. Wrangham, T. Stru- grant MH62249, and an NIH National Research Service guistic purposes, for example in the domains hsaker, Eds. (Chicago Univ. Press, Chicago, 1987), pp. Award postdoctoral fellowship to T.J.B. 306–317. of number, spatial memory, or social rela- 11. G. Hausfater, J. Altmann, S. Altmann, Science 217, Supporting Online Material tions (26, 27). Our results suggest that 752 (1982). www.sciencemag.org/cgi/content/full/302/5648/1234/ baboons organize their companions into a 12. J. B. Silk, Anim. Behav. 58, 45 (1999). DC1 13. J. B. Silk, Int. J. Primatol. 17, 445 (2002). Materials and Methods hierarchical, rule-governed structure based 14. B. Chapais, Int. J. Primatol. 22, 203 (1991). simultaneously on kinship and rank. The se- 15. J. B. Silk, S. C. Alberts, J. Altmann, Anim. Behav., in press. 2 June 2003; accepted 12 September 2003

1236 14 NOVEMBER 2003 VOL 302 SCIENCE www.sciencemag.org