American Journal of Primatology S:257-260 (1983) BRIEF REPORT Newborn Adoption in a Confined Group of Japanese Macaques R. FUCCILLO, S. SCUCCHI, A. TROISI, AND F. R. D’AMATO Department of Genetics and Molecular Biology, University of Rome, La Sapienza, Rome, Italy In a group of Japanese macaques, a multiparous high-ranking female gave birth to a n infant and, two days later, adopted a neonate abandoned right after birth by a primiparous low-ranking female. Both infants were reared successfully. Whereas the “selfish” explanation does not accord with the evidence from the present case, the “altruistic” explanation cannot be discarded definitively. However, the context and the consequences of the adoption suggest reproductive error on the part of the adoptive mother as the most likely explanation. Key words: adoption, Mucuca fuscuta, selfishness, altruism, reproductive error INTRODUCTION Students of primate behavior have expressed conflicting opinions about the adaptive significance of adoption. Permanent infant transfer, in the extreme form of kidnapping or infant stealing outside the kin network and with dire consequences for the adoptee, has been regarded as selfish behavior. In fact, it may benefit the foster mother, either directly, by providing her with opportunities to develop maternal skills [Lancaster, 19711, or indirectly, by reducing the fitness of rival females [Quiatt, 1979; Silk, 19801. In contrast, some authors have regarded permanent infant transfer a s a specific case of “altruism,” and they have viewed it as having evolutionary significance in terms of kin selection theory [e.g., West Eberhard, 1975; Riedman, 19821. Finally, Dawkins  has maintained that adoption is usually genetically maladaptive for the adopting mother a s it requires considerable maternal energy expenditure on an unrelated infant or a distantly related kin in preference to similar expenditures on genetic offspring. Natural selection may be assumed to have failed to eliminate such maladaptive behavior because of its rarity [Dawkins, 19761. In fact, adoption seems to be a very rare event in most mammalian groups since it requires the synchronous occurrence of an adoptable infant and an infantless, but lactating, female [Gibson, 19781. In sum, permanent transfer of an infant can alternatively be interpreted as selfish, altruistic, or maladaptive behavior. Almost certainly, the lack of correspondence between these functional explanations is due to a lack of rigor in defining the phenomenon in the first place. Also, statements about the adaptive significance of adoption are generally based on very little supporting evidence [Quiatt, 19791. Therefore, there is a need for detailed information about the frequency of adoption, the age and sex of the infant and the Received April 18, 1983; accepted June 21, 1983 Address reprint requests to Dr. Roberto Fuccillo, Cattedra di Ecologia ed Etologia animale, Istituto di Genetica della Facolta di Scienze, Citta Universitaria, 00185 Rome, Italy. 0 1983 Alan R. Liss, Inc. 2.58 Fuccillo et a1 adoptive caretaker, and the degree of their relatedness as well as the benefit to cost ratio associated with it [Dawkins, 1976; Quiatt, 19791. This report describes in detail the context and the consequences of a case of permanent infant transfer which spontaneously occurred in a group of freely interacting Japanese macaques. This case, as it involved a newborn infant and a mature female, represents a n example of the most interesting kind in its sociobiological implications. CASE HISTORY The adoption took place within the natural group of Japanese macaques (Macaca fuscata) confined in the Rome zoo. During the 1980 birth season, on June 21, a female named Chiarella gave birth to a female infant named Chacma. Two days later, another female of the group, Iole, after a difficult delivery, also gave birth to a female infant, Chiocciola, which she abandoned. Within a few hours, Chiocciola was seen a t Chiarella’s breast next to Chacma. From then on Chiarella took care of both infants, and now, three years later, they still live in the group enjoying good health. At the time of the event, Chiarella was an 11-year-old, high-ranking female. She had previously given birth to three male infants in the years 1977 through 1979, and interestingly, in view of her reproductive success, she gave birth to another male infant in 1981. In contrast, Iole was a six-year-old, low-ranking female a t her first birth. The behavioral indices which are generally used to infer kinship in macaques [Yamada, 19631 suggested that the two mothers were not close relatives. In fact, quantitative data on allogrooming, mutual support in agonistic interactions, and co-feeding showed no preferential relationships between them [D’Amato et al., 1982; Scucchi and Fuccillo, unpublished manuscript]. During the first 12 weeks of the infants’ lives, we collected quantitative data on social behavior of the individuals involved in the adoption. Combining focal animal sampling with complete record, we observed the adoptive mother and her infants 15 min a day, six days a week. Chiarella was recorded as participating in 17 agonistic interactions, every time as attacker, and she was recorded as being avoided by other monkeys 121 times, whereas she avoided another group member once only. Thus, after the adoption, she maintained a high social status. Iole, the biological mother, was never observed trying to get her infant back nor interacting with it. The biological mother interacted with the foster mother very rarely. Iole avoided Chiarella twice and was attacked by her once only. No grooming bout between them was recorded. DISCUSSION The evidence from the present case fits the current explanations of adoption k e . , selfish, altruistic, or maladaptive behavior) to a very variable extent. The characteristics of the individuals involved in the case and the outcome of the adoption do not accord with the “selfish” explanation. The adoptive mother, as she was a multiparous high-ranking female, was unlikely to increase her classical fitness by practicing maternal care or by obtaining status benefits. Also, she did not reduce the biological mother’s fitness since she reared the adopted infant successfully. An “altruistic” explanation based on kin selection theory cannot be definitively discarded. The inferred low degree of relatedness between the biological mother and the adoptive mother is not a conclusive argument against such explanation. First, within a population with considerably high rates of inbreeding, as seems to occur in Japanese macaques [Yamada, 19711, the chances of benefiting a relative may be quite high. Second, as West Eberhard  pointed out, a low degree of genetic relatedness can in fact serve as the basis for kin selection whenever the benefit t o cost ratio of the performed behavior is fairly high. However, the costs related to Newborn Adoption in Macaca fuscata 259 taking care of a completely helpless newborn infant seem to be rather high-indeed, the costs of lactation may exceed even those of gestation [Widdowson, 19761. In addition, the adoptive mother had much to lose in terms of classical fitness through altruism since she was already busy caring for an infant of her own. At a proximal level of explanation, the present case of adoption may be ascribed to reproductive error on the part of the adoptive mother. A permanent infant transfer is not a n unlikely possibility among females that give birth in relative synchrony. This may in part be explained in terms of “priming” and endocrine changes occurring around delivery, which would raise the level of responsiveness to infants in general [Hrdy, 19771. Often the period immediately following birth is critical for female recognition of her infant, and therefore, maternal behavior may be directed a t any young until a preferential attachment between mother and her infant has developed [Jensen, 1965; Harlow, 1971). Partial support for this view comes from another case of infant neglect which occurred in the study group during the 1979 birth season. In that case no female took care of the newborn infant, and it had to be removed to secure its survival. Remarkably, unlike the case reported here, ten days elapsed between the birth of the abandoned infant and the nearest birth. Needless to say, in general the functional explanation of a single case of adoption does not necessarily correspond to the functional explanation of adoptive behavior in nonhuman primates. A particular pattern of behavior only acquires adaptive value with reference to “average statistical circumstances” [Dawkins and Krebs, 19781. Hence, a single occurrence of that pattern is not necessarily to be seen as adaptive, i.e., it does not necessarily reflect all the circumstances that, on average, have made that pattern so fitness enhancing as to be selected during evolutionarily relevant time [Dolhinow and DeMay, 19821. These considerations might raise doubts about the relevance of single case studies to the evolutionary understanding of adoptive behavior. Yet, one must consider that the functional study of a behavior as rare as adoption is in nonhuman primates cannot be routinely conducted by an experimental approach. As research in this field relies largely on the case study method, progress in understanding the phenomenon should stem from a comprehensive evaluation of the concordance between the evidence from single cases spontaneously occurring and the explanatory hypotheses previously advanced. CONCLUSIONS 1.The context and the consequences of this case of adoption suggest reproductive error on the part of the adoptive mother as the most likely explanation. 2. Whereas the value of one case for reconstructing a general theory of adoption is weak, the systematic use of the case study method remains the main procedure to test the current functional explanations. ACKNOWLEDGMENTS We are grateful to Dr. J. Wind, who made very illuminating comments on an earlier draft of the manuscript. REFERENCES D’Amato, F.R.; Troisi, A.; Scucchi, S.; Fuc- BEHAVIOURAL ECOLOGY. J.R. Krebs cillo, R. Mating season influence on allo- and N.B.Davies, eds. Oxford, Blackwell Scigrooming in a confined group of Japanese entific Publications, 1978. macaques: A quantitative analysis. PRI- Dolhinow, P.; DeMay, M.G. Adoption: the importance of infant choice. JOURNAL OF MATES 23:220-232, 1982. HUMAN EVOLUTION 11:391-420, 1982. Dawkins, R. THE SELFISH GENE. Oxford, Gibson, K.R. 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