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Brief report Newborn adoption in a confined group of Japanese macaques.

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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 [1976] 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 [1975] 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.
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Dawkins, R. THE SELFISH GENE. Oxford,
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Quiatt, D. Aunts and mothers: Adaptive implications of alloniaternal behavior of nonhuman primates. AMERICAN ANTHROPOLOGIST 81:310-319, 1979.
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West Eberhard, M.J. The evolution of social
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WIDDOWSON, E.M. Changes in the body
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