Abstract: Cooperation, or the act of benefiting others at the cost of the benefactor's fitness, has been a central issue in evolutionary theory. Non-human animals sometimes show coalitions or male-male cooperation to confront a male rival and challenge the rank hierarchy. Here we observed novel types of coalitions in wild stump-tailed macaques; multiple males actively shared the mating opportunities, i.e., a male copulated with a female, while his ally waited his turn and guarded them. Our mathematical simulations revealed that lack of estrous signs, as well as large numbers of males in a group, possibly enhance facultative sharing of females. This is the first demonstration of the sharing of females in non-human primates, and shed light on the evolutionary theory of cooperation.
DISCUSSION
To the best of our knowledge, this is the first mammalian observation of collaborative
mate guarding by males, followed by facultative sharing of mating opportunities. Males in other
species, such as chimpanzees, olive baboons, and lions, also collaborate to guard females against
other males. The "cooperative mate guarding by coalition males" in these species appear to be
similar to those in the stump-tailed macaque; however, they fundamentally differ in social
relationships between/among coalition allies or non-allies. The stump-tailed macaque forms
multi-male multi-female societies, which includes a large number of males in the group, among
which only certain individuals tolerate sexual competition and show exclusive attitude toward
others. Male allies in a coalition exclude rivals and then share the mating opportunities with each
other. Thus, coalitions of stump-tailed macaques act as dominant males’ strategy for overcoming
reproductive competition within a group, by sharing the mating opportunities, as well as by
excluding other rivals. In the case of lions, a pride is the unit of a group, which mainly consists
of females and only few males, who collectively defend the females from other invasive males.
This is similar to coalitions of stump-tailed macaques, although alpha (the highest ranking) males
mostly monopolize the mating opportunities, whereas subordinate allies may either have no
access to the females or are allowed limited number of copulations, albeit not through active
sharing. Similarly, olive baboons are a well-known species forming male-male “coalition for
reproduction”, but differ from the stump-tailed macaques regarding the formation of coalitions.
The subordinate baboons form a coalition to jointly attack the dominant male, thereby increasing
their future access to females, while not showing any active sharing of copulations. The
observations made with one chimpanzee group might be comparable to our observations
regarding the stump-tailed macaque, where active sharing copulation (a female copulated with 8
males within a short period) was observed [29]. However, these were considered exceptions only
in the Ngogo population, which are considerably larger than the other populations [see section of
‘Contrasts with other chimpanzee communities’ in 29].
In stark contrast, stump-tailed macaques showed active sharing of mating opportunities
that they jointly obtain among the male allies. In this novel type of coalition, the alpha male
appeared to pay a reproductive cost by giving mating opportunities away to benefit his allies, and
the subordinate males in return repay in terms collaborative work efforts, as a result of which
they gain reproductive advantage as a team. Furthermore, the cooperation among three males is
another novel feature. Generally, coalition formation has been observed in the context of
aggression, characterized by triadic relations, such as the attacker, attack recipient, and supporter.
In the cognitive aspect, coalition formation may require higher abilities of social cognition,
termed "triadic awareness" [30–33], where the individual must recognize not only the dyadic
relationship between two individuals, but also the relationships with other individuals [34]. The
collaboration among three individuals, which is rarely observed in non-human animals, may
require the more expanded capacity of social cognition in this species. Hence, we consider
coalition formation in stump-tailed macaques as a unique instance of male-male cooperation to
achieve reproductive gain, which we believe is rare in non-human animals.
Why do male stump-tailed macaques, unlike males of closely related species, exhibit this
peculiar behavior? To put it in another way, what are the socio-ecological factors in stump-tailed
macaques that may have favored the evolution of this behavior? Here, we tentatively hypothesize
that the absence of signs of ovulation in female stump-tailed macaques is key to understanding
the evolution of male-male coalition, followed by facultative sharing. In many primate species,
the females exhibit visual or olfactory signs of ovulation during the fertile period of the
reproductive cycle. Conspicuous estrous signals such as sexual swellings enhance male-male
competition, providing females more opportunities for mate choice [35–37]. Advertisement of
female reproductive status is often seen in Old World monkeys living in multi-male multi-female
societies, such as most macaques, baboons, and chimpanzees [35–37]. When female
reproductive status is advertised, it is relatively easy for the alpha male to monopolize
fertilizations, as in that case he can concentrate all his guarding efforts on the females fertile at
that moment. On the other hand, when female ovulation is cryptic, the alpha male is no longer
able to adopt the selective guarding strategy, and reproductive monopoly is only possible if all
cycling females are guarded all the time. Our hypothesis is that the difficulty in establishing
reproductive monopoly by the alpha male due to concealed ovulation may have promoted
coalition formation of top-ranking males. Despite the low copulating frequency, it is surprising
that the males adopt a strategy to efficiently monopolize and share the copulating
opportunities—a critical reproductive resource—among multiple coalition males.
Our discovery of male-male coalition, followed by active sharing of mating opportunities
in stump-tailed macaques, demands a revision of the existing socioecological models in primate
social systems. To the best of our knowledge, this is the first documented case in non-human
primates of non-kin collaborative effort for acquiring resources based on active sharing among
allies. We have hypothesized that the lack of estrous signs in female stump-tailed macaques,
unlike many Old World monkeys, is a key factor enhancing male-male coalition coupled with
active sharing. Concealed ovulation is likely to reduce the extent to which fertilizations are
monopolized by dominant males. In our mathematical model, this effect is represented by the
reduction in parameter ". The model predicts that male-male coalition is more likely to occur
when " is small, confirming the logical consistency of our hypothesis. From the female's
perspective, monopolization by dominant males is indicative of limited opportunities for females
to select mates, particularly when they prefer copulations with subordinate or out-group males.
Thus, concealed ovulation may be considered as a female strategy to facilitate mate choice.
Further extending the argument, the formation of coalition followed by active sharing of mating
opportunities may be a counter strategy of dominant males. In other words, being unable to
control female reproduction on his own, the alpha male may be better suited surrendering some
fertilization opportunities to elicit cooperation by subordinates. Hence, the intensified sperm
competition in stump-tailed macaques may be a joint consequence of female concealment of
fertility states and male sharing of mating opportunities. In addition, a potentially relevant
observation is that female stump-tailed macaques do not produce copulation calls [38]. Although
the function of female copulation calls is still a matter of contention [39,40], a possible
interpretation is that female stump-tailed macaques do not make any effort to induce male mate
guarding.
The present study has also revealed the importance of the number of males in a group as
a predictor for the formation of copulation coalitions among dominant males. In other words,
male-male coalition is more likely to be formed when there are more males in a group. In our
field site, we observed five groups of stump-tailed macaques consisting of 391 individuals, or on
an average 78.2 individuals per group. The relatively large group size is primarily due to the
semi-provisioning conditions in our study site, and this factor also appears to affect the
socioeconomic sex ratio, i.e., the ratio of the number of adult females to the number of adult
males. The average socioeconomic sex ratio in our sample is 1.33, while those that have been
previously reported for other populations of stump-tailed macaques are approximately 5.7 [18].
The smaller socioeconomic sex ratio indicates more intense male-male contest. Hence, both large
number of males per group and small socioeconomic ratio may have facilitated the occurrence of
coalition formation by dominant males in our study population.
Per our observational data, the coalition sizes were two or three, but did not exceed four;
however, our current model predicts the monotonic increase of the coalition size over four,
depending on the number of males in a group. This “discrepancy” might indicate three as the
limit of the coalition size in non-human animals. Actually, psychological experiments on
cooperative tasks revealed possibilities of collaboration by two or three subjects, but difficulties
were encountered with four or more subjects even in chimpanzees, probably due to the
limitations of social cognition. For the recognition of quadradic relations, an individual has to
recognize the possible combinations of dyadic and triadic relations, exponentially increasing the
socio-cognitive loading in the brain. Thus, such a socio-cognitive background might limit the
coalition size in stump-tailed macaques. In contrast, humans have evolved a hyper-cooperative
manner beyond the triadic allies, as suggested by the Machiavellian intelligence hypothesis.
We have also observed within-species variation to the extent to which copulations are
monopolized by dominant males, which is represented by " in our model. Despite the marked
ecological similarities between groups, the estimated "′ ranged from 0.30 to 0.97. In the Third
("Z = 0.97) and Wngklm ("Z = 0.78) groups, copulations were almost completely monopolized
by the alpha males, a situation that is called "despotic." This contrasts with the conventional
classification of primate societies, in which stump-tailed macaques are characterized as having
"egalitarian" societies [41], or class 3 social systems [42]. The traditional classification intends to
place each species on a single position on the despotic-egalitarian spectrum, based largely on the
species-level characterizations of ecological factors, such as whether or not a given species is
seasonal breeder, or the abundance and spatial distribution of food resources [43]. However, our
observations clearly suggest that the level of despotism as indicated by " is determined not
necessarily in such a top-down manner, but in a more bottom-up way, such that it may vary
within species according to the idiosyncrasies of each group. For example, our field observation
indicates that the despotic nature of the Third group may have been caused not only by the
physical strength of the alpha male, THR-M01, but by the absence of competent rivals; in fact,
other males seem either too old or immature to challenge him. Therefore, it appears that bottom5 up mechanisms determine " in each group, which then determines whether the alpha male will
adopt the solo monopolization strategy or the coalition strategy.
Finally, our model predicts the future dynamics in the stump-tailed macaque groups. For
example, when youngsters in the Third group become sufficiently mature to challenge the alpha
male, and as a consequence " is reduced, our model predicts that the alpha male will form
coalition with other males. We expect that a longitudinal observation of wild stump-tailed
macaques will confirm these model predictions. In conclusion, stump-tailed macaques are
characterized by societies ranging from despotism to egalitarianism, and from monopolization of
females by a dominant male to male-male coalition coupled with active sharing of mating
opportunities. Future studies on wild stump-tailed macaques may shed new light on the origins
and evolution of altruism and cooperation in mammalian societies, including the hypercooperation in human societies.
To the best of our knowledge, this is the first mammalian observation of collaborative
mate guarding by males, followed by facultative sharing of mating opportunities. Males in other
species, such as chimpanzees, olive baboons, and lions, also collaborate to guard females against
other males. The "cooperative mate guarding by coalition males" in these species appear to be
similar to those in the stump-tailed macaque; however, they fundamentally differ in social
relationships between/among coalition allies or non-allies. The stump-tailed macaque forms
multi-male multi-female societies, which includes a large number of males in the group, among
which only certain individuals tolerate sexual competition and show exclusive attitude toward
others. Male allies in a coalition exclude rivals and then share the mating opportunities with each
other. Thus, coalitions of stump-tailed macaques act as dominant males’ strategy for overcoming
reproductive competition within a group, by sharing the mating opportunities, as well as by
excluding other rivals. In the case of lions, a pride is the unit of a group, which mainly consists
of females and only few males, who collectively defend the females from other invasive males.
This is similar to coalitions of stump-tailed macaques, although alpha (the highest ranking) males
mostly monopolize the mating opportunities, whereas subordinate allies may either have no
access to the females or are allowed limited number of copulations, albeit not through active
sharing. Similarly, olive baboons are a well-known species forming male-male “coalition for
reproduction”, but differ from the stump-tailed macaques regarding the formation of coalitions.
The subordinate baboons form a coalition to jointly attack the dominant male, thereby increasing
their future access to females, while not showing any active sharing of copulations. The
observations made with one chimpanzee group might be comparable to our observations
regarding the stump-tailed macaque, where active sharing copulation (a female copulated with 8
males within a short period) was observed [29]. However, these were considered exceptions only
in the Ngogo population, which are considerably larger than the other populations [see section of
‘Contrasts with other chimpanzee communities’ in 29].
In stark contrast, stump-tailed macaques showed active sharing of mating opportunities
that they jointly obtain among the male allies. In this novel type of coalition, the alpha male
appeared to pay a reproductive cost by giving mating opportunities away to benefit his allies, and
the subordinate males in return repay in terms collaborative work efforts, as a result of which
they gain reproductive advantage as a team. Furthermore, the cooperation among three males is
another novel feature. Generally, coalition formation has been observed in the context of
aggression, characterized by triadic relations, such as the attacker, attack recipient, and supporter.
In the cognitive aspect, coalition formation may require higher abilities of social cognition,
termed "triadic awareness" [30–33], where the individual must recognize not only the dyadic
relationship between two individuals, but also the relationships with other individuals [34]. The
collaboration among three individuals, which is rarely observed in non-human animals, may
require the more expanded capacity of social cognition in this species. Hence, we consider
coalition formation in stump-tailed macaques as a unique instance of male-male cooperation to
achieve reproductive gain, which we believe is rare in non-human animals.
Why do male stump-tailed macaques, unlike males of closely related species, exhibit this
peculiar behavior? To put it in another way, what are the socio-ecological factors in stump-tailed
macaques that may have favored the evolution of this behavior? Here, we tentatively hypothesize
that the absence of signs of ovulation in female stump-tailed macaques is key to understanding
the evolution of male-male coalition, followed by facultative sharing. In many primate species,
the females exhibit visual or olfactory signs of ovulation during the fertile period of the
reproductive cycle. Conspicuous estrous signals such as sexual swellings enhance male-male
competition, providing females more opportunities for mate choice [35–37]. Advertisement of
female reproductive status is often seen in Old World monkeys living in multi-male multi-female
societies, such as most macaques, baboons, and chimpanzees [35–37]. When female
reproductive status is advertised, it is relatively easy for the alpha male to monopolize
fertilizations, as in that case he can concentrate all his guarding efforts on the females fertile at
that moment. On the other hand, when female ovulation is cryptic, the alpha male is no longer
able to adopt the selective guarding strategy, and reproductive monopoly is only possible if all
cycling females are guarded all the time. Our hypothesis is that the difficulty in establishing
reproductive monopoly by the alpha male due to concealed ovulation may have promoted
coalition formation of top-ranking males. Despite the low copulating frequency, it is surprising
that the males adopt a strategy to efficiently monopolize and share the copulating
opportunities—a critical reproductive resource—among multiple coalition males.
Our discovery of male-male coalition, followed by active sharing of mating opportunities
in stump-tailed macaques, demands a revision of the existing socioecological models in primate
social systems. To the best of our knowledge, this is the first documented case in non-human
primates of non-kin collaborative effort for acquiring resources based on active sharing among
allies. We have hypothesized that the lack of estrous signs in female stump-tailed macaques,
unlike many Old World monkeys, is a key factor enhancing male-male coalition coupled with
active sharing. Concealed ovulation is likely to reduce the extent to which fertilizations are
monopolized by dominant males. In our mathematical model, this effect is represented by the
reduction in parameter ". The model predicts that male-male coalition is more likely to occur
when " is small, confirming the logical consistency of our hypothesis. From the female's
perspective, monopolization by dominant males is indicative of limited opportunities for females
to select mates, particularly when they prefer copulations with subordinate or out-group males.
Thus, concealed ovulation may be considered as a female strategy to facilitate mate choice.
Further extending the argument, the formation of coalition followed by active sharing of mating
opportunities may be a counter strategy of dominant males. In other words, being unable to
control female reproduction on his own, the alpha male may be better suited surrendering some
fertilization opportunities to elicit cooperation by subordinates. Hence, the intensified sperm
competition in stump-tailed macaques may be a joint consequence of female concealment of
fertility states and male sharing of mating opportunities. In addition, a potentially relevant
observation is that female stump-tailed macaques do not produce copulation calls [38]. Although
the function of female copulation calls is still a matter of contention [39,40], a possible
interpretation is that female stump-tailed macaques do not make any effort to induce male mate
guarding.
The present study has also revealed the importance of the number of males in a group as
a predictor for the formation of copulation coalitions among dominant males. In other words,
male-male coalition is more likely to be formed when there are more males in a group. In our
field site, we observed five groups of stump-tailed macaques consisting of 391 individuals, or on
an average 78.2 individuals per group. The relatively large group size is primarily due to the
semi-provisioning conditions in our study site, and this factor also appears to affect the
socioeconomic sex ratio, i.e., the ratio of the number of adult females to the number of adult
males. The average socioeconomic sex ratio in our sample is 1.33, while those that have been
previously reported for other populations of stump-tailed macaques are approximately 5.7 [18].
The smaller socioeconomic sex ratio indicates more intense male-male contest. Hence, both large
number of males per group and small socioeconomic ratio may have facilitated the occurrence of
coalition formation by dominant males in our study population.
Per our observational data, the coalition sizes were two or three, but did not exceed four;
however, our current model predicts the monotonic increase of the coalition size over four,
depending on the number of males in a group. This “discrepancy” might indicate three as the
limit of the coalition size in non-human animals. Actually, psychological experiments on
cooperative tasks revealed possibilities of collaboration by two or three subjects, but difficulties
were encountered with four or more subjects even in chimpanzees, probably due to the
limitations of social cognition. For the recognition of quadradic relations, an individual has to
recognize the possible combinations of dyadic and triadic relations, exponentially increasing the
socio-cognitive loading in the brain. Thus, such a socio-cognitive background might limit the
coalition size in stump-tailed macaques. In contrast, humans have evolved a hyper-cooperative
manner beyond the triadic allies, as suggested by the Machiavellian intelligence hypothesis.
We have also observed within-species variation to the extent to which copulations are
monopolized by dominant males, which is represented by " in our model. Despite the marked
ecological similarities between groups, the estimated "′ ranged from 0.30 to 0.97. In the Third
("Z = 0.97) and Wngklm ("Z = 0.78) groups, copulations were almost completely monopolized
by the alpha males, a situation that is called "despotic." This contrasts with the conventional
classification of primate societies, in which stump-tailed macaques are characterized as having
"egalitarian" societies [41], or class 3 social systems [42]. The traditional classification intends to
place each species on a single position on the despotic-egalitarian spectrum, based largely on the
species-level characterizations of ecological factors, such as whether or not a given species is
seasonal breeder, or the abundance and spatial distribution of food resources [43]. However, our
observations clearly suggest that the level of despotism as indicated by " is determined not
necessarily in such a top-down manner, but in a more bottom-up way, such that it may vary
within species according to the idiosyncrasies of each group. For example, our field observation
indicates that the despotic nature of the Third group may have been caused not only by the
physical strength of the alpha male, THR-M01, but by the absence of competent rivals; in fact,
other males seem either too old or immature to challenge him. Therefore, it appears that bottom5 up mechanisms determine " in each group, which then determines whether the alpha male will
adopt the solo monopolization strategy or the coalition strategy.
Finally, our model predicts the future dynamics in the stump-tailed macaque groups. For
example, when youngsters in the Third group become sufficiently mature to challenge the alpha
male, and as a consequence " is reduced, our model predicts that the alpha male will form
coalition with other males. We expect that a longitudinal observation of wild stump-tailed
macaques will confirm these model predictions. In conclusion, stump-tailed macaques are
characterized by societies ranging from despotism to egalitarianism, and from monopolization of
females by a dominant male to male-male coalition coupled with active sharing of mating
opportunities. Future studies on wild stump-tailed macaques may shed new light on the origins
and evolution of altruism and cooperation in mammalian societies, including the hypercooperation in human societies.
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