DISCUSSION
The detailed observations of female responses during male-takeovers
across fifteen years suggest that living in a multi-level society means
that females can mate with extra-unit males, form joint defense with
other females in the same OMU against male attacks, and are able to
successfully transfer to other OMUs to remove their unweaned offspring
from infanticidal males. These counter-strategies appear effective, as
in response most males would tolerate the dependent infant and/or stop
attacking any further infants when some mothers left with infants, and
thus only a small number of infants present during take-overs were
killed by males (4/31). Males in turn gain from changing their own
strategy, as tolerating unweaned infants means their mothers stay with
him, and tolerant males would have a more chance of siring offspring
with them in the future with longer tenure. These findings suggest that
social constraints might be important in shifting the balance of sexual
conflict either towards females or towards males.
In response to the threat of infanticide by males, females have been
argued to exhibit the Bruce effect, where they terminate pregnancies
after exposure to unfamiliar males as an adaptive strategy as it is
highly likely that a female’s offspring will be killed after its birth
(Roberts et al. 2012). This counter-strategy has been confirmed in other
wild mammals including a wild primate, the gelada (Theropithecus
gelada ) with 80% of pregnancies terminated in the weeks after a
dominant male is replaced. In other studies of Bruce effect (Berger
1983; Hackländer & Arnold 1999),
more than 90% pregnant females induce abortions following male
takeover. However, the rate of fetal death (25%) is much lower than
fetal death rates reported in those studies, suggesting that fetal loss
in study population is not an obligate response to male takeovers.
Therefore, abortions in golden snub-nosed monkey might be the result of
sexually selected feticide rather than the Bruce effect in instances
where the new males are aggressive towards females and their offspring,
as has been shown in savannah baboon (Zipple et al. 2017).
In golden snub-nosed monkeys, the Bruce effect has likely failed to
evolve due to several reasons. First, there is no additional benefit for
females to terminate pregnancy before August. The females could not be
conceptive shortly after abortions because golden snub-nosed monkeys are
strictly seasonal breeders with most birth occurring from March to May
and most conceptions occurring between late August and early November
(Xiang et al. 2017). Second, the risk of male infanticide is relatively
low because females have more versatile and effective
counter-strategies. Therefore, the best evolutionary strategy is not to
terminate gestation because the pregnant females have many other
counter-strategies to reduce the risk of male infanticide.
Female primates appear best able to defend their offspring against male
infanticide if they have the flexibility to interact with a range of
social partners and rely on multiple counterstrategies. Multi-male
mating by females in mammals has been indicated to be one of the most
effective strategies to prevent infanticide, as it obscures paternity
such that males refrain from killing offspring if they might be their
father (Wolff & MacDonald, 2004; Lukas & Huchard 2014). In snub-nosed
monkeys, extra-OMU mating and extra-OMU paternities occur between
females and males residing in other OMU (Li & Zhao 2007; Guo et al.
2010; Yang et al. 2014). Furthermore, we observed two cases where
females were accepted into a unit with a resident male with whom she had
previously been observed mating although there no paternities were
identified; another one case was also reported in a recent study (Qi et
al. 2020). In contrast, females very rarely mated with males residing in
the all-male unit, even though all males taking over OMUs came from this
unit because resident males from multiple OMUs collectively show intense
aggression towards these outside males in golden snub-nosed monkeys
(Xiang et al. 2014), presumably limiting opportunities for females to
mate with them and to reduce the risk of infanticide potentially even
further as it does in some polygynandrous societies.
As there is frequently pronounced dimorphism between females and males
in primates, it has been suggested that mothers would be unable to
prevent infanticide physically
(Ebensperger 1998; Palombit 2012).
In this study, we find that, while females might be unable to resist a
male attack on their own, in nearly 85% of attacks females formed joint
defenses that were effective in preventing males from killing their
offspring in that instance. Therefore, although female
joint defenses against male attacks
has sometimes been considered ineffective because females might be
unable to completely prevent males from killing offspring (de Waal
1997), our findings suggest that in snub-nosed monkeys it might create
the crucial delay for females to
exhibit other counterstrategies, in particular keeping their offspring
alive until they might have the opportunities to transfer from their
unit. This effect was more pronounced in larger units, potentially
because more adult females in an OMU can lead to stronger female-female
coalitions, vigilance and risk
detection might also be more efficient (Palombit 2012).
By transferring from their social unit mothers can remove their unweaned
offspring from a potential killer male (Hrdy 1997). Establishing a new
unit with the ousted male, as was observed in four cases here, is
presumably more likely to occur in species in which the habitat is not
saturated with groups that defend territories. Alternatively, females
can attempt to transfer into an already established social unit where a
male would be unlikely to kill the offspring (Steenbeek et al. 1997). In
multi-level societies such as in golden snub-nosed monkeys, the
potential costs of transferring into a new unit are likely to be reduced
compared to other societies. Some females already disperse as
sub-adults, and both natal and secondary dispersal of females mostly
occurs into other social units within their natal band (Guo et al.
2015). This means that females frequently have female relatives residing
in neighbor OMUs, which might help them to join and be tolerated in
these units. Some females have sexual experienced with other resident
male int the band, this might also offer her and her unweaned infant a
refuge when there is high risk of infanticide. In addition, food
competition among the band member in this species is low because
ubiquitous lichens and leaves form a major dietary constituent
throughout the year (Li 2006), facilitating units to be in close
proximity to potentially reduce predatory attacks through travelling,
feeding, and resting within the same areas (Grueter et al. 2020).
The relative low costs associated with female transfers appear to
influence male behavior, too. From the perspective of males taking over
a social unit, emigration of adult females means that they would lose
reproductive opportunities completely. While infanticide might increase
current reproductive success if its mother remains in the OMU, it
appears that on average males are likely to gain higher fitness if they
refrain from attacking the unweaned infant. It is in the case in the
study band when they do not kill their current offspring because male
tenures are significant longer than the female reproductive cycle,
tolerant males even have longer tenure than those aggressive males, and
males are likely to sire future offspring of females as the low
probability of extra-unit paternity. Similarly, a resident male of an
OMU might not only accept an immigrating lactating female because he
previously mated with her, but also because he can increase his future
reproductive success if he remains dominant for at least another
reproductive cycle of that female.
Additionally, we confirm that
females snub-nosed monkeys are able to mount versatile and effective
counterstrategies against male infanticide including extra-unit mating,
joint defense and transfer, leading to no significant difference in the
mortality
of
infant present during male replacement to the base-line mortality of
infants in stable groups (Fig 2). Furthermore, mortality from
infanticide for those infants involved male replacement in the study
population was also much lower than the mortality observed in some Asian
colobines in which females live in single-male or multi-male societies.
For example, in an uni-male society of white-headed langurs
(Trachypithecus leucocephalus ), all eleven infants younger than 6
months died of possible infanticide after male takeovers (Yin et al.
2013). In uni-male and multi-male society of hanuman langurs (Winkler et
al. 1984; Sommer 1987; Borries 1997), death rates of infant following
male replacement were 37.9% (11/29), and 21.6% (8/37) which also
higher than golden snub-nosed monkeys (12.9%, 4/31). These data might
implicate that social organization or mating system would have an
influence on the efficacy of female counterstrategies against
infanticide.
Finally, we want provide a tentative explanation for why older males are
not likely to kill the dependent infant although it would obviously
increase their fitness, they might have not enough life span to wait
another reproductive cycle of lactating female as those younger males.
We argued that it might be explained by the male’s personality which
often termed as consistent individual differences in behavior across
time and contexts. Based on the insight that the trade-off between
current and future reproduction, animal personalities could be given an
adaptive explain in polymorphic population (Wolf et al. 2007). In
snub-nosed golden monkeys of a multilevel society, where multiple OMUs
coordinate and forage together as one larger social band (Grueter et al.
2020), social complexity would allow
polymorphic personality of
resident male in the band. In this study, we have observed two kinds of
male personalities towards unweaned infants following male replacement.
An aggressive male would obviously obtain immediate reproductive success
by infanticide, and this personality may not only benefit to the females
in his OMU when competed with patch resources (i.e., one tree with more
fruit or better for sleeping) but also benefit to the population when
confronted a predator because more aggression to conspecific also mean
bolder in interspecific fight to a predator in many species (Sih et al.
2004). A tolerant male would obviously obtain future reproductive
success through longer tenures (Fig 4b) and monopolize
paternity by attracting females’ residency. Therefore, aggressive males
are favored by natural selection, and tolerance males might favor by
sexual selection in this multilevel society. In fact, we have observed
an extreme example which show the male’s personality might be stable.
For instance, in case #8 and #17, the male (NN) continue attacking the
dependent infant which result two infants were killed (Case #8) or all
two lactating females emigration (Case #17). In the first case, the
male obtained current and future reproductive success, however, he lost
all lactating females in later case.