Surprise... Female macaques compete for ‘power’ and ‘commitment’ in their male partners

Female macaques compete for ‘power’ and ‘commitment’ in their male partners. Christine B. Haunhorst et al. Evolution and Human Behavior, November 18 2019. https://doi.org/10.1016/j.evolhumbehav.2019.11.001

Abstract: The formation of male-female social bonds and the resulting competition among females for male partners is a core element of human societies. While female competition for a male partner outside the mating context is well studied in humans, evidence from non-human primates is scarce, and its evolutionary roots remain to be explored. We studied two multi male – multi female groups of wild Assamese macaques (Macaca assamensis), a species where females gain benefits from selectively affiliating with particular males. Using a behavioral data set collected over several years, we tested whether females competed over access to male social partners, whether success in competition was driven by female dominance rank, and which male traits were most attractive for females. We found assortative bonding by dominance rank between females and males, which together with females initiating and maintaining contact suggests direct female competition over males. Two male traits independently predicted male attractiveness to females: (1) current dominance rank, a measure of “power” or a male's ability to provide access to resources, and (2) prior male affiliation with immatures, a measure of a male's potential paternal proclivity or “commitment” to infant care. Both traits have been consistently identified as drivers of female partner choice in humans. Our study adds to the evidence that female competition for valuable male partners is not unique to humans, suggesting deep evolutionary origins of women's mate choice tendencies for ‘power’ and ‘commitment’.

From the author's 2016 PhD Thesis (Evolutionary origin of the human pair-bond –the adaptive significance of male-female relationships in wild Assamese macaques (Macaca assamensis), Thailand), https://ediss.uni-goettingen.de/bitstream/handle/11858/00-1735-0000-0023-3EBC-9/Dissertation_HaunhorstCB.pdf

ASSAMESE MACAQUES AS MODEL ORGANISM FOR THE EVOLUTION OF HUMAN PAIR-BONDS

In the following, I will combine hypotheses on the evolution of the human pair-bond and concealed ovulation to create a scenario how permanent pair-bonds may evolve or have evolved in Assamese macaques or humans, respectively. I will start with the assumption that in humans concealed ovulation evolved (or rather reliable sexual signals got lost) before the pair-bond evolved (Strassmann, 1981), like in Assamese macaques for reasons not debated here (but see Fürtbauer 2011for an elaborated theory). I will develop a theory how pair-bonds may evolve directly from multimale-multifemale groups with promiscuous mating system. Traits already featured by Assamese macaques (as introduced previously; Figure D3) will serve as baseline, and changes in ecological conditions as catalysts for evolutionary progression.

In Assamese macaques, the current social organization, social structure, and mating system (multimale-multifemale groups, promiscuous, social bonds between all sexes) may serve both sexes best in terms of maximizing reproductive output. The existence of dry and rainy season and the resulting seasonality in food availability favors seasonal breeding in females to time birth and lactation to highest food availability (van Schaik and van Noordwijk, 1985; Heesen et al., 2013). Given the hypothetical scenario that (for example due to climate change) seasonality may be less pronounced and food availability more or less spread evenly across the entire year, females may lose their strictly seasonal ovulation patterns (Fairbanks and McGuire, 1984). Though macaques may be less flexible to shift seasonal ovulation patterns than other primate species (Silk et al., 1981), Assamese macaques already feature prolonged sexual receptivity across four months during mating season (Fürtbauer et al., 2011a). Additionally, females may conceive later, and at the same time more often, when changed conditions favor reproduction. For instance, in 2013 infants were born between February and August, indicating a prolonged mating season, and though unexpected, the female with latest parturition gave birth again only 10 months later (personal observation; Ostner and Schülke, unpubl. data). Aseasonal food availability may also result in less clumped food patches and females ́ need to disperse further for foraging, leading to lowered male herding potential (Lukas and Clutton-Brock, 2013).

[Figure D3: Model for the evolution of pair-bonds in Assamese macaques. The current status of social structure and mating system in Assamese macaques at the top line, with its positive (+) or negative (-) influence on other traits, leading to pair-bonds. Details about necessary changes to lead to permanent pair-bonds can be found in the text.]

Female Assamese macaques would still feature concealed ovulation, resulting in lowered male-male competition for mating (Andelman, 1987; Marlowe and Berbesque, 2012), followed by a decreasing dominance skew in mate guarding ability of males. In turn, operational sex ratio may become more male-biased, because females spread receptive phases throughout the year leading to only a few fertile females at the same time, while the number of males would be constant. Male biased operational sex-ratio is supposed to be a prerequisite for the formation of stable pair-bonds (Quinlan and Quinlan, 2007). In human societies that are classified as monogamous, or serial monogamous, operational sex ratio is usually rather male-biased, while for polygynous populations the opposite holds true (Coxworth et al., 2015). On the other hand, a male biased operational sex-ratio leads again to enhanced male mating competition (Kvarnemo and Ahnesjö, 1996). The intensity of male competition should favor males successfully defending an existent bond, rather than searching for a new mate (Parker, 1974; Quinlan and Quinlan, 2007), particularly when concealed ovulation complicates finding mates at the time of ovulation. Males may then increase their chances for paternity by extending mate guarding for longer periods in which a female may be fertile (Palombit, 1999), leading to an enhanced certainty of paternity. In Assamese macaques, association patterns in the mating season already predict male paternity success with that female across all male dominance ranks (Ostner et al., 2013). At the current state dominant males still have priority of access to fertile females. If male monopolization potential is further lowered, all males may adopt strategies of prolonged associations over longer times to increase paternity success. Males should defend ratherlong-term mating relationships when facing costs by abandoning that relationship to search for another mate (Quinlan and Quinlan, 2007; Kokko and Jennions, 2008). Time may not be the restrictive condition, given that group-living is still enforced, because it holds benefits in terms of lowered predation risk and intergroup competition (Isbell, 1994; Sterck et al., 1997). However, if most females in a group are already taken by another male finding a new mate may be more complicated, resulting in unavoidable fighting risk. Additionally, in almost even operational sex ratios, female choice of partners may further lower male access to mates. Hence, in this scenario male access to multiple fertile females would be very low and abandoning an existent relationship may result in the female being fertilized by another male, while the former partner may not find a new mate.Aseasonal breeding may be followed by the females ́ needs to rely on increased male provisioning to overcome food scarcity in times of highenergy demands (i.e. birth and lactation) (Marlowe, 2003). In Assamese macaques, males do not provision females actively, but males may invest, or at least they do provide tolerance, into the female gaining more energy. This would lead to female partner choice based on traits other than dominance rank, but rather the male's willingness to provide paternal care (Strassmann, 1981; Geary, 2000). Given that males (if only accessing one fertile female) can only increase reproductive success, if the mother is in the physical condition to produce viable offspring, males should provide increased investment for the female during gestation and lactation. During lactation, the male may contribute the most to enhance his reproductive success by providing paternal care for the offspring he most likely sired (Clutton-Brock, 1988). Paternity confusion would then be lower than in a strictly promiscuous mating system, as males may havebetter knowledge of the female's mating history. This would be followed by an increase in male infanticide because most males can be certain of not being the sire of most of the infants. Hence, the male's investment in offspring protection would be mandatory to fend off potentially infanticidal males. Reappearing risk of infanticide may again lead to even tighter bonding between male and female during the highest risk of infanticide (van Schaik and Dunbar, 1990). Male care for female and offspring may also result in shortened interbirth intervals in females (cf. van Schaik and Dunbar 1990). When females reach fertility faster because of male help, the male may increase his own reproductive success further by staying with the same female, finally resulting in a permanent pair-bond.In humans now, strong male bonds may enable large societies consisting of multiple family groups (Chapais, 2013). In Assamese macaques, social bonds between adultmales are stable over several years (Kalbitz et al., 2016)and predictive of male-male coalitions (Schülke et al., 2010). Strong male bonds may increase successful defense of territories and hence overall female reproductive output through higher access to food resources (Boesch and Boesch-Achermann, 2000; Aureliet al., 2006). Additionally, for males within-group competition is lowered (Ostner and Schülke, 2014), and successful protection against incoming infanticidal males enhanced (van Schaik, 1996).

Predictability of the outcome of future interactions with the partner is important for the formation of permanent pair-bonds (Weinrich, 1977). In non-human primates emotional bookkeeping may allow long-term reciprocation between two individuals and create an environment of trust with for both individuals predictable interactions without advanced cognitive abilities (Schino and Aureli, 2010b, 2010c). The already established opposite-sex social bond in Assamese macaques may function as mediator to permanent pair-bonding, by means of predictability of future interactions with the partner. Male care, in terms of agonistic support and feeding tolerance, for females (and offspring) already exists in this species, although permanent pair-bonds are not presently existent. Male bonding is very pronounced in Assamese macaques, which would simplify the transition to rather male-bonded societies. So far, ecological conditions may favor the established social as well as mating system in Assamese macaques, but the traits required to switch social structure and mating system towards a permanently pair-bonded one are already existent.

Humans are the only species that build societies of multiple males and females living together, but with reproductive units that are entirely or primarily monogamous (Chapais, 2013). Considering that humans may also be the most successful extant species on earth, it is surprising that not more species adopted this system –in case that there is a connection. The permanent pair-bond, generated or followed by paternal care and male provisioning, builds the baseline for the development of large brains with increased cognitive abilities (Kaplan et al., 2000). Concealed ovulation in turn may have played a major role in the evolution of pair-bonds (Strassmann, 1981). The loss of this very distinctive and costly (Nunn, 1999)sexual signal in females may therefore have enforced pair-bonding in humans under certain ecologicalconditions. Both, synchrony in breeding and concealed ovulation lower male monopolization potential. Aseasonal breeding species with reliable indicators for ovulation fail to lower male mating competition and monopolization potential, making pair-bonding unattractive for males that can still enhance reproductive success by accessing several receptive females at a time. Seasonal breeding with concealed ovulation favors prolonged mate guarding activity by males only for the breeding season. Exclusively in aseasonal breeding species with concealed ovulation females would be able to prolong mate guarding, binding a particular male as potential sire to herself and resulting in paternal care, as suggested for humans (Hawkes, 2004).