Reproductive strategies of rhesus macaques

Reproductive strategies incorporate a multitude of mechanisms that have evolved to promote the reproductive success of individuals. Evolutionary perspectives tend to emphasize the advantages of male-male competition and female choice as mediators of differential reproduction. Male rhesus macaques have not been observed to fight for access to sexually receptive females, although they suffer more wounds during the mating season. An increased likelihood of attacks appears to coincide with male troop entry. Males who spend more time in consort and mate with more females tend to sire more offspring. Genetic analysis of paternity has pinpointed age and endurance rivalry, rather than agonistic competition, as key variables associated with variation in progeny production. Female rhesus macaques often copulate with multiple males during their ovulatory period, and tend to conceive on the first cycle of the mating season. Female reproductive success is more likely to be a function of offspring survivorship than the identity of particular male partners. The role of female choice as a direct mediator of male reproductive success is unresolved, but female mate selection seems to indirectly affect male reproductive success because female preference for mating with novel males seems to foster male dispersal. Evaluating whether mating preferences for particular male phenotypes affectsfemale reproductive success is a task for the future. A common denominator to the reproductive strategies of both female and male rhesus macaques is that feeding patterns affect body condition which influences reproductive output and regulates relative reproductive success.     

Reproductive behavior of free-ranging Lemur catta at Beza Mahafaly Special Reserve,Madagascar

Observations of reproductive behavior in free-ranging Lemur catta were carried out during one annual cycle. Variability in the behavior of female ringtailed lemurs during parturition appears to be mainly a function of the female's parity and thus her experience. Females within a troop show estrous asynchrony and characteristically mate with more than one male. Females also exhibit proceptive behavior toward and mate with some males from other troops and with transferring males. The potential for a male to monopolize mating opportunities during a female's short estrous period is therefore limited. Male mating strategies in ringtailed lemurs can be seen as adaptations to female mate choice during a highly restricted breeding season. In this species the dominance hierarchy does not break down with regard to the order of mating. The highest ranking male (central male) mates first and shows precopulatory guarding and longer postejaculatory guarding, which may increase his chances of siring the offspring. Subsequent mating partners have developed various counterstrategies to mitigate mating order effects.     

Male Mate Choice in Lemur catta

Though females are generally more selective in mate choice, males may also derive reproductive benefits from exercising mate selectivity if one or more factors limit male reproductive success and females differ in reproductive potential. I used male mating effort as a proxy for male mate choice in ring-tailed lemurs (Lemur catta). I calculated mating effort as the rate of male-male agonism during each female's estrous period 30 min before and 30 min after the first and last mountings with intromission. I collected data on 1 free-ranging Lemur catta troop during 2 consecutive breeding seasons on St. Catherines Island, USA. In both yrs, male mating effort differed significantly among troop females once I adjusted male-male agonistic rates to reflect agonistic intensity, and I corrected for the number of observed mates per female (2000: χ² = 27.43, df = 3, p < 0.0001; 2001: χ² = 21.10, df = 3, p < 0.001). Results strongly suggest male mate choice. Contrary to expectation, males did not expend the greatest mating effort for females with the highest dominance status nor the highest reproductive success. Males preferred females that either: (1) belonged to the age class in which fecundity and infant survival is the highest at this site (4–9 yrs), or 2) were older females (≥10 yrs) with high reproductive success. Female reproductive potential appears to be an important variable determining male mating effort in Lemur catta.     

Costs of Mate Guarding and Opportunistic Mating Among Wild Male Japanese Macaques

A trade-off relationship between mating and feeding effort is important when considering reproductive strategies of long-lived species. I compared the influence of male sexual activities, female mate-choice behaviors and the daily activity budget on male mating success among males in a group of wild Japanese macaques (Macaca fuscata yakui) on Yakushima Island. The 1st-ranking male, which had immigrated into the troop at this rank, more frequently approached peri-ovulatory females, spent more time grooming peri-ovulatory females and in mounting series and spent less time feeding than subordinate males did. The 1st-ranking male attained the highest mating success as a result of his high expenditure of time and energy in sexual behaviors directed toward peri-ovulatory females. Mating success of subordinate males did not relate to the amount of sexual effort, but instead to the frequency of female approaches, female rush toward males and the number of peri-ovulatory females within the group. The pattern of intermale competition shifted from nearly contest competition to scramble competition as the number of peri-ovulatory females in the group increased. Feeding time of subordinate males did not vary between the days when they copulated and the days when they did not. The findings demonstrate that mate guarding in the 1st-ranking male is a high-cost mating tactic, while opportunistic mating in subordinate males is a low-cost mating tactic. The differences in male mating tactics are probably related to male life history and to the formation of groups with a high socionomic sex ratio.     

Male mate choice in Tibetan macaques Macaca thibetana at Mt. Huangshan, China

Though females are generally more selective in mate choice, males may also benefit from mate choice if male reproductive success is limited by factors other than simply the number of female mates, and if females differ in short-term reproductive potential. We studied male mate choice in a free-ranging troop of Tibetan macaques Macaca thibetana at Mt. Huangshan,China, from August 2007 to April 2008. We employed focal animal sampling and all occurrence sampling to record sexual related behaviors. Eight adult females were divided into three female quality categories according to the females' age, rank and parity.Using male mating effort as a proxy for male mate choice, we found that males do distinguish female quality and show time-variant mating strategies. Specifically, females with dominant rank, high fecundity, and middle age attracted significantly more males. Our results suggest that female short-term reproductive potential appears to be an important variable in determining male mating effort. Male Tibetan macaques do exercise mate choice for higher quality females as well as reduce useless reproductive cost, which is consistent with the direct benefits theory of mate choice.     

MHC-associated mating strategies and the importance of overall genetic diversity in an obligate pair-living primate

Mate choice is one of the most important evolutionary mechanisms. Females can improve their fitness by selectively mating with certain males. We studied possible genetic benefits in the obligate pair-living fat-tailed dwarf lemur (Cheirogaleus medius) which maintains life-long pair bonds but has an extremely high rate of extra-pair paternity. Possible mechanisms of female mate choice were investigated by analyzing overall genetic variability (neutral microsatellite marker) as well as a marker of adaptive significance (major histocompatibility complex, MHC-DRB exon 2). As in human medical studies, MHC-alleles were grouped to MHC-supertypes based on similarities in their functional important antigen binding sites. The study indicated that females preferred males both as social and as genetic fathers for their offspring having a higher number of MHC-alleles and MHC-supertypes, a lower overlap with female’s MHC-supertypes as well as a higher genome wide heterozygosity than randomly assigned males. Mutual relatedness had no influence on mate choice. Females engaged in extra-pair mating shared a significant higher number of MHC-supertypes with their social partner than faithful females. As no genetic differences between extra-pair young (EPY) and intra-pair young (IPY) were found, females might engage in extra-pair mating to ‘correct’ for genetic incompatibility. Thus, we found evidence that mate choice is predicted in the first place by the ‘good-genes-as-heterozygosity hypothesis’ whereas the occurrence of extra-pair matings supports the ‘dissassortative mating hypothesis’. To the best of our knowledge this study represents the first investigation of the potential roles of MHC-genes and overall genetic diversity in mate choice and extra-pair partner selection in a natural, free-living population of non-human primates.     

Influence of fluctuation in the operational sex ratio to mating of troop and non-troop male Japanese macaques for four years on Kinkazan Island, Japan

Taking advantage of a marked yearly fluctuation in the number of estrous females, I studied the differences in mating success between troop males and non-troop males in an unprovisioned group of Japanese macaques. Fluctuation in the defendability of estrous females by troop males, as predicted by the operational sex ratio (the number of estrous females per troop male), strongly affected the mating with ejaculation (successful mating) per observation day of both troop and non-troop males. When operational sex ratio was low, troop males monopolized successful mating inside the troop. No successful mating of non-troop males was observed inside the troop. In contrast, both troop and non-troop males were able to mate often inside the troop when operational sex ratio was high. These findings suggest that troop males obtained the benefit of secured successful mating in the troop because troop males could mate successfully even in mating seasons with a low operational sex ratio, and the chance of successful mating for non-troop males will increase as the ability of troop males to monopolize estrous females decreases.     

Courtship song, male agonistic encounters, and female mate choice in the house cricket,Acheta domesticus (Orthoptera: Gryllidae)

Whether female crickets choose among males based on characteristics of the courtship song is uncertain, but in many species, males not producing courtship song do not mate. In the house cricket,Acheta domesticus, we examined whether a female chose or rejected a male based on his size, latency to chirp, latency to produce courtship song, or rate of the high-frequency pulse of courtship song (“court rate”). We confirmed that females mated only with males that produced courtship song, but we found no evidence that the other factors we measured affected a female’s decision to mate. In addition, we investigated whether the outcome of male agonistic encounters affected the subsequent production of courtship song. In one experiment, we observed courtship and mating behavior when a single female was placed with a pair of males following a 10-min interaction period between the two males. Winners of male agonistic encounters had higher mating success. However, winners and losers of agonistic encounters were not different in their likelihood or latency to produce courtship song or in the number of times they were disrupted by the other male in the pair. In a second experiment, we allowed two males to interact for a 10-min period, but following this interaction period, we placed a female with each male separately and observed courtship and mating behavior. The mating success of winners and losers was not different under these circumstances, and we found no differences between winners and losers in any subsequent courtship or mating behavior examined. We conclude that winning agonistic encounters influences a male’s mating success in ways other than his production of courtship song and this effect is lost when winning and losing males are separated and each is given an opportunity to mate.     

Mating patterns,mate choice,and birth season heterosexual relationships in free-ranging rhesus macaques

Birth season adult heterosexual nonkin relationships of 50 free-ranging female rhesus macaques (Macaca mulatta) in two social groups at Cayo Santiago, Puerto Rico were examined using focal follow (289 hr) and ad lib data. Eighty-eight percent of subjects had at least one relationship characterized by particularly high frequencies of spatial proximity, grooming, or both. These were designated “friendships.” Males intervened in aggressive interactions more frequently on behalf of Friends than non-Friends. Female aggressive support of males was extremely rare. Higher-ranking males experienced more friendships than lower-ranking males. High-ranking females had higher-ranking Friends than low-ranking females. Older females had higher-ranking Friends than younger females. Females groomed high-ranking Friends more than they were groomed by them, whereas they groomed low-ranking Friends less than they were groomed by them. In one social group, high-ranking females were more likely than low-ranking females to groom their Friends more than they were groomed by them. Males were more responsible than females for spatial proximity maintenance in 9 of 14 Friend dyads for which sufficient data were available. Neither male nor female dominance rank affected responsibility for proximity maintenance in Friend dyads. Eight of 24 females had friendships with males with whom they had completed copulations during their conception peri-ovulatory period of the preceding mating season. Two of 19 females completed peri-ovulatory copulations with Friends during the following mating season. Friendship was not correlated with either of two demonstrated female mate choice indicators: (1) proximity maintenance during estrus; or (2) cooperation with male “hip-grasp” courtship attempts. Males directed “muzzle-up” courtship signals at lower rates toward Friends than toward non-Friends. These and other investigators' results indicate that (1) protection from aggression is the primary benefit to female rhesus macaques of birth season heterosexual relationships; (2) the most effective protectors are in greatest demand as Friends; and (3) friendship has no effect or an inhibitory effect on mate choice in this species. Benefits to males of friendships were not apparent from this study but may include coalitional support against lower-ranking males.     

Mate Choice in Male Mandrills (Mandrillus sphinx)

Male primates that attempt to monopolize access to receptive females by mate‐guarding expend time and energy and risk injury, making reproduction costly. Males should therefore show mate choice and preferentially allocate mating effort to females that are likely to be fertile and those that will produce high‐quality offspring. Specifically, males should preferentially mate‐guard high‐ranking females rather than low‐ranking females, as such females are more likely to be fertile and are able to invest more in offspring. Males should also prefer parous females to nullipares, for similar reasons. Finally, males should avoid mating with close relatives, to avoid the deleterious effects of inbreeding. We investigated 13 group‐years of mate‐guarding observations for two semi‐free‐ranging groups of mandrills to examine the influence of these factors on male investment in mate‐guarding. We found that males mate‐guarded higher‐ranking females more than lower‐ranking females, and parous females more than nullipares. Female age, true relatedness and maternal kinship did not influence male mate‐guarding. Our results suggest that male mandrills do exercise mate choice for higher‐quality females, in the form of higher‐ranking and parous females. As alpha males are responsible for the great majority of mate‐guarding, this can lead to assortative mating, where high‐ranking males reproduce with high‐ranking females, and has important implications for social relationships and kin selection.     

Mate selection,consortship formation,and reproductive tactics in adult female savanna baboons

Mate selection is a proximate mechanism influencing the probability that two individuals will engage in reproductive activity. The degree to which mate selection by female savanna baboons (Papio cynocephalus anubis) affects consortship formation and the characteristics of males that they prefer to mate with were analyzed based upon a 19-month study in Kenya. Sexual solicitations by females had a positive impact on the probability that males would establish consort relationships. The most preferred mating partners were young, high ranking, newcomer males, but these same males did not have the highest mating success. Friendships between male and female baboons almost always developed subsequent to conception cycles. Female savanna baboon reproductive tactics appear to be based upon maximizing the probability that males will provide care for offspring.     

Female Defensibility in a Small Troops of Japanese Macaques vis-à-vis Nontroop Males and Copulation on the Periphery of the Troop

I provide data compiled over 4 yr on the mating behavior in small troops of wild Japanese macaques on Yakushima Island. The key parameters are the number of sexually receptive females, the number of nontroop males (NTMs), and copulation on the periphery of the troop. I analyzed the following aspects: 1) changes in the proportion of copulation with high-ranking males (HRMs) and NTMs, 2) variations in factors such as fluctuation in the number of sexually receptive females and troop males and their effects on the number of visiting NTMs, 3) the effect of attempted interruption of mounting series by other males, and 4) some aspects of copulation on the periphery of the troop. Throughout the study, 56% of the total number of females mated most frequently with the α-male in a single mating season. However, the relative mating success of HRMs varied over the years and between individuals. The number of visiting NTMs varied depending on the number of receptive females and troop males. Females tended to mate with the NTMs when they appeared around their troops. The direct effect of interruption of the mounting series by other males is equivocal. The females mated with the low-ranking males (LRMs) and NTMs on the periphery of the troop, which increased the possibility of mounting series ending with ejaculation. Females actively sought opportunities for copulation on the periphery of the troop by moving there or initiating close proximity with LRMs and NTMs there. On Yakushima Island, the mating success of HRMs was not always as high as that predicted by the priority of access model. The injury status of the HRM, the number of visiting NTMs, and female choice are all considered to influence a male’s mating success.     

Female mate choice and male–male competition in Tonkean macaques: Who decides?

The theory of sexual selection predicts that females should be discriminatory in the choice of sexual partners. Females can express their choice in two ways. In direct mate choice, they show preferences for certain partners. In indirect mate choice, they select partners by displaying sexually attractive traits, thus eliciting contest competition between males. We focused on a primate species in which females advertise the timing of their ovulation and studied the balance between these two choice strategies. We tested predictions related to three hypotheses about direct and indirect female choice, namely the best‐male, graded‐signal and weak‐selectivity hypotheses. We investigated the sexual and agonistic interactions occurring during oestrous periods in five captive groups of Tonkean macaques (Macaca tonkeana). The results showed that dominant males used mate guarding to monopolise sexual access to parous females that were in the fertile stage of their reproductive cycle, while lower‐ranking males monitored only nulliparous females. The distribution of sexual presentations indicated that females accepted different types of partners, supporting the weak‐selectivity hypothesis regarding direct mate choice. The analysis of behavioural sequences revealed that mate‐guarding males used mild coercive behaviours to prevent females from mating with other males at conception time. The distribution of mounts showed that females mainly mated with dominant males, which leads us to argue that the best‐male hypothesis provides the most parsimonious explanation regarding indirect mate choice in Tonkean macaques. At the individual level, it may be concluded that male competitive strategies prevented females from exercising direct mate choice. At the evolutionary level, however, female sexual advertising and thus indirect choice promoted competition between males. The outcome is that indirect mate choice appears more important than direct mate choice in female Tonkean macaques.     

A longitudinal analysis of reproductive skew in male rhesus macaques

One of the basic tenets of sexual selection is that male reproductive success should be large in polygynous species. Here, we analysed 6 years of molecular genetic data from a semi-free-ranging population of rhesus macaques (Macaca mulatta), using Nonac's B index, to assess the level of male reproductive skew in the study troop. On average, the top sire in each year produced 24% of the infants, while 71% of troop males sired no offspring at all. Consequently, 74% of infants had at least one paternal half-sibling in their own birth cohort. Reproductive success was greatest for high-ranking males, males who spent the whole mating season in the troop and males of 9-11 years of age. Heterozygosity for major histocompatibility complex (MHC) class II gene DQB1 was the strongest single predictor of male reproductive success. A negative relationship suggestive of female mate choice was noted between the B index and the proportion of extragroup paternities. Reproductive skew was not associated with relatedness among potential sires or with female cycle synchrony. We conclude that reproductive skew in male rhesus macaques is best accounted for by the 'limited-control' model, with multiple factors interacting to regulate individual reproductive output.     

Part-Time Mate Guarding Affects Paternity in Male Reed Buntings (Emberiza schoeniclus)

Male mate guarding by close following has been reported in many socially monogamous bird species and is generally believed to function as a paternity guard. Many aspects of the dynamics and effectiveness of this behavior are still however poorly understood. Here, we describe the temporal variation in mate guarding behavior in male reed buntings (Emberiza schoeniclus) with a particular focus on how males allocate their mating effort between mate guarding and extrapair mating in a context of intense sperm competition. In our highly synchronous study population most males have to balance the simultaneous and mutually exclusive demands of mate guarding and seeking extrapair copulations (EPCs). We found that males frequently switched between guarding their mates and performing intrusions to neighboring territories. Both activities seemed to have significant fitness payoffs, as male mate guarding effort had a positive effect on paternity, and a large fraction of extrapair fertilizations occurred during the days when the sire guarded its own female. The reed bunting is thus an example of how discontinuous or part‐time mate guarding can still be effective in securing paternity. Female reed buntings were not particularly active in initiating EPCs as they never were observed performing extraterritorial forays. We argue that the absence of female‐initiated EPCs is a prerequisite for males to trade mate guarding against seeking EPCs. Otherwise, if females circumvent male mate guarding by timing their EPCs to periods of male absence, males should guard their mates almost continuously or rely on alternative paternity guards.     

Male Mating Tactics in Captive Rhesus Macaques (Macaca mulatta): The Influence of Dominance, Markets, and Relationship Quality

Male mating success in a multimale–multifemale group can depend on several variables: body condition, dominance, coalitions, “friendship,” or an exchange of services for mating access. Exchange patterns may also be determined by market effects or social relationships. We studied the mating tactics of males in a captive, multimale–multifemale group of rhesus macaques and the resulting patterns of mating and paternity to determine the influence of dominance rank, mating markets, and relationship quality on their mating tactics. Male rank was positively related to the total number of copulations and the number of mating partners, but did not explain male mating distribution completely. Moreover, male fertilization success was not related to male rank. Males did not exchange grooming for mating access on the same day and neither the supply nor the rank (as a proxy for quality) of receptive females affected the amount of male grooming, suggesting that market effects did not explain male mating access. However, there was a positive correlation between long-term grooming patterns of both males and females and mating access, indicating that social relationships were important for male mating access. Paternity data revealed that these social relationships were also important for male reproductive success. We conclude that both male rank and male–female “friendship” determined male mating access in these rhesus macaques, but that “friendship” was more important in determining paternity, emphasizing the importance of intersex social bonds in male mating success in multimale primate societies.     

Sexual strategies of female Japanese macaques (Macaca fuscata)

Evidence is reviewed that female Japanese macaques have multiple male mating partners when they are available and show a preference for mating with sexually unfamiliar males. Several lines of evidence suggest that this aspect of female sexual behavior results in the offspring of an individual female being sired by more than one male thereby maintaining the genetic diversity of the troop. Evidence is presented in this paper that a decrease in the number of adult troop males and a lack of extra-troop migrant males in the Arashiyama West troop of Japanese macaques following transplantation to a ranch in south Texas had consequences for the sexual behavior of the females.     

Aggressiveness during monogamous pairing in the sleepy lizard, <Emphasis Type="Italic">Tiliqua rugosa</Emphasis>: a test of the mate guarding hypothesis

The Australian sleepy lizard, Tiliqua rugosa, maintains monogamous associations for an average of 6 weeks before mating each spring. One hypothesis to explain this prolonged partnership is that males are guarding their female partners from rival males. This hypothesis has three predictions, that males are more aggressive than females to conspecific males, that male aggression will increase as the time of mating gets closer, and that males will be more aggressive towards conspecific males when they are with their partner than when they are alone. We tested those predictions with indirect evidence of aggression, using counts of scale damage on randomly encountered lizards, and with direct observations of their responses to approaches by conspecific and heterospecific models. As predicted by the mate guarding hypothesis, males showed more evidence of aggression towards conspecifics than did females. However, in contrast to the hypothesis, males did not become more aggressive as the time of mating came closer, and males in pairs were less aggressive than males on their own. Mate guarding cannot be the only process that has led to the prolonged monogamous associations in this species. Parental care is also unknown in these lizards, and we suggest that monogamy may be maintained through some form of female coercion, allowing females to gain additional fitness from the enhanced vigilance that results from male proximity.     

Mate guarding behaviour in the supralittoral isopod,Ligia dentipes (Oniscidea) from the Andaman and Nicobar Islands

Precopulatory mate guarding is a characteristic feature in the mating behaviour of many Malacostraca, and a necessary prerequisite for those species in which female receptivity for males is restricted to a short period of time after the pubertal/reproductive moult. This study deals with the pre-mate guarding behaviour of the semi-terrestrial isopod Ligia dentipes living in the crevices of coral boulders and rocks in the supralittoral region of the Andaman Islands. As in other isopods, moulting in L. dentipes is biphasic, in which the posterior body part invariably moults first. The guarding male aids the female partner in the removal of the moulted exoskeleton. Mating occurs immediately after the posterior body exuviates. The male leaves the female after copulation and goes in search of another receptive female, demonstrating a polygamous mating system in these isopods. The mated females also re-mate with several other males without mate guarding. Females that had mated several times produced more young, compared to females mated only once in the laboratory. Female receptivity ceases following moulting of the anterior half. Intrasexual encounters among males lead to the large males acquiring receptive females. This study reveals interesting deviations from the general pattern of mate guarding already reported in other isopods and decapods. The evolutionary and ecological significances of mate guarding, intrasexual and intersexual conflicts, found in these semi-terrestrial isopods, are discussed.     

Male Gryllus bimaculatus Guard Females to Delay Them from Mating with Rival Males and to Obtain Repeated Copulations

Three hypotheses for the function of postcopulatory mate guarding were tested in the field cricket Gryllus bimaculatus De Geer. The duration of spermatophore attachment was greater in the absence than in the presence of a guarding male. The ejaculate protection hypothesis was, therefore, rejected. The duration of mate guarding was found to be equal to the interval between copulations, supporting the spermatophore renewal hypothesis. In support of the rival exclusion hypothesis, the presence of a guarding male did increase the duration of spermatophore attachment when a rival male was also present. The presence of a guarding male also delayed the female from mating with the rival male. Female mating status had a significant effect on the duration of spermatophore attachment. Females mating for the first time retained the spermatophore for a significantly longer period of time than females that had mated previously.