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.     

Age-related and individual differences of reproductive success in male and female barbary macaques (Macaca sylvanus)

Age-related and individual differences in longterm reproductive success were analyzed in two social groups of free-ranging Barbary macaques. Maternity data were obtained from continuous birth records and paternity was determined with oligonucleotide-fingerprinting. The fathers of 246 of 286 investigated individuals could be identified. They were born during a 14-year period and represented 73 and 34% of all known offspring from the females of the study groups B/F and C, respectively. Only these infants were considered when comparing male reproductive success with that of females. The necessary adjustment of the female data resulted in small deviations from the true values in one group, but substantially increased individual differences in female fertility in the second group. Subadult males, 4.5 – 6.5 yrs old, had a much lower reproductive success than adult males (7.5 – 25 yrs old) and same-aged females. Reproductive success of adult males was not significantly affected by age, while females invariably ceased reproduction during the first half of the third decade of life. Males were more likely than females to leave no offspring, unless they survived 9 – 10 yrs of age. The number of years with breeding opportunities was important for male reproductive success but less significant than that for females. Reproductive success of several males during the 14-year study period was similar to or even exceeded that possible for a female in her whole lifetime. Variance of male reproductive success significantly exceeded that of females in both study groups.     

Inbreeding avoidance and female mate choice shape reproductive skew in capuchin monkeys (Cebus capucinus imitator)

Reproductive skew in multimale groups may be determined by the need for alpha males to offer reproductive opportunities as staying incentives to subordinate males (concessions), by the relative fighting ability of the alpha male (tug‐of‐war) or by how easily females can be monopolized (priority‐of‐access). These models have rarely been investigated in species with exceptionally long male tenures, such as white‐faced capuchins, where female mate choice for novel unrelated males may be important in shaping reproductive skew. We investigated reproductive skew in white‐faced capuchins at Sector Santa Rosa, Costa Rica, using 20 years of demographic, behavioural and genetic data. Infant survival and alpha male reproductive success were highest in small multimale groups, which suggests that the presence of subordinate males can be beneficial to the alpha male, in line with the concession model's assumptions. None of the skew models predicted the observed degree of reproductive sharing, and the probability of an alpha male producing offspring was not affected by his relatedness to subordinate males, whether he resided with older subordinate males, whether he was prime aged, the number of males or females in the group or the number of infants conceived within the same month. Instead, the alpha male's probability of producing offspring decreased when he was the sire of the mother, was weak and lacked a well‐established position and had a longer tenure. Because our data best supported the inbreeding avoidance hypothesis and female choice for strong novel mates, these hypotheses should be taken into account in future skew models.     

Life history variables of wild troops of formosan macaques (Macaca cyclopis) in Kenting,Taiwan

A study on population dynamics of wild Formosan macaques (Macaca cyclopis) in Kenting, southern Taiwan, was conducted from March 1985 to August 1990. At first, only one monkey troop was studied. It fissioned in 1987 and both of the daughter troops have been observed since then. Total number of animals increased from 10 to 29 over the years, but the sizes of individual troops have never been more than 20. Seasonality in breeding has been detected: copulations were concentrated in the period from November to January and 75% of all the 28 births occurred between April and June. Time of birth by parous females without offspring from the preceding year was earlier than that of lactating females. Young females gave their first births at 4 or 5 years of age. Total birth rate over the study period was 0.8 infant per female per year. Hunting was the main cause of death while natural mortality rate was low for the animals. There was only one adult male in each troop for most of the time. Troop males in the two daughter troops have been replaced two or three times in the three years by some solitary males that moved around in the area. The reproductive parameters of Formosan macaques in Kenting were found to be more similar to that of rhesus monkeys than to Japanese macaques. And a case of higher reproductive success in a high-ranking matriline was reported.     

Male rank,reproductive behavior,and reproductive success in free-ranging rhesus macaques

Paternity assessment through DNA fingerprinting by synthetic oligonucleotide probes was applied to one birth cohort in a social group of free-ranging rhesus macaques (Macaca mulatta) on Cayo Santiago. The 11 group males and 9 males from other groups were observed mating with the females. Paternity was determined for 11 of the 15 infants. Male dominance rank was not associated with reproductive success. High-ranking resident males (N=5) sired 27% of the infants born during a one-year study. Four of the 11 infants of known paternity were sired by males of other social groups. The four infants of unknown paternity were sired either by males not observed mating with the females or the low-ranking male who was not fingerprinted. Male dominance rank was not associated with reproductive activity during conception cycles. These results suggest that the effect of rank on male reproductive success is not a predictable correlation, but a conditional probability.     

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.     

Sex differences in the drivers of reproductive skew in a cooperative breeder

Many cooperatively breeding societies are characterized by high reproductive skew, such that some socially dominant individuals breed, while socially subordinate individuals provide help. Inbreeding avoidance serves as a source of reproductive skew in many high‐skew societies, but few empirical studies have examined sources of skew operating alongside inbreeding avoidance or compared individual attempts to reproduce (reproductive competition) with individual reproductive success. Here, we use long‐term genetic and observational data to examine factors affecting reproductive skew in the high‐skew cooperatively breeding southern pied babbler (Turdoides bicolor). When subordinates can breed, skew remains high, suggesting factors additional to inbreeding avoidance drive skew. Subordinate females are more likely to compete to breed when older or when ecological constraints on dispersal are high, but heavy subordinate females are more likely to successfully breed. Subordinate males are more likely to compete when they are older, during high ecological constraints, or when they are related to the dominant male, but only the presence of within‐group unrelated subordinate females predicts subordinate male breeding success. Reproductive skew is not driven by reproductive effort, but by forces such as intrinsic physical limitations and intrasexual conflict (for females) or female mate choice, male mate‐guarding and potentially reproductive restraint (for males). Ecological conditions or “outside options” affect the occurrence of reproductive conflict, supporting predictions of recent synthetic skew models. Inbreeding avoidance together with competition for access to reproduction may generate high skew in animal societies, and disparate processes may be operating to maintain male vs. female reproductive skew in the same species.     

扩散或不扩散：雄性太行山猕猴繁殖成功比较研究

典型的猕猴（Macaca multta）社群为多雄多雌型,雌性留群并形成母系单元,雄性多在亚成年或成年期离开出生群,而群内成年雄性多为外部迁入个体。雄性的迁出被认为可降低近亲繁殖或提升繁殖成功。然而,诸多野外数据显示,少数本群出生雄性个体会居留于出生群一年或数年。尽管驱动雄性离群的因素较复杂（如社会关系、近亲回避、繁殖成功）,但繁殖成功的差异可能是驱动雄性离群的主导因素。为探讨居留于出生群是否影响雄性的繁殖成功,于2010年3月至2014年1月,在太行山猕猴国家级自然保护区王屋山地区,以一群野生太行山猕猴为研究对象,采用非损伤取样法并结合分子生物学方法,分析了群内出生和迁入成年雄性个体的繁殖成功（以子代数量评估）。研究发现：(1)群内51只子代个体中有36只个体可以匹配到其遗传学父亲;(2)4个迁入雄性繁衍了34个子代,仅1只群内出生雄性ZM繁衍了2只子代,但群内出生的雄性BB未匹配到子代。本研究提示,迁入雄性较本群出生雄性的繁殖成功较高,即迁移有助于繁殖成功的提升。     

Paternity in wild ring‐tailed lemurs (Lemur catta): Implications for male mating strategies

In group‐living species with male dominance hierarchies where receptive periods of females do not overlap, high male reproductive skew would be predicted. However, the existence of female multiple mating and alternative male mating strategies can call into question single‐male monopolization of paternity in groups. Ring‐tailed lemurs (Lemur catta) are seasonally breeding primates that live in multi‐male, multi‐female groups. Although established groups show male dominance hierarchies, male dominance relationships can break down during mating periods. In addition, females are the dominant sex and mate with multiple males during estrus, including group residents, and extra‐group males—posing the question of whether there is high or low male paternity skew in groups. In this study, we analyzed paternity in a population of wild L. catta from the Bezà Mahafaly Special Reserve in southwestern Madagascar. Paternity was determined with 80–95% confidence for 39 offspring born to nine different groups. We calculated male reproductive skew indices for six groups, and our results showed a range of values corresponding to both high and low reproductive skew. Between 21% and 33% of offspring (3 of 14 or three of nine, counting paternity assignments at the 80% or 95% confidence levels, respectively) were sired by extra‐troop males. Males siring offspring within the same group during the same year appear to be unrelated. Our study provides evidence of varying male reproductive skew in different L. catta groups. A single male may monopolize paternity across one or more years, while in other groups, >1 male can sire offspring within the same group, even within a single year. Extra‐group mating is a viable strategy that can result in extra‐group paternity for L. catta males.     

Differential reproductive success and facultative adjustment of sex ratios among captive female bonnet macaques (Macaca radiata)

In a group of captive bonnet macaques (Macaca radiata) housed at the California Primate Research Center, variance in reproductive success among females is primarily due to differences in infant survival. The infants of low-ranking females have a smaller probability of surviving to 6 months of age than do the infants of other females. In addition, the juvenile daughters of low-ranking females are more vulnerable to behaviourally induced mortality than are other immature animals. Observational evidence indicates that this mortality is the direct result of aggression by unrelated, higherranking adult females. Although infants' sex is not consistently related to survival, yearly fluctuations in the survival of male and female infants are reflected in the extent and direction of the skew in the sex ratio of offspring produced the following year. Years in which the highest proportion of male infants survive are followed by years in which the largest proportions of the birth cohorts are composed of males, and years in which the largest proportions of females survive are followed by years in which the largest proportions of birth cohorts are composed of females. For infant females the probability of surviving is reduced when a substantial proportion of the birth cohort is composed of females. The same pattern is evident among the sons of low-ranking females. The adaptive significance of behaviourally induced variation in reproductive success among females is considered in relation to these data.     

Troop history,female reproductive strategies and timing of male change in Hanuman langurs,Presbytis entellus

Female reproductive data are presented from 9 years of longitudinal observations on two troops of Hanuman langurs (Presbytis entellus) living around Jodhpur, India. On the basis of 89 live births interbirth intervals were calculated to examine the effect of demographic factors on reproductive behaviour and troop composition. Sex of an infant seems to influence the length of intervals which are longer after the birth of female infants at an average of 1.7 months. It is suggested that this may be an outcome of differential maternal investment by allocating more time and energy towards female infants who run a higher mortality risk than male infants, at least up to an age of 27 months. Troopspecific interbirth intervals are influenced by social events. If the last infant is still alive when the next one is conceived, the intervals are significantly longer than after the premature loss of an infant (Bijolai troop: 15.6 vs. 12.1 months; Kailana-1 troop: 16.7 vs. 11.4 months). During undisturbed male tenureship intervals are shorter than after a male change (Bijolai troop: 14.3 vs. 16.0 months; Kailana-I troop: 15.6 vs. 17.5 months). Thus the frequency of male changes can influence the demography of a troop. Furthermore, the data suggest that take-overs are optimally timed by males. New males tend to take over a troop when most of the females are cycling.     

Reproductive efficiency of captive Chinese- and Indian-origin rhesus macaque (Macaca mulatta) females

Reproductive and survival records (n=2,913) from 313 Chinese-origin and 365 Indian-derived rhesus macaques at the Tulane National Primate Research Center (TNPRC) spanning three generations were studied. Least-squares analysis of variance procedures were used to compare reproductive and infant survival traits while proportional hazards regression procedures were used to study female age at death, number of infants born per female, and time from last birth to death. Chinese females were older at first parturition than Indian females because they were older when placed with males, but the two subspecies had similar first postpartum birth interval (1st PPBI) and lifetime postpartum birth interval (LPPBI). Females that gave birth to stillborn infants had shorter first postpartum birth intervals (1st PPBI) than females giving birth to live infants. Postpartum birth intervals decreased in females from age 3 to 12 but then increased again with advancing age. Chinese infants had a greater survival rate than Indian infants at 30 days, 6 months, and 1 year of age. Five hundred and forty-three females (80.01%) had uncensored, or true records for age at death, number of infants born per female, and time from the birth until death whereas 135 females (19.91%) had censored records for these traits. Low- and high-uncensored observations for age at death were 3 and 26 years for Chinese, and 3 and 23 years for Indian females. Uncensored number of infants born per female ranged from 1 to 15 for Chinese females and 1 to 18 for Indian females. Each of these traits was significantly influenced by the origin×generation interaction in the proportional hazards regression analyses, indicating that probabilities associated with age at death, number of infants born per female, and time from last birth to death for Chinese and Indian females did not rank the same across generations.     

Strong male/male competition allows for nonchoosy females: high levels of polygynandry in a territorial frog with paternal care

Our knowledge about genetic mating systems and the underlying causes for and consequences of variation in reproductive success has substantially improved in recent years. When linked to longitudinal population studies, cross-generational pedigrees across wild populations can help answer a wide suite of questions in ecology and evolutionary biology. We used microsatellite markers and exhaustive sampling of two successive adult generations to obtain population-wide estimates of individual reproductive output of males and females in a natural population of the Neotropical frog Allobates femoralis (Aromobatidae), a pan-Amazonian species that features prolonged iteroparous breeding, male territoriality and male parental care. Parentage analysis revealed a polygynandrous mating system in which high proportions of males (35.5%) and females (56.0%) produced progeny that survived until adulthood. Despite contrasting reproductive strategies, successfully reproducing males and females had similar numbers of mating partners that sired the adult progeny (both sexes: median 2; range 1-6); the numbers of their offspring that reached adulthood were also similar (both sexes: median 2; range 1-8). Measures of reproductive skew indicate selection on males only for their opportunity to breed. Reproductive success was significantly higher in territorial than in nonterritorial males, but unrelated to territory size in males or to body size in both sexes. We hypothesize that female polyandry in this species has evolved because of enhanced offspring survival when paternal care is allocated to multiple partners.     

Male reproductive competition in spawning aggregations of cod (Gadus morhua, L.)

Reproductive competition may lead to a large skew in reproductive success among individuals. Very few studies have analysed the paternity contribution of individual males in spawning aggregations of fish species with huge census population sizes. We quantified the variance in male reproductive success in spawning aggregations of cod under experimental conditions over an entire spawning season. Male reproductive success was estimated by microsatellite-based parentage analysis of offspring produced in six separate groups of spawning cod. In total, 1340 offspring and 102 spawnings distributed across a spawning season were analysed. Our results show that multiple males contributed sperm to most spawnings but that paternity frequencies were highly skewed among males, with larger males on average siring higher proportions of offspring. It was further indicated that male reproductive success was dependent on the magnitude of the size difference between a female and a male. We discuss our results in relation to the cod mating system. Finally, we suggest that the highly skewed distribution of paternity success observed in cod may be a factor contributing to the low effective population size/census population size ratios observed in many marine organisms.     

Behavioural dominance and reproductive success in female Japanese monkeys (Macaca fuscata)

Eight years of reproductive data (including 248 births) from a translocated troop of Japanese monkeys (Macaca fuscata) living in a 42-ha enclosure provided three measures of female reproductive success: fecundity, survival of infants to 1 year of age, and age at first parturition. No significant relationship was found between social dominance and these measures. Social dominance was considered with respect to both matrilineal and individual female rank. Additional data on female dominance ranks over four generations of adult females revealed no significant concordance over time. The finding that ranks may not be stable over the lifetime of a female is a significant one because the variation in reproductive success among the females of a group is likely to be further diminished by any instability. For 34 females that were adults for the 8-year period considered, there was no significant correlation between the average rank of a female and either fecundity or survivorship of infants to 1 year of age. These data considered along with the results of other studies of female dominance and reproduction suggest that any effect of female social dominance on reproductive success is probably dependent upon resource availability, with significant benefits accruing to high-ranking individuals only during subsistence periods. It is suggested that dominance competition among female macaques may be a behavioural strategy with a variable payoff.     

Measuring male-female relationships during the mating season in wild Japanese macaques (Macaca fuscata yakui)

Heterosexual relationships during one mating season were examined in a wild troop of Japanese macaques (Macaca fuscata yakui) on Yakushima Island, Japan. Validation tests of putative mate choice behaviors demonstrated that female initiation and maintenance of proximity, female lookback at the male, and sexual presents to the male, were associated with increased mating. Male grooming the female was also associated with increased mating. Ten dyadic social behaviors were subject to principal components analysis to empirically define behavioral dimensions of male-female relationships. The analysis yielded four relationship dimensions: ‘Mutual Choice and Male Coercion,’ ‘Female Choice’ (two types), and ‘Mutual Choice’ Dyads tended to be characterized by more than one dimension. The results suggested that females sought matings with multiple males of various dominance ranks. Female relationships with high ranking males contained elements of male coercion and mate guarding, however, because these males attempted to inhibit females from mating with lower ranking males. The correlation between each relationship dimension and mating success depended, in part, on the dominance rank of males. Relationships involving high ranking males, which were most likely to contain elements of male coercion and mate guarding, were associated with mating success. Relationships involving low ranking males, which usually lacked such coercive elements. were less strongly correlated with mating success. These results, obtained from a wild troop, are compared to those previously obtained in captive and provisioned groups of Japanese macaques.     

Reproductive success in reindeer males in a herd with varying sex ratio

In polygynous species, male reproductive success is often correlated with dominance status of individual males and sex ratio in the population. Reindeer, Rangifer tarandus, is a polygynous species, and here we compared the variation in male reproductive success and dominance status during two successive years in a herd with a male:female sex ratio of 1:7 and 1:3. Copulations were recorded, together with data on male dominance hierarchy and size of mating groups. Male reproductive success was estimated by paternity analysis of calves using microsatellite DNA markers. The distribution of reproductive success among the males was highly skewed for both years with the most dominant male also being the most successful. The largest mating group was established in the herd with the least skew in sex ratio. In this herd some of the adult males present were less reproductively successful than some of the more subordinate younger males. Estimates of the mating group size of males, correcting for dominance status when more than one male is present in the groups, gave good prediction of individual males' reproductive success.     

Reproductive skew and relatedness in social groups of European badgers, Meles meles

Reproductive skew is a measure of the proportion of individuals of each sex that breed in a group and is a valuable measure for understanding the evolution and maintenance of sociality. Here, we provide the first quantification of reproductive skew within social groups of European badgers Meles meles , throughout an 18-year study in a high-density population. We used 22 microsatellite loci to analyse within-group relatedness and demonstrated that badger groups contained relatives. The average within-group relatedness was high ( R =  0.20) and approximately one-third of within-group dyads were more likely to represent first-order kin than unrelated pairs. Adult females within groups had higher pairwise relatedness than adult males, due to the high frequency of extra-group paternities, rather than permanent physical dispersal. Spatial clustering of relatives occurred among neighbouring groups, which we suggest was due to the majority of extra-group paternities being attributable to neighbouring males. Reproductive skew was found among within-group candidate fathers ( B  = 0.26) and candidate mothers ( B  = 0.07), but not among breeding individuals; our power to detect skew in the latter was low. We use these results to evaluate reproductive skew models. Although badger society best fits the assumptions of the incomplete-control models, our results were not consistent with their predictions. We suggest that this may be due to female control of paternity, female–female reproductive suppression occurring only in years with high food availability resulting in competition over access to breeding sites, extra-group paternity masking the benefits of natal philopatry, and/or the inconsistent occurrence of hierarchies that are linear when established.     

Sexual selection in a lekking bird: the relative opportunity for selection by female choice and male competition

Leks are classic models for studies of sexual selection due to extreme variance in male reproductive success, but the relative influence of intrasexual competition and female mate choice in creating this skew is debatable. In the lekking lance-tailed manakin (Chiroxiphia lanceolata), these selective episodes are temporally separated into intrasexual competition for alpha status and female mate choice among alpha males that rarely interact. Variance in reproductive success between status classes of adult males (alpha versus non-alpha) can therefore be attributed to male-male competition whereas that within status largely reflects female mate choice. This provides an excellent opportunity for quantifying the relative contribution of each of these mechanisms of sexual selection to the overall opportunity for sexual selection on males (I males). To calculate variance in actual reproductive success, we assigned genetic paternity to 92.3% of 447 chicks sampled in seven years. Reproduction by non-alphas was rare and apparently reflected status misclassifications or opportunistic copulations en route to attaining alpha status rather than alternative mating strategies. On average 31% (range 7-44%, n=6 years) of the total I males was due to variance in reproductive success between alphas and non-alphas. Similarly, in a cohort of same-aged males followed for six years, 44-58% of the total I males was attributed to variance between males of different status. Thus, both intrasexual competition for status and female mate choice among lekking alpha males contribute substantially to the potential for sexual selection in this species.     

The association between rank and reproductive success of male rhesus monkeys

The paternity of 202 of 220 offspring of rhesus monkeys housed in six separate half-acre field cages at the California Primate Research Center was determined by genetic marker techniques. Reproductive success of the adult males was statistically significantly correlated (r = 0.76, P <0.0005) with rank. Marked systematic changes in reproductive success were, however, observed for two adult males during the three years covered by this study. Based upon these results and those of another study, it is argued that changes in rank position typically follow, rather than precede, changes in reproductive success.