Reproductive success in relation to dominance rank in the absence of prime-age males in Barbary macaques

In some primate species dominance rank of males is correlated with reproductive success, whereas in other species this relationship is inconsistent. Barbary macaques (Macaca sylvanus) live in a promiscuous mating system in which males are ranked in a dominance hierarchy that influences their access to females. High-ranking males usually monopolize fertile females during their estrous period and show increased mating activities. Subadult males generally rank below adult males. For Barbary macaque females in the Gibraltar colony, there was no correlation between dominance status and reproductive success. Paternity data for 31 offspring collected over four consecutive breeding seasons were used to test whether male social rank was associated with reproductive success and whether reproductive success was mainly confined to a small number of males. Genetic variation was assessed using 14 microsatellite markers for a dataset of 127 individuals sampled in all five social groups of the Gibraltar colony. Paternity analysis was conducted for offspring in one social group only, where all in-group males were sampled. Eighty-three percent of the offspring could be assigned to an in-group candidate father; none of the extra-group males appeared to have sired an infant. Male dominance rank was not found to contribute to the observed variation in male reproductive output. Fifty-nine percent of the offspring was sired by two low-ranking males, whereas the two top-ranking males sired one-fifth. A highly significant correlation was found for male age and dominance rank. Reproductive success of subadult males might be explained by the gap in the age distribution of male group members. These missing prime males are usually regarded as serious competitors for older males. Subadult males may have gained easier access to females in their absence. In addition, the presence of inbreeding avoidance mechanisms, which might also have overpowered possible rank effects, cannot be excluded.     

Correlates of Male Consortship Rate in Free-Ranging Rhesus Macaques (Macaca mulatta)

Male–male competition for access to receptive females can take the form of nonrecurring fights and/or a sustained contest over mating opportunities. Male physical condition has been linked to dominance rank and reproductive success in species characterized by intrasexual fights for dominance and access to females. In group-living species characterized by endurance rivalry, however, factors contributing to male reproductive success are less well understood. In such species, particularly seasonally breeding ones with low sexual dimorphism and seniority-based rank, age and social factors other than rank may prove important. In the absence of genetic data, male mate guarding or consortship can serve as an indicator of male reproductive success. To evaluate the contribution of age and intragroup sociality to male consortship rate, I collected behavioral data during one nonmating and one mating season in two social groups of free-ranging rhesus macaques that experience no predation or food scarcity. Higher-ranking males, younger males, or males that exhibited lower rate of intrasexual aggression had higher consortship rates. Male–female dyads that groomed outside consortship did not form consortships as often as dyads that did not engage in nonconsort grooming. This is the first study to identify the significance of male–male aggression and male–female affiliation to male consortship rate in a species characterized by endurance rivalry, high male rank stability, and strong female mate choice. Social behaviors and male age may be particularly important in determining male reproductive success in populations experiencing high food availability and a lack of predation, which are typical of an increasing number of vertebrates in areas densely populated by humans.     

Application of paternity discrimination by DNA polymorphism to the analysis of the social behavior of primates

Paternity in many primate species cannot be established reliably on behavioral grounds. For instance, Japanese macaques (Macaca fuscata) have a multi-male group structure and promiscuous mating patterns. On the other hand, accurate evaluation of male reproductive success is needed to analyze primate behavior. DNA finger-printing techniques were applied to 2 captive groups of Japanese macaques in the Primate Research Institute of Kyoto University for identification of paternity. Also, mating behavior of a captive group was observed in order to compare the reproductive success of each male with that expected on the basis of his observed mating activity. The number of offspring of full adult males was not related to their social rank although the number of copulations with ejaculation was highly correlated with their social rank. Monitoring of the female sexual cycles from the plasma profiles of gonadotropins and ovarian hormones suggested that males could not choose females at days of ovulation. The results of two-free-ranging wild troops, like those of the captive groups, indicated that high-ranking males could not monopolize the paternity of offspring. The results of paternity discrimination in Japanese macaques were compared with results from patas monkeys (Erythrocebus patas) in a discussion of social structure and male reproductive success. Some aspects of polymorphism detection techniques are also discussed.     

Polygamous mating system and protogynous sex change in the gobiid fish <Emphasis Type="Italic">Fusigobius neophytus</Emphasis>

Whereas mating behaviors and social structure have been studied extensively in monogamous hermaphroditic gobiid species, such studies are relatively limited for polygamous gobiid species. To investigate the reproductive strategy of polygamous gobies, mating groups of the common fusegoby Fusigobius neophytus were observed on reefs of Kuchierabu-jima Island, southern Japan. Males established mating nests on flat-rock surfaces within their territorial home ranges on sandy rubble flats. Females maintained independent home ranges outside the male home ranges during nonreproductive periods, but they shifted their home ranges to overlap with male ranges and actively visited male mating nests during their reproductive periods (1–3 days at ca. 7-day intervals). Females often changed mates during their serial mating. The mating system used by the common fusegoby fits with the definition of male-territory-visiting polygamy. The sex ratio within the study population was female-biased. Nest-holding males were significantly larger than females and were polygynous (mating with up to eight females). These characteristics fit well with the prediction of protogyny by the size-advantage model. Some of the females were observed to undergo functional sex changes to nest-holding males. In addition, small floating males demonstrated sneaking behavior. None of the floating males were derived from females that had changed sex, suggesting a diandric life-history pathway for F. neophytus.     

Effects of high density on spacing behaviour and reproduction in Akodon azarae: A fencing experiment

We studied the short term spacing behavioural responses of Pampean grassland mouse (Akodon azarae) with regard to population density in four 0.25 ha enclosures (two control and two experimental) in the 2011 breeding season. Based on the hypothesis that A. azarae breeding females exhibit spacing behaviour, and breeding males show a fusion spatial response, we tested the following predictions: (1) home range size and intrasexual overlap degree of females are independent of population density values; (2) at high population density, home range size of males decreases and the intrasexual home range overlap degree increases. To determine if female reproductive success decreases at high population density, we analyzed pregnancy rate, size and weight of litters, and period until fecundation in both low and high enclosure population density. We found that both males and females varied their home range size in relation to population density. Although male home ranges were always bigger than those of females in populations with high density, home range sizes of both sexes decreased. Females kept exclusive home ranges independent of density values meanwhile males decreased home range overlap in high breeding density populations. Although females produced litters of similar size in both treatments, weight of litter, pregnant rate and period until fecundation varied in relation to population density. Our results did not support the hypothesis that at high density females of A. azarae exhibit spacing behaviour neither that males exhibit a fusion spatial response.     

Social Dominance among Male Meadow Voles is Inversely Related to Reproductive Success

Intrasexual selection can occur through direct aggressive interactions between males for access to females. We tested the relationship between social dominance and male reproductive success among meadow voles, Microtus pennsylvanicus. Dominance ranks of wild‐caught males were determined using neutral arena trials, with the winner of two of three trials considered dominant. These males were then released into field enclosures and allowed to visit females housed in nestboxes for 8 wk, and males’ home range sizes were determined using weekly grid trapping. Male reproductive success was determined using molecular paternity analysis (six microsatellite primers) for all pups born during the field experiment. Males with higher dominance ranks had larger home ranges. However, male dominance rank was not predictive of the number of total visits to females’ nestboxes or the number of visits to each male's most frequently visited nestbox. Males that made more visits to nestboxes sired more litters. Males that had higher dominance ranks sired fewer litters. These results suggest that there is a reproductive disadvantage to having higher dominance rank among male meadow voles.     

The effects of sexual selection and life history on the genetic structure of redfronted lemur, Eulemur fulvus rufus, groups

We examined genetic consequences of basic predictions of life history and sexual selection theory in a wild population of redfronted lemurs. Because group living in lemurs evolved independently from other primates, and because polygynous lemurs deviate in several sexually selected traits from theoretical predictions, data on genetic correlates of their social and mating systems can make important contributions to studies of convergence in social evolution, but such data are not available from wild populations. We extracted DNA from tissue samples obtained from 59 animals living in Kirindy forest, Madagascar, and examined individual variability at several microsatellite loci and the mitochondrial D-loop. We found that closely related females of a single matriline formed the core of the four main study groups. Virtually all haplotypes of adult males differed from those of coresident females, and many male haplotypes were represented by only one or two individuals. Paternity analyses for infants from groups with detailed behavioural data revealed that a disproportionate share of infants were sired by the central, dominant male of a group, despite promiscuous mating. Extragroup paternities were not detected. The skew in male reproductive success cannot be reconciled with the lack of sexual dimorphism and the even adult sex ratios. We therefore conclude that these group-living lemurs converge with many other primates in sex-specific life history trajectories, including female philopatry and male dispersal, but that the observed skew in male reproductive success makes the apparent lack of adaptation to intrasexual selection in certain behavioural, demographic and morphological traits even more puzzling. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Male competition and its hormonal correlates in Assamese macaques (Macaca assamensis)

In polygynous mammals, where males compete over access to females, the potential of males to monopolize reproductive females largely depends on the spatio-temporal distribution of reproductive females. We investigated mechanisms of male reproductive competition and its hormonal basis in a cercopithecine species with reduced contest potential owing to female reproductive synchrony and concealed ovulation. Over 16 months including two mating seasons we collected 1218 h of observational focal animal data and 1254 fecal samples of 11-12 adult and large subadult male Assamese macaques (Macaca assamensis) living in their natural habitat in Thailand. Androgen output along with aggressive behavior showed a seasonal pattern, with highest values being obtained by all males during the mating season and by those males experiencing acute social challenges, e.g. rank change and dispersal. Individual androgen levels and rates of attacks were linked across the study period, suggesting a promoting function of androgens for aggressive behavior. Dominance rank predicted neither mating success nor androgen levels consistently, indicating a reduced selective advantage of high social status for general mating access. However, high ranking males engaged in extended consortships with reproductive females. Distribution of consortships across males followed a priority of access distribution, with the two top ranking males accounting for 75% of consort activity, suggesting that high social status also carries fitness benefits in a species characterized by low contest potential.     

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.     

Determinants of male mating success in a large group of Barbary macaques (Macaca sylvanus) at Affenberg Salem

Male mating activities in relation to the likelihood of ovulation and conception were studied in a large group of semifree-ranging Barbary macaques (Macaca sylvanus) during two successive mating seasons. In both mating seasons, adult males attained a significantly higher mating success than subadult males, and they monopolized high ranking females more effectively than low ranking females during the period when conception was most probable. Also, in both mating seasons male rank was significantly correlated with male mating success if all sexually mature males were included. Nevertheless, mating success was not a linear function of age or rank. In both mating seasons mating success of 5-year-old males was much higher than that of dominant but peripheralized 6- and 7-year-old males. Moreover, a significant correlation between rank and measures of mating success among adult males was found in the second but not in the first mating season. The results indicate that mating and, most probably, reproductive success of male Barbary macaques is dependent on the male's social position in the group, which is defined not only by the outcome of dyadic agonistic encounters but also by the ability to get a central position in the group, and on the stability of rank relations.     

The association between rank,mating effort,and reproductive success in male Barbary macaques (Macaca sylvanus)

The association between social rank, mating effort, and reproductive success of male Barbary macaques (Macaca sylvanus) has been evaluated by longterm behavioral observations and subsequent paternity determination via oligonucleotide DNA fingerprinting in a large semifreeranging group. All offspring born between 1985 and 1988 that survived to at least 1 year of age (n=75) were available for paternity testing. The exclusion of all but one of the potential fathers from paternity was possible in 70 cases (93%). Mating activities were recorded using ad lib. and focal female sampling techniques. The analysis of male mating effort was restricted to the most likely days of conception. Male rank correlated significantly with male mating success in all four breeding seasons and with male reproductive success in three of the four seasons. Mating success and reproductive success also showed a significant correlation, with the exception of one breeding season, in which the proportion of males per fertilizable female was especially high. Poor mating success was almost always associated with poor reproductive success, while good mating success was less predictive for a male's actual reproductive success. This was apparently a consequence of sperm competition, resulting from the promiscuous mating system. Male mating success is not necessarily an unreliable indicator for reproductive success, provided that sufficient sample sizes are available and that conception periods can be determined. Sperm competition and other factors may weaken the association, however.     

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.     

Male rank and reproductive activity in Savanna baboons

Access to sexually receptive baboon females has been linked to male dominance rank. An intensive 19-month field study of mate choice and mate competition among savanna baboons was undertaken in order to elucidate those factors influencing mating success. During this study, male agonistic rank was not correlated with male mating success among adult males. However, the inclusion of adolescent males into the analysis yielded significant correlations between rank and mating success. Examination of prior fieldwork revealed that no baboon field study has conclusively demonstrated a significant correlation between male rank and reproduction among adult males. Most studies reporting a correlation between male rank and reproduction have included subadult males in the analysis. It is concluded that male rank is an unreliable predictor of male reproductive activity among adult male baboons. A low agonistic rank need not reduce male mating success because adult male baboons utilize a variety of reproductive tactics in gaining access to consort females.     

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.     

Mating Group Size and Stability in Reindeer Rangifer tarandus: The Effects of Male Characteristics,Sex Ratio and Male Age Structure

In polygynous mating systems, males compete intensely for mates and may mate several females during a single reproductive season. Accordingly, factors influencing the ability of males to control a larger number of females during the breeding season can provide information on the processes underlying sexual selection. In ungulates, age, body mass and social rank are considered good predictors of the reproductive success of males, but how male age structure and sex ratio in the population influence mating group (MG) dynamics has received little empirical testing. Between 1996 and 2005, we manipulated male age‐ and sex structure and monitored MG dynamics in a reindeer (Rangifer tarandus) population. We investigated the influence of male characteristics, percentage of males and male age structure on MG size and stability. We found that males with higher social rank (that were also older and heavier) controlled larger MGs (therefore had greater mating opportunities) and had more stable MGs (corresponding to a higher ability to maintain and control females) than males of lower social rank. Moreover, MG size and MG stability decreased as the percentage of males in the population increased, most likely resulting from greater male–male competition and increased female movements. Male age structure did not influence MG stability. Given the positive relationship between mating success and MG size (and likely MG stability), frequent female movements and intense competition among males to control females seem to be the principal components of reindeer MGs dynamic.     

The influence of female age on male mating preference and reproductive success in cabbage beetle,Colaphellus bowringi

The influence of female age on male mating preference and reproductive success has been studied using a promiscuous cabbage beetle, Colaphellus bowringi Baly （Coleoptera： Chrysomelidae）. In a simultaneous choice test, middle-aged females had significantly greater mating success than young and old females. In single pair trials, when paired with middle-aged virgin males, middle-aged females mated faster, copulated longer, and had greater fecundity and fertility than young or old females, while the longevity of males was not significantly affected by female age. This study on C. bowringi suggests that middle-aged females are more receptive to mating, which can result in the highest male reproductive success.     

Woodland fragmentation affects space use of Eurasian red squirrels

When habitats become fragmented, variation in patch size and quality are expected to impose changes on the spacing pattern and social organization of animal populations. General theory predicts different possible responses including shrinking home ranges (fission response), increasing range overlap (fusion) and incorporation of multiple patches in the home range (expansion response) as fragmentation increases. We studied space use and social organization in a metapopulation of red squirrels (Sciurus vulgaris) in 15 woodland fragments differing in size and tree species composition. Home ranges and core areas of males were larger than females, and fragmentation had different and complex effects on the spacing pattern of both sexes. In food-supplemented patches, high densities led to increased intra-sexual overlap. In linear-shaped patches, squirrels used smaller home ranges and core areas and had lower male–male and male–female overlap levels, independent of patch quality or size. Home range and core area size of males increased with patch size, and male core areas overlapped extensively those of other males and females. Hence males seemed to show a fission response only in some patches. In contrast, home range and core area size of females was not related with patch size, but decreased with habitat quality, supporting predictions of a fusion response and intra-sexual defense of food-based core areas. Hence, where patch size and shape strongly affected space use of male red squirrels, social organization of females was only affected in small, food-supplemented patches, suggesting that the basic spatio-social organization of adult females is very resistant to fragmentation.     

Space use by the Japanese fluvial sculpin, Cottus pollux, related to spatio-temporal limitations in nest resources

Space use by the Japanese fluvial sculpin, Cottus pollux, as related to nest availability was studied in a Japanese mountain stream. Males had larger home ranges than females before breeding. A measure of nest resource limitation was L < 1 and the same nest rock was used by two males successively in three cases, indicating a limited supply of suitable nest rocks for males. All males included the nest rocks in their home ranges, but the timing of nest occupation was apparently dependent on male size, suggesting the presence of male-male competition for the nest rocks. Females, on the other hand, exhibited two different patterns in space use, independent of body size: (1) they spawned in their home ranges, or (2) they spawned out of their home ranges and returned. Nest cavity area did not affect male reproductive success. Spatial separation between female home ranges and nest location was the main reason for the females' movement out of their home ranges. The limitation in the male mating phase (5.7 days on average) might also have forced the females to move out of their home range to spawn. The reason behind such temporal limitation in the male mating interval was discussed from the viewpoint of the energy cost accompanying male parental care.     

Spacing behaviour and its implications for the mating system of a precocial small mammal: an almost asocial cavyCavia magna ?

Socioecological models for small mammals attempt to explain the causal relations between the spatiotemporal distributions of food resources, females and males. We tested their predictions for a wild population of Cavia magna, a grazing, precocial rodent, by analysing spacing behaviour in relation to various demographic features. Between May 1999 and January 2001 we collected capture-recapture data on 309 individuals and monitored 55 females and 49 males by radiotelemetry in periodically inundated wetland in Uruguay. Cavies showed a nonstationary use of space: monthly home ranges drifted over the whole study site. Female home ranges overlapped with those of several others. Females were randomly distributed and we found no evidence for socially mediated reproductive synchrony. Males ranged over larger areas than females, showing even less site fidelity, and also overlapped with several rivals. This basic spacing system remained stable over a wide range of densities and sex ratios. Independent of sex, animals used overlap zones randomly with respect to each other. Significant dynamic (spatiotemporal) interaction was most frequent between males and females. However, interaction analyses revealed no evidence for stable social bonds between animals, regardless of sex. We suggest that unpredictable female locations prevent males monopolizing females spatially. Because females are solitary, males could monopolize only one female by maintaining close proximity, rendering a roaming mating tactic more successful. Our findings point to a solitary ‘social’ system and overlap promiscuity as the likely mating system for the C. magna population studied. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Reproductive success in the mandrill, Mandrillus sphinx: correlations of male dominance and mating success with paternity, as determined by DNA fingerprinting

Considerable controversy exists concerning possible effects of sexually selected phenotypes via intermale competition on reproductive success. The mandrill ( Mandrillus sphinx ) is an extreme example of evolution by sexual selection, and hence we have studied a semi-free-ranging colony of mandrills in Gabon to gather information on male rank, mating success and paternity, as determined by DNA fingerprinting. Two morphological variants or adult male were identified; 'fatted' males, with maximum secondary sexual coloration, which occupied dominant positions in the social group, and 'non-fatted' males, with muted secondary sexual adornments, smaller testes and lower plasma testosterone levels, which lived as peripheral/solitary individuals. DNA fingerprinting analyses on infants born over five successive years showed that only the two most dominant, fatted males in the group had fathered off spring. Throughout the annual mating season these males attempted to mate-guard and copulate with females during periods of maximal sexual skin tumescence. Male rank and mating success were strongly positively related and the alpha male sired 80–100% of the resulting offspring during three consecutive years. Non-fatted adult males and group associated subadult males engaged in infrequent, opportunistic matings and did not guard females. Loss of alpha status resulted in a fall in reproductive success, but the effect was gradual; the deposed alpha male continued to father 67% and 25% of infants born during the next two years. Thus these results of behavioural and genetic studies on mandrills demonstrate unequivocally that clear-cut relationships exist between male secondary sexual development, social dominance, copulatory behaviour and reproductive success in the social group.