Male Tenure Research Articles

Female‐biased dispersal in a bat with a female‐defence mating strategy

The ultimate causes for predominant male-biased dispersal (MBD) in mammals and female-biased dispersal (FBD) in birds are still subject to much debate. Studying exceptions to general patterns of dispersal, for example, FBD in mammals, provides a valuable opportunity to test the validity of proposed evolutionary pressures. We used long-term behavioural and genetic data on individually banded Proboscis bats (Rhynchonycteris naso) to show that this species is one of the rare mammalian exceptions with FBD. Our results suggest that all females disperse from their natal colonies prior to first reproduction and that a substantial proportion of males are philopatric and reproduce in their natal colonies, although male immigration has also been detected. The age of females at first conception falls below the tenure of males, suggesting that females disperse to avoid father-daughter inbreeding. Male philopatry in this species is intriguing because Proboscis bats do not share the usual mammalian correlates (i.e. resource-defence polygyny and/or kin cooperation) of male philopatry. They have a mating strategy based on female defence, where local mate competition between male kin is supposedly severe and should prevent the evolution of male philopatry. However, in contrast to immigrant males, philopatric males may profit from acquaintance with the natal foraging grounds and may be able to attain dominance easier and/or earlier in life. Our results on Proboscis bats lent additional support to the importance of inbreeding avoidance in shaping sex-biased dispersal patterns and suggest that resource defence by males or kin cooperation cannot fully explain the evolution of male philopatry in mammals.

Applicability of Age-Based Hunting Regulations for African Leopards

In species in which juvenile survival depends strongly on male tenure, excessive trophy hunting can artificially elevate male turnover and increase infanticide, potentially to unsustainable levels. Simulation models show that the likelihood of safe harvests can be improved by restricting offtakes to males old enough to have reared their first cohort of offspring to independence; in the case of African leopards, males were ≥7 years old. Here, we explore the applicability of an age-based approach for regulating trophy hunting of leopards. We conducted a structured survey comprising photographs of known-age leopards to assess the ability of wildlife practitioners to sex and age leopards. We also evaluated the utility of four phenotypic traits for use by trophy hunters to age male leopards in the field. Our logistic regression models showed that male leopard age affected the likelihood of survey respondents identifying the correct sex; notably, males <2 years were typically misidentified as females, while mature males (≥4 years) were sexed correctly. Mature male leopards were also more likely to be aged correctly, as were portrait photographs. Aging proficiency was also influenced by the profession of respondents, with hunters recording the lowest scores. A discriminant model including dewlap size, the condition of the ears, and the extent of facial scarring accurately discriminated among male leopard age classes. Model classification rates were considerably higher than the respective scores attained by survey respondents, implying that the aging ability of hunters could theoretically improve with appropriate training. Dewlap size was a particularly reliable indicator of males ≥7 years and a review of online trophy galleries suggested its wider utility as an aging criterion. Our study demonstrated that an age-based hunting approach is practically applicable for leopards. However, implementation would require major reform within the regulatory framework and the hunting industry.

Male greater sac-winged bats gain direct fitness benefits when roosting in multimale colonies

Social groups that are characterized by the presence of male kin are rare in mammals. Theory predicts that males reproducing in such groups need to overcome the costs of local mate competition, which are supposedly severe in polygynous or promiscuous mating systems. Here, we studied in a polygynous mammal with male philopatry whether male group size renders direct fitness benefits for males that could outweigh the costs of competing with related males for access to territories and mates. We used long-term behavioral observations and genetic data of the greater sac-winged bat to investigate the factors affecting lifetime breeding success (LBS) of harem males living in colonies that contain varying numbers of male residents. We show that tenure of harem males increased with the number of male coresidents and that harem male tenure explained a large proportion of variation in their LBS. Thus, our results provide evidence that males gain direct fitness benefits from a social organization in colonies that include additional harem territories and nonharem males. Immigration of males into colonies was significantly lower when nonharem males (young males that are often related to harem males) were permanently present in colonies, suggesting that larger male groups may be better able to maintain a patriline in a colony and thus also ensure future indirect fitness benefits. Key words: female-biased dispersal, lifetime breeding success, male tenure, Saccopteryx bilineata, social organization. [Behav Ecol]

Paternity and Dominance Loss in Male Breeders: The Cost of Helpers in a Cooperatively Breeding Mammal

Paternity insurance and dominance tenure length are two important components of male reproductive success, particularly in species where reproduction is highly skewed towards a few individuals. Identifying the factors affecting these two components is crucial to better understand the pattern of variation in reproductive success among males. In social species, the social context (i.e. group size and composition) is likely to influence the ability of males to secure dominance and to monopolize reproduction. Most studies have analyzed the factors affecting paternity insurance and dominance tenure separately. We use a long term data set on Alpine marmots to investigate the effect of the number of subordinate males on both paternity insurance and tenure of dominant males. We show that individuals which are unable to monopolize reproduction in their family groups in the presence of many subordinate males are likely to lose dominance the following year. We also report that dominant males lose body mass in the year they lose both paternity and dominance. Our results suggest that controlling many subordinate males is energetically costly for dominant males, and those unable to support this cost lose the control over both reproduction and dominance. A large number of subordinate males in social groups is therefore costly for dominant males in terms of fitness.

Troop Takeover and Reproductive Success of Wild Male Japanese Macaques on Yakushima Island (Macaca fuscata yakui)

Troop takeover is common in one-male primate groups, but there are few reports in multimale groups. Japanese macaques (Macaca fuscata) form multimale groups and males commonly join troops at the bottom rank. On Yakushima island, however, where group size is relatively small, entrance into groups at the alpha position is also observed. This paper reports on the general features of troop takeover, on the predictors of takeover events, and on the reproductive success of takeover males. Troop takeovers occurred only in the mating season; nontroop males (NTMs) did not cooperate with each other; former alpha males were rarely expelled from the troop; new alpha males did not commit infanticide; new alpha male tenure in the group was usually less than two years. Logistic regression analysis showed that the number of NTMs associating with a troop predicted the occurrence of troop takeover. Paternity discrimination revealed that 33.3% (3/9) of takeover males succeeded in siring offspring. Contrary to this low success rate, binary logistic regression analysis revealed that the takeover males can expect higher reproductive success compared to troop males. Entering a troop and out-competing the alpha male is one of many available strategies to attain reproductive success in male Japanese macaques.

Determinants of Paternity Success in a Group of Captive Vervet Monkeys (Chlorocebus aethiops sabaeus)

Paternity success of high-ranking primate males is affected by the number of males and the number of fertile females and their cycle synchrony. Female vervets in the wild show strong reproductive seasonality and do not advertise the ovulatory period with conspicuous signals or behavior. Because this makes it difficult for males to monopolize fertile females, it can be expected that male reproductive skew in this species is lower than in other cercopithecines living in multimale groups that advertise the ovulatory period. We assessed male reproductive success in a captive vervet group, initially consisting of 4 males and 12 unrelated females. Besides a general low reproductive skew, we predicted paternity success of the alpha males to be dependent on the overlap of synchronously fertile females, month into alpha male tenure, and housing conditions (the subjects were kept in a large park but had to be locked in a small indoor compartment during the winter months). Further, because the number of males reaching their prime increased over time, we predicted a decrease in reproductive success of the alpha male with increasing tenure length of the alpha male. To assess this we collected genetic samples from 27 of 32 offspring born into the group during 3 yr, using 7 polymorphic human microsatellite markers. Contrary to our predictions, reproductive success of the males occupying the alpha position during the study was among the highest found in cercopithecines, with the alpha males siring 78% of all offspring. The degree of overlapping fertile periods did not affect paternity success, nor did paternity success of the alpha male differ between the 2 housing conditions. Only the alpha male’s tenure length had an effect. Alpha male reproductive success decreased over time, which we attribute to either a shift in female mate choice toward younger males or to increased competition among the males in the later stage of the alpha male’s tenure. This study demonstrates the importance of assessing reproductive success of males throughout >1 season and should spawn more research into the role of female choice and postcopulatory mechanisms in this species.

Social dynamics of the golden snub‐nosed monkey (Rhinopithecus roxellana): female transfer and one‐male unit succession

Among primates that form multilevel societies, understanding factors and mechanisms associated with the movement of individuals between groups, clans, and one-male social units offers important insight into primate reproductive and social strategies. In this research we present data based on an 8-year field study of a multilevel troop of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains of China. Our study troop contained 78-126 individuals, and was usually organized into 6-8 one-male units (OMU). The majority of OMUs were composed of networks of unrelated females and their offspring. We found that 59.7% (43/72) of subadult and adult females in our study troop transferred between OMUs (n=66) or disappeared (n=7) from the troop. In the majority of cases, two or more females transferred together into new OMUs or troops. In R. roxellana, new OMUs formed in several ways. During 2001-2008, 16 adult males appeared in the study troop. Over this period, we observed 13 different males who became harem leaders either by taking over an existing harem or by attracting females from other OMUs into their harem. We also observed four OMUs from a neighboring troop to successfully immigrate into the study troop. The number of individuals in these newly immigrated OMUs was significantly smaller than that number of individuals in resident OMUs. During harem formation, fighting between adult males was rarely observed, and female mate choice appeared to play a crucial role in harem male recruitment and replacement. These results suggest that golden snub-nosed monkeys are organized in a nonmatrilineal social system. Female mate choice and possibly incest avoidance appear to play important roles in female transfer, male tenure, and OMU stability.

Female dispersal in a female-philopatric species, Cebus capucinus

[White-faced capuchins ( Cebus capucinus ) reside in multimale–multifemale groups characterized by female philopatry and frequent male dispersal. However, over the years we have observed five females immigrate into our study groups and 23 disappear/emigrate. We examined long-term demographic and behavioural data on three groups of C. capucinus residing in Santa Rosa, Costa Rica, between 1986 and 2007. During this time, 56 females resided in our study groups and as of June 2007, 23 were still present, ten were confirmed/presumed dead and 23 were missing. Here we review the circumstances surrounding the five immigrations and 23 missing females and evaluate three main hypotheses to explain female dispersal in a female philopatric species: inbreeding avoidance, reduction of intragroup feeding competition and infanticide avoidance. The two main predictions of the inbreeding avoidance hypothesis were not supported by our study; male tenure did not exceed female age at first birth and the majority of dispersers were parous females. The reduction in intragroup feeding competition hypothesis received moderate support; dispersing/disappearing females tend to leave during the dry season and they have fewer matrilineal kin than females remaining in their natal group. Our data were most consistent with the infanticide avoidance hypothesis in that females are more likely to disperse/disappear during years with male replacements, a time when infant deaths are also more common. These data provide further evidence of the large impact that the movement and actions of adult male white-faced capuchins have on the lives of females in this species., White-faced capuchins ( Cebus capucinus ) reside in multimale–multifemale groups characterized by female philopatry and frequent male dispersal. However, over the years we have observed five females immigrate into our study groups and 23 disappear/emigrate. We examined long-term demographic and behavioural data on three groups of C. capucinus residing in Santa Rosa, Costa Rica, between 1986 and 2007. During this time, 56 females resided in our study groups and as of June 2007, 23 were still present, ten were confirmed/presumed dead and 23 were missing. Here we review the circumstances surrounding the five immigrations and 23 missing females and evaluate three main hypotheses to explain female dispersal in a female philopatric species: inbreeding avoidance, reduction of intragroup feeding competition and infanticide avoidance. The two main predictions of the inbreeding avoidance hypothesis were not supported by our study; male tenure did not exceed female age at first birth and the majority of dispersers were parous females. The reduction in intragroup feeding competition hypothesis received moderate support; dispersing/disappearing females tend to leave during the dry season and they have fewer matrilineal kin than females remaining in their natal group. Our data were most consistent with the infanticide avoidance hypothesis in that females are more likely to disperse/disappear during years with male replacements, a time when infant deaths are also more common. These data provide further evidence of the large impact that the movement and actions of adult male white-faced capuchins have on the lives of females in this species.]

Höner et al. reply

Replying to: R. C. Van Horn, H. E. Watts & K. E. Holekamp , 10.1038/nature07122 (2008) We demonstrated that female mate-choice, rather than male inbreeding avoidance, resources or male–male competition, drives male-biased dispersal in spotted hyaenas (Crocuta crocuta)1. We further showed that females use two simple rules based on male tenure to choose their sires, and that males gain substantial fitness benefits by responding to these preferences1. Van Horn et al.2 accept our principal conclusions but claim that females base mate-choice on dispersal status rather than tenure. Their argument overlooks the fact that at least one of the two female mate-choice rules cannot be explained by dispersal status, and it is based on statistical analyses and a selection of males that we consider inappropriate for tests of female mate preference.

Factors affecting the reproductive success of dominant male meerkats

Identifying traits that affect the reproductive success of individuals is fundamental for our understanding of evolutionary processes. In cooperative breeders, a dominant male typically restricts mating access to the dominant female for extended periods, resulting in pronounced variation in reproductive success among males. This may result in strong selection for traits that increase the likelihood of dominance acquisition, dominance retention and reproductive rates while dominant. However, despite considerable research on reproductive skew, few studies have explored the factors that influence these three processes among males in cooperative species. Here we use genetic, behavioural and demographic data to investigate the factors affecting reproductive success in dominant male meerkats (Suricata suricatta). Our data show that dominant males sire the majority of all offspring surviving to 1 year. A male's likelihood of becoming dominant is strongly influenced by age, but not by weight. Tenure length and reproductive rate, both important components of dominant male reproductive success, are largely affected by group size and composition, rather than individual traits. Dominant males in large groups have longer tenures, but after this effect is controlled, male tenure length also correlates negatively to the number of adult females in the group. Male reproductive rate also declines as the number of intra- and extra-group competitors increases. As the time spent in the dominant position and reproductive rate while dominant explain > 80% of the total variance in reproductive success, group composition thus has major implications for male reproductive success.

Female-biased dispersal and patrilocal kin groups in a mammal with resource-defence polygyny.

In most mammals, dispersal rates are higher in males than in females. Using behavioural and genetic data of individually marked bats, we show that this general pattern is reversed in the greater sac-winged bat (Saccopteryx bilineata). Dispersal is significantly female biased and male philopatry in combination with rare male immigration causes a patrilineal colony structure. Female dispersal helps avoid father-daughter inbreeding, as male tenure exceeds female age at first breeding in this bat species. Furthermore, our data suggest that females may engage in extra-harem copulations to mate with genetically dissimilar males, and thus avoid their male descendants as mating partners. Acquaintance with the natal colony might facilitate territory takeover since male sac-winged bats queue for harem access. Given the virtual absence of male immigration and the possible lower reproductive success of dispersing males, we argue that enhancing the likelihood of settlement of male descendants could be adaptive despite local mate competition. We conclude that resource defence by males is important in promoting male philopatry, and argue that the potential overlap of male tenure and female first conception is the driving force for females to disperse.

The effect of male tenure and female mate choice on paternity in free‐ranging Japanese macaques

In this study, the paternity of all the infants born in 2002 and 2003 in a free-ranging Japanese macaque (Macaca fuscata) group at Arashiyama in Kyoto, Japan, was analyzed in relation to males' age, dominance rank, and tenure and females' mate choice. The fathers of 20 out of 23 infants were determined by DNA analyses. Central adult (high-ranking) males sired two infants, whereas peripheral adult (low-ranking) males sired 14 infants. Young males sired only one infant. Among adult males, tenure was the most dominant factor that negatively affected male reproductive success. The mating behavior of females who gave birth was also analyzed. The number of male copulations in the peri-fertilization period was positively correlated with the number of infants that they sired. Females copulated with central males with a long tenure only when fertilization was unlikely or impossible. The females probably avoided insemination by males with a long tenure and selected males with a shorter tenure as their mating partners during the ovulation period.

All-offspring dispersal in a tropical mammal with resource defense polygyny

In polygynous mammals, males are usually responsible for gene flow while females are predominantly philopatric. However, there is evidence that in a few mammalian species female offspring may disperse to avoid breeding with their father when male tenure exceeds female age at maturity. We investigated offspring dispersal and local population structure in the Neotropical bat Lophostoma silvicolum. The mating system of this species is resource defense polygyny, with the resource being active termite nests, excavated by single males, which are then joined by females. We combined field observations of 14 harems during 3 years and data about the genetic structure within and between these groups, calculated with one mitochondrial locus and nine nuclear microsatellite loci. The results show that both male and female offspring disperse before maturity. In addition, we estimated life span of excavated termite nests and the duration they were occupied by the same male. Our findings suggest that long male tenure of up to 30 months is indeed a likely cause for the observed dispersal by female offspring that can reach maturity at a low age of 6 months. We suggest that dispersal by offspring of both sexes may occur quite frequently in polygynous tropical bats and thus generally may be more common in mammals than previously assumed.

Resource quality or harem size: what influences male tenure at refuge sites in tree weta (Orthoptera: Anostostomatidae)?

Rather than seeking females directly, males in many animal species locate and defend sites that contain spatially limited resources essential for female survival and reproduction. In these cases, resident males successfully repelling conspecific rivals will mate with sexually receptive females that seek to use the resident’s resources. Theory predicts that if resources are limiting in nature, are costly to procure, and if residency at the resource site increases male reproductive success, each site should be monopolised by a single adult male. Moreover, if females aggregate at these sites, males should be sedentary and monopolise harems. This predicts that males should reside at resource sites longer than females and male tenure should be positively correlated with harem size. I address these hypotheses using a wild population of the Wellington tree weta, Hemideina crassidens, a sexually dimorphic insect in which males use mandibular weapons in fights to control resource sites (galleries in trees) required by females for diurnal refuge. In a longitudinal study using artificial galleries, I show that male tenure in a gallery is positively related to harem size and, contrary to prediction, not gallery size per se. Moreover, contrary to prediction, females are more sedentary than males: males appear to move frequently between galleries to search for novel mates. I show experimentally that galleries represent mating sites to males: males prefer galleries housing adult females whereas females prefer unoccupied galleries. Females likely avoid male-occupied galleries because they incur injuries when interacting with males.

Life history in male mandrills (Mandrillus sphinx): Physical development, dominance rank, and group association

We assess life history from birth to death in male mandrills (Mandrillus sphinx) living in a semifree-ranging colony in Gabon, using data collected for 82 males that attained at least the age of puberty, including 33 that reached adulthood and 25 that died, yielding data for their entire lifespan. We describe patterns of mortality and injuries, dominance rank, group association, growth and stature, and secondary sexual character expression across the male lifespan. We examine relationships among these variables and investigate potential influences on male life history, including differences in the social environment (maternal rank and group demography) and early development, with the aim of identifying characteristics of successful males. Sons of higher-ranking females were more likely to survive to adulthood than sons of low-ranking females. Adolescent males varied consistently in the rate at which they developed, and this variation was related to a male's own dominance rank. Males with fewer peers and sons of higher-ranking and heavier mothers also matured faster. However, maternal variables were not significantly related to dominance rank during adolescence, the age at which males attained adult dominance rank, or whether a male became alpha male. Among adult males, behavior and morphological development were related to a male's own dominance rank, and sons of high-ranking females were larger than sons of low-ranking females. Alpha males were always the most social, and the most brightly colored males, but were not necessarily the largest males present. Finally, alpha male tenure was related to group demography, with larger numbers of rival adult males and maturing adolescent males reducing the time a male spent as alpha male. Tenure did not appear to be related to characteristics of the alpha male himself.

Male tenure and reproductive success in single-male vs. multi-male groups of free-ranging howling monkeys in Costa Rica

No abstract

Genetic diversity and reproductive success in mandrills (Mandrillus sphinx).

Recent studies of wild animal populations have shown that estimators of neutral genetic diversity, such as mean heterozygosity, are often correlated with various fitness traits, such as survival, disease susceptibility, or reproductive success. We used two estimators of genetic diversity to explore the relationship between heterozygosity and reproductive success in male and female mandrills (Mandrillus sphinx) living in a semifree ranging setting in Gabon. Because social rank is known to influence reproductive success in both sexes, we also examined the correlation between genetic diversity and social rank in females, and acquisition of alpha status in males, as well as length of alpha male tenure. We found that heterozygous individuals showed greater reproductive success, with both females and males producing more offspring. However, heterozygosity influenced reproductive success only in dominant males, not in subordinates. Neither the acquisition of alpha status in males, nor social rank in females, was significantly correlated with heterozygosity, although more heterozygous alpha males showed longer tenure than homozygous ones. We also tested whether the benefits of greater genetic diversity were due mainly to a genome-wide effect of inbreeding depression or to heterosis at one or a few loci. Multilocus effects best explained the correlation between heterozygosity and reproductive success and tenure, indicating the occurrence of inbreeding depression in this mandrill colony.

Sexual conflicts in spotted hyenas: male and female mating tactics and their reproductive outcome with respect to age, social status and tenure.

We investigated the reproductive outcomes of male and female mating tactics in the spotted hyena, Crocuta crocuta, a female-dominated social carnivore with high maternal investment, an absence of paternal care and female control over copulation. Paternity was determined using microsatellite profiling of 236 offspring in 171 litters from three clans. We found little evidence that male tactics that sought to coerce or monopolize females were successful. Polyandry and sperm competition appeared to counter effectively pre-copulatory male tactics, such as harassment, monopolization and other tactics, such as infanticide, that were against the evolutionary interests of females, and may have contributed to the stability of the male dominance hierarchy, which operated as a social queue. At least 39% of 54 females mated multiply, and 35% of 75 twin litters were fathered by two sires. Polyandry may also serve to ensure fertilization, compensate for an initial poor-quality mate or ensure fertilization by genetically compatible mates. Female mate choice matched observed patterns of affiliative male-female behaviour, indicating that affiliative behaviour is a successful male mating tactic, and was consistent with the idea that male tenure may serve as an index of male quality, although male fertility may decline with extreme old age.

Changes of dominance rank, age, and tenure of wild Japanese macaque males in the Kinkazan a troop during seven years.

Male age-rank and tenure-rank relationships were studied for seven years in unprovisioned Japanese macaque (Macaca fuscata fuscata) troop on Kinkazan Island, Japan. Males whose estimated ages were between 15 and 19 yr old monopolized the highest ranks, while older males whose estimated ages were > or = 20 yr old tended to decline in rank, resulting in a humped age-rank curve. The ranks of males tended to rise as their tenure in the troop increased. The departure of higher-ranking males was the social mechanism for changes in rank, suggesting that the disappearance of higher-ranking males plays an important role in determining rank dominance.

Mate selection in Litoria chloris and Litoria xanthomera: Females prefer smaller males

AbstractIt is generally accepted that high quality males are those that succeed in male–male competition: in either aggression or rivalry to attract and be selected by females. Previous studies of amphibians have suggested that the main characters influencing male mating success include variation in call characteristics (e.g. call rate, call intensity), calling behaviour, body condition, age and chorus tenure. In the present paper, several of the characters influencing female mate choice (male body size, body condition, call rate, call frequency and chorus tenure) are investigated in two closely related, explosive breeding frog species Litoria chloris and Litoria xanthomera. Smaller males of both species are shown to be more successful than larger males and this success is attributed to the increased chorus tenure of smaller males in L. xanthomera. This increased chorus tenure was attributed to the lower total energy used per call by a small male calling at a higher frequency. Whether increased chorus tenure explains female mate choice in L. chloris is uncertain but is highly probable given the strong similarity between the two species in both ecology and call characteristics.