Non-resident Males Research Articles

Paternity success for resident and non-resident males and their influences on paternal sibling cohorts in Japanese macaques (Macaca fuscata) on Shodoshima Island

Reproductive success can be attributed to both resident and non-resident males in non-human primates. However, reproductive success of non-resident males has rarely been investigated at an individual level. As resident males achieve different degree of reproductive success with regard to various factors, such as male dominance relationships or female mate choice, the degree of reproductive success for non-resident males may vary between individuals. As male reproductive success is highly skewed towards specific individuals, the percentage of similar-aged paternal siblings within groups is expected to increase. However, the extent to which each male contributes to the production of cohorts of paternal siblings remains unclear. Here we examined the paternity of offspring born over five consecutive years in a free-ranging group of Japanese macaques Macaca fuscata on Shodoshima Island, Kagawa Prefecture. Genotypes of 87 individuals at 16 autosomal microsatellite loci were analyzed and paternity of 34 offspring was successfully assigned to a single candidate father. We quantitatively assessed paternity success for resident and a few non-resident males whose genetic samples were successfully collected. We quantitatively assessed the percentages of paternal siblings in the same age cohorts produced by those males. Non-resident males sired similar percentage of offspring compared to resident males. A large prime-aged non-resident male was the most successful sire among males in two of the five years. These results provide new insights that male reproductive success could be highly skewed toward a specific non-resident male. Subadult males had a lower percentage of paternity success, which may be because females may prefer physically mature males. Various males, including non-resident males, contributed to the creation of paternal sibling in the same age cohort. The overall results highlighted that not only resident but also non-resident males play an important role in shaping within-group kin structures.

Female Mate Choice in Wild Kenyan Blue Monkeys (Cercopithecus mitis).

Female mate choice may drive sexual selection, but discerning whether female behaviors reflect free expression of choice or responses to constraints can be difficult. We investigated the efficacy of female choice in wild blue monkeys using 10 years of behavior and paternity data (N = 178 male-female dyads). Although blue monkeys live modally in one-male polygynous groups, where male-biased intersexual power is expected, females can access multiple potential mates during seasonal male influxes and occasional intergroup encounters. Additionally, extra-group males sire offspring. We examined female resistance rates to male-initiated sexual interactions, and unsolicited proceptive behavior that females directed to males (corrected for male availability). Females seldom resisted male solicitation, but initiated sexual interactions more than males. Females generally preferred residents. Those who preferred non-residents tended to have residents with longer tenures, but neither female parity nor rank influenced the tendency to prefer non-residents vs. residents. The male most solicited by a particular female fathered that female's infant 82% of the time; odds of siring were 26 times higher for most vs. nonpreferred males. Female preference predicted paternity even more strongly among non-resident males, with odds of siring 33 times higher for most vs. nonpreferred non-residents. Neither female rank nor parity influenced her likelihood of having her preferred partner as sire. Paternity by preferred males did not affect infant survival. While we cannot fully discount the effect of male-male competition on paternity, these results suggest that blue monkey females can exercise choice successfully, even in a polygynous mating system.

Can females differentially allocate resources to offspring sired by different males?

Abstract The viviparity-driven conflict hypothesis postulates that the evolution of matrotrophy (postfertilization maternal provisioning) will result in a shift from a pre- to postcopulatory mate choice and thus accelerate the evolution of postcopulatory reproductive isolation. Here, we perform artificial insemination experiments on Heterandria formosa, a matrotrophic poeciliid fish, to probe for evidence of postcopulatory female choice. We established laboratory populations from Wacissa River (WR) and Lake Jackson (LJ). The WR females normally produce larger offspring than the LJ females. We artificially inseminated females with sperm from each population or from both populations simultaneously. When LJ females were inseminated with sperm from WR and LJ males, they allocated fewer resources to WR-sired offspring than when they were inseminated with WR sperm alone. The LJ females carrying developing offspring sired by males from different populations were thus able to discriminate against non-resident males when allocating resources to developing young. The WR females, which normally produce larger offspring than LJ females, did not discriminate among males from different localities. These findings provide insights into the ability of females from one population to exercise a form of postcopulatory mate selection.

Sneaky copulations by subordinate males suggest direct fitness benefits from male-male associations in spotted bowerbirds (Ptilonorhynchus maculatus).

Male spotted bowerbirds (Ptilonorhynchus maculatus) build and defend a structure of sticks and straw-the bower-decorated with colourful objects to attract mates during the breeding season. Specific non-territorial, subordinate males are tolerated by resident males at bowers over multiple breeding seasons. Prior research showed that these male-male associations exhibit attributes of coalitionary behaviour and that subordinate males gain delayed benefits from associating with bower owners, namely future bower inheritance. Yet, it remained unclear whether subordinate males may additionally gain direct fitness benefits from attending established bowers. Here, we report on four separate instances of sneaky copulations (or attempts of copulating) by subordinate males at resident males' bowers. Multiple non-resident males disrupted the ongoing copulations between the bower owner and a receptive female, and these events were followed by violent aggressive interactions. These observations shed new light on same-sex social dynamics in spotted bowerbirds and support the hypothesis that subordinate males are sexually mature individuals that occasionally obtain access to females while attending established bowers. We discuss these findings in light of the literature on male courtship coalitions and agonistic behaviour in bowerbirds, and highlight further aspects of subordinate behaviour that require empirical investigation.

In Space and Time: Territorial Animals are Attracted to Conspecific Chemical Cues.

Territorial animals lay scent marks around their territories to broadcast their presence, but these olfactory signals can both attract and repel con-specifics. Attraction or aversion can have a profound impact in terms of space use and thereby influence an individual's access to resources and mates. Here, we test the impact of chemical signals on the long-term space use and activity of receivers, comparing the response of males and females, territory holders, and temporary visitors in Sceloporus undulatus lizards in the field. We placed either male femoral gland secretions (chemical) or blank (control) cues on resident male landmarks, repeatedly over 5 d, while monitoring the activity and location of all lizards in the vicinity. We found that resident males and females, but not non-resident males, were active on more days near landmarks treated with chemical cues than landmarks treated with control cues. Non-resident males remained closer to chemical than control cues. These results suggest that territorial scent marks are attractive to conspecifics and impact space use, but that the specific effects depend on receiver sex and residency status. Such subtle or gradual changes in behavior may frequently be overlooked by short-term choice experiments. Future studies investigating the behavioral significance of a communicative signal should consider these finer details of behavior for a more comprehensive assessment.

Nesting phenology, mate choice, and genetic divergence within a partially migratory population of American Kestrels

ABSTRACT Studies across annual cycles are important for understanding the consequences of carryover effects and predicting species' responses to environmental change. Partially migratory populations, which consist of resident and migratory individuals, are excellent systems for studying how wintering strategies may affect reproduction. We examined whether wintering strategy (residency or nonresidency) created temporal divides in egg-laying date within a local breeding population of American Kestrels (Falco sparverius) and thus led to assortative mating and genetic divergence between early- and late-breeding birds. For 3 yr, we trapped and marked kestrels in winter and recaptured mated pairs in nest boxes in the subsequent spring. We then genotyped early- and late-breeding kestrels using 6 polymorphic microsatellite loci. Residents nested earlier than nonresidents, but not after the warmest and driest winter of the study. Resident females were more likely to mate with resident males than nonresident males,...

Spatial aspects of movements, mating patterns, and nest distributions influence gene flow among population subunits of Blanding’s turtles (Emydoidea blandingii)

The core habitats of semi-aquatic organisms are centered on wetlands, but also include terrestrial habitats. Patterns of movements among core area components can influence rates of genetic and demographic exchange among populations. A combination of 33 years of data on the life history and spatial biology of Blanding’s turtles (Emydoidea blandingii) on the E. S. George Reserve (ESGR) and 8 years of genetic data (N = 244 adults and 611 offspring) were used to document resident wetlands, identify mating pairs, and estimate cohort levels of coancestry and degree of spatial genetic structuring. For ESGR resident females, 34 % of clutches were sired by non-resident males, whereas 56 % of clutches of non-resident females that nested on the ESGR were sired by ESGR resident males. The mean number of mates for males and females was 1.6 (SD = 0.67) and 2.02 (SD = 1.05), respectively, and the annual occurrence of multiple paternity averaged 47.6 % (min–max = 15.4–55.6 %, N = 8). Repeat paternity was common (69.6 %), regardless of residence of parents. The probability of adults mating with individuals from different residence wetlands and tendencies for hatchlings to disperse to wetlands other than their mother’s residence contributed to demographic and genetic connectivity among residence wetlands. Similar allele frequencies among individuals from different residence wetlands (Fst = 0.002, P > 0.05) were consistent with the frequency and geographic extent of adult and juvenile movements. Data on mating patterns, individual movements, and core-habitat use helped identify mechanisms that influence genetic structuring within a population comprised of multiple sub-units.

Attacks on adult females with infants by non-resident males in the François langur

Infanticide by males is a common phenomenon in mammals, especially primates, as lactation lasts much longer than gestation in many species. Usually, infanticidal episodes occur soon after group takeovers, and are traditionally considered a male reproductive strategy (i.e., support the sexual selection hypothesis, Hrdy, 1974). To verify the validity of this conception, we observed one group of Francois' langurs in the Nonggang Nature Reserve, China, between August 2003 and July 2004. During the study period, a Francois' langur female with the youngest infant in the group was attacked three times by immigrating males, and later disappeared by the third day after the final attack. We suggest that these attacks on the female-infant dyad represent infanticide attempts by males, and may be the cause of the adult female and her infant's disappearance. Presumably, that female dispersed with her infant to avoid infanticide and was not killed. Though these observations do not completely verify the sexual selection hypothesis, they are not inconsistent with it.

Stress factors in local water-vole population

The physiologic mechanisms of stress have multiple effects on the adaptive capacity of an individual. Thus, the analysis of factors that determine the level of stress in animals in a changing environment acquires considerable ecologic and evolutionary significance. The results of long-term studies performed at the site of an irrigation canal, which is annually populated by water voles, are described in this paper. A high level of stress in male water voles has been found when the resources (food and mates) are scarce. The activation of adrenocortical function under the conditions of insufficient resources occurs due to the intensification of the intraspecific competition, which takes place after a decrease in both the food supply and the ratio of females in the local population. The effects of these factors are mediated by changes in spatial and ethologic structure of a studied population appearing as an increasing overlap of individual areas. The food supply and insufficient number of females affect the levels of glucocorticoids differently in resident and nonresident males. Our results suggest that social interactions act as actual stress factors in water voles, even if a considerable decrease occurs in water vole populations, which takes place in North Baraba due to the reduction of watering in the area and the decrease in territories suitable for summer habitation.

Mating promiscuity and reproductive tactics in female black and gold howler monkeys (Alouatta caraya) inhabiting an island on the Parana river, Argentina

In several primate species, females mate promiscuously and several adult males peacefully co-reside in the same social group. We investigated female mating behavior in two neighboring multimale-multifemale groups of Alouatta caraya in northern Argentina (27 degrees 20'S-58 degrees 40'W). All adult individuals in each group were marked with identification anklets and ear tags, and followed for five consecutive full days per month during 20 consecutive months. We recorded 219 copulations for eight resident females in these two groups. Thirty-two percent of matings involved extra-group copulations and 68% were with resident males. During periods when females were likely to conceive and during periods when females were nonfertile (pregnancy and lactation), there were no significant differences in the average number of resident and nonresident males with which they copulated (G-test: G(adj)=0.1, df=3, P>0.05). In both of our study groups, adult males were tolerant of the mating activities between resident males and resident females, but acted aggressively and collectively (howling, border vigilance, and fighting) when extragroup males attempted to enter the group and mate with resident females. Given the frequency of extragroup matings, we examined the distance females traveled to engage in these copulations, time engaged in pre- and postcopulatory behavior, and the risk of injury during extragroup copulations. These costs were found to be relatively small. We suggest that female promiscuity is the prime driver or constraint on male reproductive opportunities in this species. Female promiscuity in A. caraya appears to represent a mixed mating strategy that may serve to increase opportunities for genetic diversity between a female's successive offspring as well as minimize the risk of infanticide by spreading paternity estimates across a larger number of adult males.

Dishonest signalling of fighting ability and multiple performance traits in the fiddler crab Uca mjoebergi

Signals used during male combat are expected to be honest indicators of fighting ability. However, recent studies show that dishonesty in male signalling is more prevalent than previously believed. 2. Here we show that regenerated (leptochelous) claws in male Uca mjoebergi fiddler crabs are not only dishonest signals of two types of whole-organism performance capacities that are likely to be useful during fights (claw closing force and pull-resisting force), but they are also less effective as weapons in situations where males are unable to bluff. 3. Original (brachychelous) male claws are statistically significant predictors (independent of body size) of both closing force and the force required to pull a male out of a tunnel. By contrast, leptochelous claw size does not convey information on those performance capacities following control for body size. 4. Furthermore, claw size affects fighting ability such that leptochelous residents are at a significant competitive disadvantage to brachychelous residents, although claw type does not affect the ability of non-resident males to win fights. 5. This study is among the first to show that male armaments can dishonestly signal performance traits that are likely important for winning fights, and is the first to show evidence for dishonest signalling of multiple components of fighting ability.

Determinants of Outcomes of Agonistic Interactions among Male California Sea Lions (Zalophus californianus)

Agonistic behavior in territorial male California sea lions (Zalophus californianus) may be influenced by multiple factors, including who initiates an interaction and who owns the territory on which an encounter takes place. We studied predictors of the outcomes of agonistic interactions between territorial male California sea lions on 3 islands (Los Islotes, Granito, and San Jorge) in the Gulf of California, Mexico, during the 2005 breeding season. We evaluated both displays and fights among males to examine the hypotheses that initiators of agonistic interactions and that territory owners were more likely to win disputes. The outcomes of agonistic encounters (win or lose) were independent of the types of interaction (displays or fights) by the initiator and, hence, all agonistic interactions were pooled for analyses. We used an overdispersed binomial logistic regression to determine if initiators and resident males were more likely to win an interaction than noninitiators and nonresidents, respectively. We found that initiators of agonistic interactions were more likely to win agonistic disputes. Resident and nonresident males were equally likely to initiate agonistic interactions and were also equally likely to win agonistic disputes. Our results suggest that agonistic interactions among male California sea lions are influenced by which individual initiates the encounter and not by territory ownership.

Mating success of resident versus non-resident males in a territorial butterfly

Male–male competition over territorial ownership suggests that winning is associated with considerable benefits. In the speckled wood butterfly, Pararge aegeria, males fight over sunspot territories on the forest floor; winners gain sole residency of a sunspot, whereas losers patrol the forest in search of females. It is currently not known whether residents experience greater mating success than non-residents, or whether mating success is contingent on environmental conditions. Here we performed an experiment in which virgin females of P. aegeria were allowed to choose between a resident and a non-resident male in a large enclosure containing one territorial sunspot. Resident males achieved approximately twice as many matings as non-residents, primarily because matings were most often preceded by a female being discovered when flying through a sunspot. There was no evidence that territorial residents were more attractive per se, with females seen to reject them as often as non-residents. Furthermore, in the cases where females were discovered outside of the sunspot, they were just as likely to mate with non-residents as residents. We hypothesize that the proximate advantage of territory ownership is that light conditions in a large sunspot greatly increase the male's ability to detect and intercept passing receptive females.

Social common mole-rats enhance outbreeding via extra-pair mating

Females in many species engage in matings with males that are not their social mates. These matings are predicted to increase offspring heterozygosity and fitness, and thereby prevent the deleterious effects of inbreeding. We tested this hypothesis in a cooperative breeding mammal, the common mole-rat Cryptomys hottentotus hottentotus. Laboratory-based studies suggested a system of strict social monogamy, while recent molecular studies indicate extensive extra-pair paternity despite colonies being founded by an outbred pair. Our data show that extra-pair and within-colony breeding males differed significantly in relatedness to breeding females, suggesting that females may gain genetic benefits from breeding with non-resident males. Extra-colony male mating success was not based on heterozygosity criteria at microsatellite loci; however, litters sired by extra-colony males exhibited increased heterozygosity. While we do not have the data that refute a relationship between individual levels of inbreeding (Hs) and fitness, we propose that a combination of both male and female factors most likely explain the adaptive significance of extra-pair mating whereby common mole-rats maximize offspring fitness by detecting genetic compatibility with extra-pair mates at other key loci, but it is not known which sex controls these matings.

Post-conception mating in wild long-tailed macaques ( Macaca fascicularis): Characterization, endocrine correlates and functional significance

In many anthropoid primates, mating activity is not restricted to the ovarian cycle but also occurs during pregnancy. Although it has been suggested that the main function of this post-conception mating is to confuse paternity, studies showing whether or not male primates can distinguish between the fertile phase of the conception cycle (FPCC) and the period of peak post-conception mating (peak PCM) are almost non-existent. Here, we examine whether the pattern of female sexual traits (specific sexual behaviors, sexual swelling) and female attractiveness to males differ between FPCC and peak PCM in 6 wild female long-tailed macaques. We also use fecal hormone analysis to investigate whether female traits during peak PCM are related to changes in female sex hormones. All females exhibited a distinct period of heightened mating activity around days 45–60 of gestation. During peak PCM, swelling size and frequency of female solicitations (but not reaching back) were significantly correlated with changes in the estrogen to progestogen ratio. Swelling size, frequency of female sexual behaviors and copulations and proportion of male-initiated copulations and ejaculations were not significantly different between FPCC and peak PCM. Although males spent significantly less time consorting females during peak PCM, all (particularly low-ranking and non-resident males) invested heavily in terms of reproductive costs associated with mate-guarding and mating during pregnancy. We conclude that post-conception mating in wild long-tailed macaques is not merely a by-product of endocrine changes and devoid of adaptive function. Our results more strongly support the hypothesis that it may form part of a female reproductive strategy to confuse paternity, which appears to apply particularly to low-ranking and extra-group males.

Philopatry and reproductive success in Bornean orang‐utans (Pongo pygmaeus)

Behavioural observations suggest that orang-utans are semi-solitary animals with females being philopatric and males roaming more widely in search of receptive partners, leading to the prediction that females are more closely related than males at any given site. In contrast, our study presents evidence for male and female philopatry in the orang-utan. We examined patterns of relatedness and parentage in a wild orang-utan population in Borneo using noninvasively collected DNA samples from animals observed to defecate, and microsatellite markers to assess dispersal and mating strategies. Surprisingly, resident females were equally as related to other resident females (mean r(xy) = 0.303) as resident males were to other resident males (mean r(xy) = 0.305). Moreover, resident females were more related to each other and to the resident males than they were to nonresident females, and resident males were more related to each other (and resident females) than they were to nonresident males. We assigned genetic mothers to 12 individuals in the population, while sires could be identified for eight. Both flanged males and unflanged males achieved paternity, similar to findings reported for Sumatran orang-utans.

Genetic population structure of the white sifaka (Propithecus verreauxi verreauxi) at Beza Mahafaly Special Reserve, southwest Madagascar (1992–2001)

Gene flow within and between social groups is contingent on behaviourally mediated patterns of mating and dispersal. To understand how these patterns affect the genetic structure of primate populations, long-term data are required. In this study, we analyse 10 years of demographic and genetic data from a wild lemur population (Propithecus verreauxi verreauxi) at Beza Mahafaly Special Reserve, southwest Madagascar. Our goal is to specify how patterns of mating and dispersal determine kinship and genetic diversity among animals in the population. Specifically, we use microsatellite, parentage, and census data to obtain estimates of genetic subdivision (FST), within group homozygosity (FIS), and relatedness (r) within and among social groups in the population. We analyse different classes of individuals (i.e. adults, offspring, males, females) separately in order to discern which classes most strongly influence aspects of population structure. Microsatellite data reveal that, across years, offspring are consistently more heterozygous than expected within social groups (FIS mean = -0.068) while adults show both positive and negative deviations from expected genotypic frequencies within groups (FIS mean = 0.003). Offspring cohorts are more genetically subdivided than adults (FST mean = 0.108 vs. 0.052) and adult females are more genetically subdivided than adult males (FST mean = 0.098 vs. 0.046). As the proportion of females in social groups increases, the proportion of offspring sired by resident males decreases. Offspring are characterized by a heterozygote excess as resident males (vs. nonresident males) sire the majority of offspring within groups. We link these genetic data to patterns of female philopatry, male dispersal, exogamy, and offspring sex-ratio. Overall, these data reveal how mating and dispersal tactics influence the genetic population structure in this species.

Twilight fighting in the evening brown butterfly, Melanitis leda (L.) (Nymphalidae): age and residency effects

Butterflies are conspicuous among animals that fight for mating opportunities because it is not clear how contest costs could accrue. Nevertheless, the bulk of research in this group suggests that contests are settled on the basis of asymmetries in fighting ability (the superior competitor hypothesis). There is also a consistent effect on contest escalation due to apparent 'confusion' over residency, which could result from resident butterflies playing different tactics than non-residents, or from a causal link between residency and fighting ability. I addressed these hypotheses by studying contest behavior in the crepuscular species Melanitis leda (L.) (Nymphalidae) over a 5-month period in tropical Australia. Males competed via conspicuous two-stage maneuvers of a form unique among butterflies. Prior residents won 77% of all contests. Non-resident males arrived and perched in occupied sites until challenged by incumbent residents, and the aggressiveness of these interlopers increased as a function of the time before they were detected. Contest winners also tended to be younger than losers, and contest escalation was negatively related to both the age of the losing male and the magnitude of the between-combatant age asymmetry. These results are consistent with the superior competitor hypothesis based upon age as a determinant (or correlate) of fighting ability, but also suggest residency has a unique influence on contest behavior. Further research is clearly required to unravel the effects of age, residency and other potential biophysical determinants of fighting ability in this species.

Observations of the common vampire bat (Desmodus rotundus) and the hairy-legged vampire bat (Diphylla ecaudata) in captivity

Summary We investigated roosting patterns, reproduction, morphometry, and ontogeny of a group of common vampire bats ( Desmodus rotundus ) and a group of the hairy-legged vampire bats ( Diphylla ecaudata ) both maintained for > 3 years in captivity. The basic social structure observed in Desmodus was of a “principal colony” or “harem” composed of females and their offspring and a few adult males, termed “resident males” and a separate group of the other males, termed “non-resident males”. The roosting patterns of Diphylla differed little from those observed in Desmodus , but the hierarchical segregation of non-resident males appeared to be less strict. In both species the non-resident males are accepted into the principal colony when the ambient temperature lowers. This behavior suggests social thermoregulation. Parturition of both species occurred once a year, and most of the births took place in spring or summer. The average duration of palpable pregnancy and lactation was longer in Desmodus than in Diphylla . In both species some lactating females that had lost their young continued suckling the babies of other females. Desmodus is larger in size than Diphylla . This may be related to the size and type of prey; Desmodus preys principally on large mammals and Diphylla preys on birds. We observed female biased sexual dimorphism in Desmodus and isometrical sexes in Diphylla . This may be related to the differential duration of lactation and maternal care periods, as the breeding cycle in Desmodus is longer than in Diphylla . The average time of reaching maturity: epiphysis closure of wing bones, adult weight, scrotal testes, and first pregnancy, as well as the first flight time and the time when males begin to roost apart from the principal colony, were later in Desmodus than in Diphylla . The variation between the two genera for duration of ontogeny and maternal care periods may be related to the learning needs for predation on different types of prey.

The phalloid organ, orgasm and sperm competition in a polygynandrous bird: the red-billed buffalo weaver ( Bubalornis niger )

The buffalo weavers, Bubalornis spp., are unique amongst birds in possessing a phalloid organ, a phallus-like structure anterior to the cloaca. We studied the red-billed buffalo weaver Bubalornis niger, to determine whether the phalloid organ has evolved in response to sperm competition. The phalloid organ was significantly longer in males that were resident at nests than in non-resident males, and among resident males was significantly longer in those males with a harem than in those without. Red-billed buffalo weavers bred colonially and had either a cooperatively polygynandrous (usually two unrelated males and several females) or a polygynous (one male and several females) mating system. Cooperative polygynandry provided females with the opportunity to copulate with more than one male and paternity analyses using DNA fingerprinting revealed that 63% of 16 multiple-offspring broods, comprising 43 offspring, had multiple sires, which included both nest-owning males and extra-group males. Sperm competition was therefore intense. Observations and experiments with buffalo weavers in captivity revealed that the phalloid organ was not intromittent during copulation, but functioned as a stimulatory organ which necessitated protracted copulation in order to induce male 'orgasm' and ejaculation, a feature apparently unique to this species.