Male chimpanzees exchange political support for mating opportunities

Male chimpanzees, Pan troglodytes, differ from males in most other mammalian taxa because they remain in their natal communities throughout their lives, form close bonds with one another, and cooperate in a range of activities [1]. However, males also compete fiercely for status within their groups [2,3], and high rank enhances male reproductive success [4,5]. Males rely partly on coalitions to achieve and maintain status [2,3,6-9], and shifts in male alliances can have dramatic political effects [2,3,6]. It is not known what benefits are obtained by low-ranking coalition partners. Here we report that the highest-ranking (alpha) male in one well-studied community of chimpanzees rewarded his allies by allowing them preferential access to mates.     

Hormonal correlates of social status and courtship display in the cooperatively lekking lance-tailed manakin

Though cooperative behavior has long been a focus of evolutionary biology, the proximate hormonal mechanisms underlying cooperative interactions remain poorly understood. Lance-tailed manakins (Chiroxiphia lanceolata) are tropical passerines that form long-term male-male partnerships and cooperate in paired male courtship displays. To elucidate patterns of natural hormonal variation in relation to cooperation and reproductive behavior, we examined circulating androgen levels of male lance-tailed manakins in relation to social status, display behavior, and time of year. We found significantly higher circulating androgen levels in alpha-ranked (breeding) males compared to non-alpha adult males in the population. Beta males, which participated in courtship displays but did not copulate, had androgen levels indistinguishable from those of unpaired adult males that never displayed for females, suggesting that an elevated concentration of plasma testosterone in tropical lekking birds may be associated primarily with copulatory behavior or other status-specific traits, and not the performance of courtship display. Androgens decreased throughout the breeding season for males of all status categories. Interestingly, alphas that displayed for females in the observation session prior to sampling had lower androgen levels than alphas that did not display for females. This pattern may result from female discrimination against alpha males at display areas with high levels of social conflict among males, as social disruption is linked to elevated testosterone in many species. However, recent change of a display partner was not related to alpha androgen levels. We discuss alternative explanations and the possible implications of these results, and generate several testable predictions for future investigations.     

Divorce in the barn owl: securing a compatible or better mate entails the cost of re‐pairing with a less ornamented female mate

Two nonmutually exclusive hypotheses can explain why divorce is an adaptive strategy to improve reproductive success. Under the ‘better option hypothesis’, only one of the two partners initiates divorce to secure a higher‐quality partner and increases reproductive success after divorce. Under the ‘incompatibility hypothesis’, partners are incompatible and hence they may both increase reproductive success after divorce. In a long‐term study of the barn owl (Tyto alba), we address the question of whether one or the two partners derive fitness benefits by divorcing. Our results support the hypothesis that divorce is adaptive: after a poor reproductive season, at least one of the two divorcees increase breeding success up to the level of faithful pairs. By breeding more often together, faithful pairs improve coordination and thereby gain in their efficiency to produce successful fledglings. Males would divorce to obtain a compatible mate rather than a mate of higher quality: a heritable melanin‐based signal of female quality did not predict divorce (indicating that female absolute quality may not be the cause of divorce), but the new mate of divorced males was less melanic than their previous mate. This suggests that, at least for males, a cost of divorce may be to secure a lower‐quality but compatible mate. The better option hypothesis could not be formally rejected, as only one of the two divorcing partners commonly succeeded in obtaining a higher reproductive success after divorce. In conclusion, incompatible partners divorce to restore reproductive success, and by breeding more often together, faithful partners improve coordination.     

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

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

Social organization,home ranges,and extraterritorial forays of black-backed jackals

We radio-tracked 15 black-backed jackals (Canis mesomelas) from 8 adjacent family groups on Benfontein Game Farm (i.e., Benfontein) in South Africa to investigate their movement patterns and social organization. Jackal family groups consisted of mated pairs (alphas), 0–3 nonbreeding adults (betas), and pups, depending on the season. Mean (±SE) home-range size of alphas (9.4 ± 1.2 km², n = 6) did not differ (P = 0.766) from betas (9.8 ± 0.7 km², n = 8). Most beta jackals (8 of 10) remained philopatric on Benfontein, apparently because of the high density of springbok (Antidorcas marsupialis), their preferred prey. Three of 5 alphas and all 8 betas went on extraterritorial forays (i.e., forays). Generally, betas spent more of their active time on forays (2–20% of time) than alphas (0–3%; P = 0.048), and betas went farther on forays (2–8 km) than alphas (2–3 km; P = 0.003). The number of forays differed (P < 0.001) among seasons; most forays occurred during summer (64%) when jackals visited neighboring livestock farms, apparently to predate on domestic sheep. Overall, our results indicate forays by jackals are affected by social status, seasonal availability of preferred prey, and the reproductive cycle of jackals. To reduce jackal predation on livestock farms near reserves, we recommend that preventative measures (e.g., use of herders, jackal control activities) be increased during summer when jackals are most likely to travel outside reserves. © 2019 The Wildlife Society.     

Costs and benefits of variable breeding plumage in the red-backed fairy-wren

The red-backed fairy-wren is a socially monogamous passerine bird which exhibits two distinct types of breeding male, bright males that breed in bright red and black plumage and dull males that breed in dull brown plumage. Most males spend their first potential breeding season in dull plumage and subsequent breeding seasons in bright plumage, but a relatively small proportion of males develop bright plumage in their first breeding season. This study quantifies morphology, behavior, and reproductive success of dull and bright males to assess the adaptive costs and benefits of bright plumage while controlling for age. Older bright males (two years of age or older) attempted to increase their reproductive success via copulations with extrapair females, whereas younger (one-year old) bright males and dull males did not. Thus, older bright males spent less time on their own territories, intruded on neighboring groups with fertile females more frequently, gave more courtship displays, and had larger sperm storage organs than did younger bright males and dull males. Microsatellite analyses of paternity indicate that the red-backed fairy-wren has extremely high levels of sexual promiscuity, and that older bright males had higher within-brood paternity than dull males or younger bright males. Regardless of age, bright males were more attractive to females in controlled mate choice trials than were dull males, and both age classes of bright males obtained higher quality mates earlier in the breeding season than did dull males, when nesting success was higher. In conclusion, although it appears that bright plumage increases access to higher quality mates, age also plays a central role in determining a male's overall reproductive success because of the high levels of sexual promiscuity exhibited by the red-backed fairy-wren.     

‘O father: where art thou?’— Paternity assessment in an open fission–fusion society of wild bottlenose dolphins (Tursiops sp.) in Shark Bay,Western Australia

Sexually mature male bottlenose dolphins in Shark Bay cooperate by pursuing distinct alliance strategies to monopolize females in reproductive condition. We present the results of a comprehensive study in a wild cetacean population to test whether male alliance membership is a prerequisite for reproductive success. We compared two methods for inferring paternity: both calculate a likelihood ratio, called the paternity index, between two opposing hypotheses, but they differ in the way that significance is applied to the data. The first method, a Bayesian approach commonly used in human paternity testing, appeared to be overly conservative for our data set, but would be less susceptible to assumptions if a larger number of microsatellite loci had been used. Using the second approach, the computer program cervus 2.0, we successfully assigned 11 paternities to nine males, and 17 paternities to 14 out of 139 sexually mature males at 95% and 80% confidence levels, respectively. It appears that being a member of a bottlenose dolphin alliance is not a prerequisite for paternity: two paternities were obtained by juvenile males (one at the 95%, the other at the 80% confidence level), suggesting that young males without alliance partners pursue different mating tactics to adults. Likelihood analyses showed that these two juvenile males were significantly more likely to be the true father of the offspring than to be their half-sibling (P < 0.05). Using paternity data at an 80% confidence level, we could show that reproductive success was significantly skewed within at least some stable first-order alliances (P < 0.01). Interestingly, there is powerful evidence that one mating was incestuous, with one calf apparently fathered by its mother's father (P < 0.01). Our study suggests that the reproductive success of both allied males, and of nonallied juveniles, needs to be incorporated into an adaptive framework that seeks to explain alliance formation in male bottlenose dolphins.     

Partner switching can favour cooperation in a biological market

Intraspecific cooperation and interspecific mutualisms can be promoted by mechanisms that reduce the frequency with which cooperative organisms are exploited by unhelpful partners. One such mechanism consists of changing partners after interacting with an uncooperative individual. I used McNamara et al.'s (Nature, 451, 2008, 189) partner switching model as a framework to examine whether this mechanism can select for increased cooperative investment by house sparrows (Passer domesticus) collaborating to rear offspring; previous research on this species has shown that substantial cooperative investments by both pair members are required to achieve high pay‐offs from collaborating. I found that the poorer the outcome of a breeding attempt relative to the number of eggs the female invested, the greater the likelihood of partner switching. The incidence of partner switching changed seasonally, with peak switching coinciding with an increase in the number of alternative partners available to females. After females switched partners, their breeding outcomes rose to match those of females that remained with the same partner; this was not the case for males that switched partners. Consistent with the model's prediction, males in stable partnerships achieved over 25% higher than average reproductive success, which was attributable to both persistently good breeding outcomes and their older partners' high fecundity. These results provide empirical support for the hypothesis that partner switching favours increased cooperative investment levels, and they demonstrate that variation in the relative value of by‐product benefits can enhance that process.     

Large Numbers of Matings Give Female Field Crickets a Direct Benefit but not a Genetic Benefit

Female crickets can potentially gain both direct and indirect benefits from mating multiple times with different males. Most studies have only examined the effects of small numbers of matings, although female crickets are capable of mating many times. The goal of this paper is to examine the direct and indirect benefits of mating large numbers of times for female reproductive success. In a previous experiment, female Gryllus vocalis were found to gain diminishing direct benefits from mating large numbers of times. In this study I attempt to determine whether mating large numbers of times yields similar diminishing returns on female indirect benefits. Virgin female Gryllus vocalis crickets were assigned to mate five, ten or 15 times with either the same or different males. Females that mated more times gained direct benefits in terms of laying more eggs and more fertilized eggs. Females that mated with different males rather than mating repeatedly with the same male did not have higher offspring hatching success, a result that is contrary to other published results comparing female reproductive success with repeated versus different partners. These results suggest that females that mate large numbers of times fail to gain additional genetic benefits from doing so.     

Testing three models on the adaptive significance of protandric simultaneous hermaphroditism in a marine shrimp

Protandric simultaneous hermaphroditism, as reported for shrimps in the genus Lysmata, is a sexual system in which individuals invariably reproduce as males first and later in life as simultaneous hermaphrodites. I tested three models (i.e., sex-dependent energetic costs, sex-dependent mortality rates and sex-dependent time commitments) in an attempt to explain the adaptive value of protandric simultaneous hermaphroditism in the shrimp L. wurdemanni. Specific assumptions and predictions of each model were evaluated using manipulative experiments. In the laboratory, males grew faster than simultaneous hermaphrodites of the same size and age, an indication that the female function incurs higher energetic costs of reproduction than the male function. Also, large SHPs were more successful in monopolizing food than small males. The sex-dependent growth rate and size-dependent resource holding power agree with predictions of the sex-dependent energetic cost model. The time that simultaneous hermaphrodites required for replenishing their sperm reservoirs after mating as males was much shorter (2 days) than the time required to brood one clutch of embryos (11 days). Also, small simultaneous hermaphrodites experienced heavier mortality due to predatory fishes than large ones. The sex-dependent reproductive time commitment and size-dependent mortality agree with predictions of the sex-dependent time commitment model. Conversely, I found no evidence that the sex-dependent mortality model explains protandric simultaneous hermaphroditism in the studied species. In contrast to model predictions, mortality due to predatory fishes suffered by simultaneous hermaphrodites was not greater than that suffered by males of the same body size. In L. wurdemanni, the relationship between sex-specific investment and reproductive success seems to change during ontogeny in a way that is consistent with an adaptive adjustment of sex allocation to improve age-specific reproductive success.     

Sex-biased dispersal of adults mediates the evolution of altruism among juveniles

Population viscosity has been proposed as an important mechanism for the evolution of cooperation. The idea is that if individuals do not disperse far during the course of their lives, they will tend to interact with their genealogical relatives, which may give kin-selected benefits for cooperation. However, in the simplest model of population structure, the evolution of cooperation is unaffected by the rate of dispersal, owing to dispersal also mediating competition between social partners. This surprising result has generated much research interest in recent years. Here I show that dispersal does matter if there is a sex difference in dispersal rate, even when the expression of cooperation is not conditional upon the actor's dispersal status or sex. In particular, I show that cooperation among juveniles is relatively favoured when there is a small sex bias in adult dispersal in favour of the sex with the greatest variance in reproductive success, and is relatively disfavoured when this sex bias is large or in the opposite direction. This is because dispersal by individuals of each sex can have different consequences for the genetic structure of the population.     

Spatial structure and interspecific cooperation: theory and an empirical test using the mycorrhizal mutualism

Explaining mutualistic cooperation between species remains a major challenge for evolutionary biology. Why cooperate if defection potentially reaps greater benefits? It is commonly assumed that spatial structure (limited dispersal) aligns the interests of mutualistic partners. But does spatial structure consistently promote cooperation? Here, we formally model the role of spatial structure in maintaining mutualism. We show theoretically that spatial structure can actually disfavor cooperation by limiting the suite of potential partners. The effect of spatial structuring depends on the scale (fine or coarse level) at which hosts reward their partners. We then test our predictions by using molecular methods to track the abundance of competing, closely related, cooperative, and less cooperative arbuscular mycorrhizal (AM) fungal symbionts on host roots over multiple generations. We find that when spatial structure is reduced by mixing soil, the relative success of the more cooperative AM fungal species increases. This challenges previous suggestions that high spatial structuring is critical for stabilizing cooperation in the mycorrhizal mutualism. More generally, our results show, both theoretically and empirically, that contrary to expectations, spatial structuring can select against cooperation.     

Recognition of Individual Males' Songs by Female Dunnocks: a Mechanism Increasing the Number of Copulatory Partners and Reproductive Success

Previous studies have shown that a female dunnock Prunella modularis increases her reproductive success on average by copulating with more than one male resident on her territory and thereby obtaining extra help in raising offspring. Here we document behavior by females that affects which males copulate with them. During her period of receptivity to copulation, a female in a territory shared by two males often left the dominant (or alpha) male, which guarded her most of the time, and approached the subordinate (or beta) male when he sang. A female's responses to individual males thus tend to increase her own reproductive success by increasing her chances for copulation with both males sharing her territory. Playbacks of tape-recorded songs in the field showed that females approached only songs of resident males, not neighbors. They can therefore discriminate individual males by their songs alone, a capability not previously established for female songbirds. Despite intensive guarding of females by males, mating success among male dunnocks depends in part on female choice.     

New colony formation in the "highly inbred" eusocial naked mole-rat: outbreeding is preferred

If the adaptive significance of sexual reproduction derivesfrom genetic recombination, then sexual organisms that severelyinbreed minimize the benefits of sexuality without fully escapingits costs. Local populations of the eusocial naked mole-ratare extremely genetically uniform, and colonies have the highestinbreeding coefficient known for wild mammals. Because non-breedingworkers cooperate to rear the queen's offspring, researchershave speculated that the inclusive fitness benefits of closerelatedness outweigh the benefits of genetic recombination,thus leading to the adaptive avoidance of outbreeding. However,I show that in laboratory colonies in which each individualhad an equal number of familiar siblings and unfamiliar distantkin (UDK) as potential mates, mating pairs were significantlymore likely to consist of UDK. Some form of kin recognitionmust have been used in order for this pattern to result. Aggressionwas not mitigated by relatedness, however, as both fightingand cooperation occurred as frequently between siblings as betweenUDK. By studying the early stages of colony development I wasable to investigate correlations between physical characteristicsof workers and success in attaining breeding status. I alsoobserved allonursing, hitherto unseen in this species, and suggestthat it is less likely to occur later in colony development.     

Determinants of Paternity Success in a Group of Captive Vervet Monkeys (<Emphasis Type="BoldItalic">Chlorocebus aethiops sabaeus</Emphasis>)

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.     

Male sexual ornament size is positively associated with reproductive morphology and enhanced fertility in the stalk-eyed fly <Emphasis Type="Italic">Teleopsis dalmanni</Emphasis>

Background  

Exaggerated male ornaments and displays often evolve in species where males only provide females with ejaculates during reproduction. Although "good genes" arguments are typically invoked to explain this phenomenon, a simpler alternative is possible if variation in male reproductive quality (e.g. sperm number, ejaculate content, mating rate) is an important determinant of female reproductive success. The "phenotype-linked fertility hypothesis" states that female preference for male ornaments or displays has been selected to ensure higher levels of fertility and has driven the evolution of exaggerated male traits. Females of the stalk-eyed fly Teleopsis dalmanni must mate frequently to maintain high levels of fertility and prefer to mate with males exhibiting large eyespan, a condition-dependent sexual ornament. If eyespan indicates male reproductive quality, females could directly increase their reproductive success by mating with males with large eyespan. Here we investigate whether male eyespan indicates accessory gland and testis length, and then ask whether mating with large eyespan males affects female fertility.     

How conception risk affects competition and cooperation with attractive women and men

We investigated competition and cooperation for resources across the menstrual cycle in the context of bargaining games. Although bargaining has been studied within an evolutionary framework, little attention has been paid specifically to the role of mating motives in economic behavior. To investigate how motives related to reproductive success affect bargaining, participants at high or low risk for conception or who were on oral contraceptives played ultimatum and dictator games with partners who varied in sex and facial attractiveness. In ultimatum games, women in the fertile phase were more competitive over resources with attractive women than with less attractive women. Intrasexual competition was not observed in dictator games. Women were more cooperative with attractive men than with less attractive men in both games, regardless of fertility status. Low fertility women were more cooperative with attractive members than with less attractive members of both sexes in both games. Results support the view that, during periods of high fertility, when women are most intrasexually competitive for mates, withholding resources from potential rivals would enable women to gain the means to enhance their attractiveness and weaken competitors' abilities to do the same at a time when relative advantages in appearance are most crucial to reproductive success. The lack of a fertility effect for cooperation with potential mates supports the view that displays of generosity accrue benefits for women across the cycle in their efforts to attract men who will invest in relationships.     

Fitness effects of parasite-mediated spatial heterogeneity within a swarm

The fitness consequences associated with the position an individualadopts within a dynamic group are not well understood. I investigatedmate acquisition by male chironomid midges using a simple swarmingmodel and empirically collected data on midge aerobatic ability.Previous work has suggested that the aerobatic ability of amale is an important predictor of his reproductive success,although there is contrary (and counterintuitive) evidence thatinfection with ectoparasitic mites increases a male's chanceof mating, despite having negative effects on flight speed.The model used here suggests that a male's location within theswarm, brought about passively through interindividual differencesin flight speed, may explain these contradictory results. Specifically,slower flying males (including those burdened with mites) adoptedpositions nearer the center of the swarm, whereas faster malestended to occupy the periphery. This in turn affected theiraccess to females because any mechanism that brought femalesnearer the swarm's center before capture (including high femaleflight speed and selective pairing by either males or females)significantly increased the relative reproductive success ofboth larger and parasitized males, with the benefits of parasitismpeaking at around 4 mites per host. There may be selective pressureon hosts and parasites to maintain this optimal mite densitybecause both are likely to benefit from the relationship: hostsenjoy an increased reproductive success, whereas only throughhost copulation can mites transfer to a female midge and returnto water (their next life-history stage) during host oviposition.     

Coalition Formation by Male Vervet Monkeys (Chlorocebus pygerythrus) in South Africa

Unrelated male primates frequently cohabit in bisexual groups and, despite being reproductive competitors, have been shown to cooperate in ways that are associated with reproductive success. Such coalitions between males are common in some taxa, where they can serve two primary functions – status management and improved mating opportunities – that subserve long‐ and short‐term objectives. Here, we use observational data to provide information on male coalitions in vervet monkeys (Chlorocebus pygerythrus), a guenon with a multimale group structure. We recorded a total of 62 coalitions from two troops across a 10‐mo period at Samara Game Reserve, South Africa. We found that males who were more frequently associated spatially and who had groomed one another were more likely to form coalitions and did so against higher‐ranking opponents. This was not linked to any evidence that coalitionary aggression provided either short‐ or long‐term reproductive benefits for the aggressors and coalitions were not restricted to the mating season. There was little evidence that particular individuals were targeted, reciprocation between partners was not observed, and recent immigrant males were not targeted disproportionately. Our data suggest that within‐group coalition formation between vervet males may represent something close to an ancestral state whereby males form ad hoc coalitions opportunistically, joining an ongoing dyadic contest to target an opponent without facing the possible risks of dyadic contest, such as a greater chance of injury.     

Paternity analysis of alternative male reproductive routes among the langurs (Semnopithecus entellus) of Ramnagar

Because primate males usually invest very little in offspring, male reproductive success will mainly be determined by access to fertile females with differences in access leading to differential male reproductive success. To determine the outcome of alternative male reproductive routes, we investigated a wild population of Hanuman langurs at Ramnagar, South Nepal, where groups were either one-male or multimale. Paternity was established by DNA analysis from faeces for 42 infants in five groups. In one-male groups all infants were sired by the only resident male in the group. In multimale groups the alpha male fathered significantly more infants (57%) than all other resident males. Nonresident males sired at least 21% of all infants born into multimale groups. Because of the lower mean number of infants sired by alpha males during their whole tenure as alpha compared with males in one-male groups (2.3 versus 6.8) and the higher maximum value (8.9 versus 6.0), the alpha male route is considered the riskier option. Based on demographic data we suggest that the considerable variance in short-term reproductive success might not translate to the same degree into differences in long-term reproductive success. Copyright 2001 The Association for the Study of Animal Behaviour.