Beta Males Research Articles

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.

Age and growth of the gulf toadfishOpsanus betabased on otolith increment analysis

In the present study, sagittal otoliths of confirmed male and female specimens of the gulf toadfish Opsanus beta that were collected monthly over the course of a year from Biscayne Bay, Florida, U.S.A. were analysed. The timing and frequency of O. beta spawning seasons are reported by examination of the gonado-somatic index. The estimated ages of males and females ranged from <1 year to 6 and 5 years, respectively. Strong sexual dimorphism in growth was apparent with von Bertalanffy parameter estimates for males of Linfinity=393.8 mm, K=0.30, t0=0.36 and females of Linfinity=201.1 mm, K=0.79, t0=0.47. Comparison with previously published growth trajectories of the more northerly distributed conspecific Opsanus tau showed that O. beta males had a higher growth rate. Female O. beta and O. tau growth trajectories appear similar, with an indication that the former becomes asymptotic at least a year before the latter. Results are discussed in the context of temperature regimes, reproductive energy allocation and waste urea excretion in the two species.

Seizing the Opportunity: Subordinate Male Fowl Respond Rapidly to Variation in Social Context

AbstractDominance affects mating and reproductive success in many group‐living species. Potential mechanisms include subordinates being inherently less attractive and social constraints imposed by dominant individuals. To test the former possibility, we measured morphology in 45 male fowl, Gallus gallus, prior to group formation. Males were then assigned to social groups (three males and three females in each). None of the measured traits predicted subsequent social status, suggesting that subordinates were not inherently unattractive. We then manipulated social constraints in each group to test if subordinates were socially constrained. We removed either the alpha (experimental) or the gamma male (control) for 40 min and observed the effect on the beta male’s reproductive behavior. Controls accounted for putative group size and disturbance effects, and ensured that the only difference between treatments was the relative dominance of the remaining male. In each trial, we measured the beta male’s courtship effort and his mating success, as well as his proximity to females and to the remaining male. Results show that social context did not affect mating success, but had a significant impact on courtship behavior. Beta males courted significantly more often when they had exclusive access to a female, as opposed to when another male was nearby. Furthermore, their courtship effort was higher if the nearby male was a fellow subordinate, as opposed to the dominant male. We conclude that both the proximity and social status of nearby males affects, either directly or indirectly, the courtship efforts of subordinate male fowl.

Christopher Moore and the Creation of the Beta Male

Christopher Moore and the Creation of the Beta Male

Agonistic Behaviour and Sexual Conflict in Atypical Reproductive Groups: The Case of Bearded VultureGypaetus barbatusPolyandrous Trios

AbstractSocial behaviour in species forced to form atypical breeding coalitions is poorly documented. The saturation of optimum territories in the Bearded vultureGypaetus barbatuspopulation in the Pyrenees has led floating males to settle in already occupied territories, thereby forming polyandrous trios. We examined the patterns of intrasexual aggression in five trios (nine reproductive events in total) during courtship. Alpha males initiated 82% of agonistic encounters that were mainly aimed at preventing or disrupting copulations. During the fertile period in recently formed groups, intrasexual aggression had a negative influence on the frequency of heterosexual copulations, which may be a contributing factor to the lower productivity of polyandrous trios. Females rejected a higher proportion of beta male‐ than alpha male‐initiated copulations, and rejected copulations with both alpha and beta males more often when the other male was present close by. These results indicate that alpha males cannot effectively prevent all copulation attempts by beta males and that females avoid harassment by minimizing sexual activity when both males are present. Aggression between males decreased with time, occurring less often in established than in recent trios, despite the fact that the frequency of heterosexual copulations – the cause of conflicts – was similar. The frequency of homosexual interactions tended to increase in established trios, suggesting that this behaviour may help to regulate aggression within these groups, although no significant relationship between homosexual interactions and aggression was found. In summary, reproductive conflicts in trios seem to be unavoidable, although they tend to decrease if the group is maintained. This suggests that, for birds in these groups, the maintenance of a quality territory is more important than solving sexual conflicts.

Adaptive Advantages of Cooperative Courtship for Subordinate Male Lance‐Tailed Manakins

Male lance-tailed manakins (Chiroxiphia lanceolata) cooperate in complex courtship displays, but the dominant (alpha) partner monopolizes mating opportunities. This raises the question of why subordinates (betas) cooperate. Three nonexclusive hypotheses explain the adaptive basis of helping behavior by subordinate males: cooperation may increase (1) subordinates' immediate reproductive success, (2) the reproductive success of close relatives, or (3) subordinates' chances of future reproduction. I demonstrated that beta males rarely sired chicks and were unrelated to their alpha partners but received delayed direct benefits from cooperation; betas had an increased probability of becoming an alpha when compared to males that had not been betas. To investigate the mechanism by which betas attain these adaptive benefits, I examined betas' success in replacing their alpha partners both in natural turnover events and when alphas were experimentally removed. Beta males did not consistently inherit alpha roles in the same territories where they served their beta tenure, arguing that queuing for status does not fully explain the benefits of cooperation for betas. Instead, betas may be apprenticing to develop effective and appropriate displays that enhance their subsequent success as alphas. Complex social affiliations appear to mediate selective pressure for cooperation in this species.

Repeated maternal glucocorticoid treatment affects activity and hippocampal NMDA receptor expression in juvenile guinea pigs

The behavioural consequences of prenatal glucocorticoid exposure are not well understood, though emerging studies in humans indicate hyperactivity and altered cognitive development can occur. Further, recent reports indicate that N-methyl-d-aspartate receptors (NMDARs) may mediate the development of postnatal stress behaviours. We hypothesized that prenatal betamethasone (Beta) administration would alter behaviour and the expression of hippocampal NMDAR subunits NR1, NR2A and NR2B in juvenile guinea pig offspring. We found that repeated maternal Beta (1 mg kg(-1)) treatment on gestational days (gd) 40/41, 50/51 and 60/61 (term approximately 70 days) had no significant effect on birthweight or early growth. However, Beta produced sex-specific effects on open-field activity and hippocampal NMDAR subunit expression compared with controls. Female Beta offspring exhibited significantly increased locomotor activity while there was no effect in Beta males. Beta males exhibited a tendency for decreased anxiety-like behaviour. With respect to NMDAR subunit expression, Beta-exposed females exhibited significantly reduced NR1 mRNA in CA1/2 and CA3 subfields of the hippocampus; there were no effects in Beta males. In conclusion, repeated maternal treatment with Beta, in a similar regimen to that administered to pregnant women at risk of delivering preterm, has profound consequences on behaviour and development of crucial neurotransmitter systems in postnatal life.

SEXUAL DIMORPHISM, DISPERSAL PATTERNS, AND BREEDING BIOLOGY OF THE TAIWAN YUHINA: A JOINT-NESTING PASSERINE

Abstract We studied the breeding ecology of Taiwan Yuhinas (Yuhina brunneiceps) at the Highlands Experiment Farm at Meifeng, National Taiwan University, in 1995 and from 1997–2002. The Taiwan Yuhina is a joint-nesting, cooperatively breeding species endemic to Taiwan. Males had significantly longer wing chords and tail lengths than females, probably due to sexual selection. Males also had a longer residence time at Meifeng than their female mates, which could be explained by philopatry being greater in males. Alpha males had a significantly longer residence time at Meifeng than beta males, but this was not the case for females, because females did not remain in the same group as males did after their mates disappeared. The breeding season was approximately 6 months long and multiple brooding was common. Nest building took 3 days, egg laying occurred over 3–4 days, the average incubation period was 14 days, and the nestling period was 12 days. Breeding success did not decrease later in the breeding season....

Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis)—male monopolisation, female mate choice or post-copulatory mechanisms?

One of the basic principles of sexual selection is that male reproductive success should be skewed towards strong males in species with anisogamous sex. Studies on primate multi-male groups, however, suggest that other factors than male fighting ability might also affect male reproductive success. The proximate mechanisms leading to paternity in multi-male primate groups still remain largely unknown since in most primate studies mating rather than reproductive success is measured. Furthermore, little research focuses on a female’s fertile phase. The aim of this study was to investigate the relative importance of male monopolisation and female direct mate choice for paternity determination. We also investigated the extent to which paternity was decided post-copulatory, i.e. within the female reproductive tract. We used a combined approach of behavioural observations with faecal hormone and genetic analysis for assessment of female cycle stage and paternity, respectively. The study was carried out on a group of wild long-tailed macaques living around the Ketambe Research Station, Gunung Leuser National Park, Indonesia. Our results suggest that both male monopolisation and post-copulatory mechanisms are the main determinants of male reproductive success, whereas female direct mate choice and alternative male reproductive strategies appear to be of little importance in this respect. Female cooperation may, however, have facilitated male monopolisation. Since paternity was restricted to alpha and beta males even when females mated with several males during the fertile phase, it seems that not only male monopolisation but also post-copulatory mechanisms may operate in favour of high-ranking males in long-tailed macaques, thus reinforcing the reproductive skew in this species.

Reproductive partitioning among polyandrous alpha and beta pale chanting-goshawk males

This study investigates the reproductive and parental roles of polyandrous male pale chanting-goshawks, Melierax canorus, and speculatively reviews the fitness outcomes of different skew and relatedness scenarios. The study was conducted over five years in the Little Karoo, South Africa. Although, polyandrous males participated equally in building nests, provisioning prey and incubating, in the fertility window the dominant alpha males copulated 31–5 days before the females laid, whereas subordinate beta males only copulated 5–3 days before laying. If this copulation timing by alpha males was indicative of a high reproductive skew, alpha males breeding as full sibs could skew paternity in their favour (ratio 68:32) and produce 0.69 offspring equivalents. Under this scenario, they compensated beta males with indirect fitness benefits by allowing them to produce 0.54 offspring equivalents, equal to monogamous males. Alternatively, if beta males controlled reproduction while breeding with non-relatives under a high skew scenario, they would have to restrain themselves to avoid eviction and produce 0.28 offspring equivalents to allow the fitness of alpha males at least to equal that of monogamous males. I suggest that alpha males and their females altered their reproductive roles to accommodate beta males, thereby increasing their inclusive fitness, whereas beta males tolerated subordination to acquire reproductive skills that non-breeder males do not have access to.

Speckled warblers break cooperative rules: absence of helping in a group-living member of the Pardalotidae

In the majority of cooperatively breeding bird species, subordinates help the dominant pair to provision the young, regardless of the origin of groups and relatedness between members. Within the family that includes speckled warblers, Chthonicola sagittata, there is considerable variation in social organization and parental behaviour, but the societies of other group-living species in this family are of kin, and subordinates provision the young of breeders. Speckled warblers differ in that offspring are never philopatric, and breeding groups comprise unrelated individuals. We used behavioural observations and DNA fingerprinting to examine genetic parentage and the mating system of the group-living speckled warbler in Canberra, Australia. Speckled warblers breed as pairs or in trios consisting of a female with two males. Alpha males are socially dominant to beta males and maintain dominance through aggression. Beta males never helped to feed nestlings or fledglings, even though they competed for copulations and in one case gained paternity of two of three young in a brood. The social system is therefore polyandrous but not cooperative. As well as competing for copulations with females on their own territories, beta males and single males (those that had lost their breeding partner) regularly undertook extraterritorial forays, most often when the neighbouring female was fertile. Failure by beta males to help even with broods containing their own offspring may be adaptive in this species and may result from increased opportunity for extrapair fertilizations or enhancement of prospects for future reproduction through the formation of alliances with females.

JOINT NESTING IN TAIWAN YUHINAS: A RARE PASSERINE CASE

Abstract Joint nesting, in which more than one pair contributes eggs to a group nest, is rare among cooperatively breeding birds. Early reports of the breeding biology of Taiwan Yuhinas (Yuhina brunneiceps) described them as joint nesters; however, these studies were preliminary and did not involve color-banded individuals. We conducted a 7-year study on the breeding biology of yuhinas. We found that the frequency of joint nesting was extremely high (90% of groups). Breeding groups were composed of two to seven adults (mode = 4). Most of the juveniles (78%) disappeared from our study site the year after they hatched. Only 6% remained in their natal groups; therefore, our study groups appeared to be composed primarily of non-kin. Within each group, there was a linear hierarchy of socially monogamous pairs. Mean reproductive skew index, as determined by microsatellite markers, was low (0.19). Alpha males had longer wings than beta males, whereas females did not show any differences in body size. Breeding gr...

State-dependent sentinels: an experimental study in the Arabian babbler.

Natural patterns of cooperative sentinel behaviour in Arabian babblers, Turdoides squamiceps, have proven consistent with state-dependent models of individually selfish anti-predator strategies. Here we demonstrate experimentally that sentinel effort within groups is determined simply by individual state. The two highest-ranking males in eight groups were separately fed a supplement of mealworms, each for one day at a time. Control days before and after each treatment confirmed that no carry-over effects occurred, and that most normal sentinel activity was carried out by alpha males, then beta males and then by the rest of the group. When supplemented, both alpha and beta males exhibited similar marked increases in sentinel activity, relative to control days. Unsupplemented males and the rest of the group incompletely compensated for these increases with reductions in sentinel effort. Differences in individual body mass within groups reflected natural and experimental variation in sentinel effort. Alpha and beta males weighed more than other group members, and gained mass only when supplementally fed. There was no evidence either for competitive sentinel behaviour, nor for any increased interference between males during the supplementation treatments. These results therefore provide strong evidence in support of the state-dependent approach to cooperative sentinel behaviour.

Reproduction by subordinates in cooperatively breeding Arabian babblers is uncommon but predictable

In a genetic analysis of the mating system of cooperatively breeding Arabian babblers (Timalidae: Turdoides squamiceps), we identified which individuals in the population are breeding, and how reproductive success was distributed among group members with respect to their dominance rank, for both males and females. The population was characterized by an asymmetrical distribution of reproductive success; behaviorally dominant males produced 176 of 186 (95%) of the offspring in 44 social groups analyzed, and alpha females produced 185 of 186 (99.5%). We evaluated models of reproductive skew by examining genetic and demographic correlates of reproduction by␣subordinates. Subordinate (beta) males that sired young were more likely to be recent dispersers from their natal groups or members of newly formed groups than betas that did not reproduce. Breeding beta males had spent smaller proportions of their lives with the current alpha male and female as alphas than had beta males that did not sire young. One consequence of the linkage of dispersal with breeding in newly formed, nonnatal groups is that beta males that sired young had significantly lower genetic similarity to the alpha males in their groups (based on band-sharing coefficients using multilocus minisatellite DNA fingerprinting) than those that did not sire young. This pattern may occur generally in species in which group membership accrues both through nondispersal of young (forming groups of relatives) as well as through dispersal involving coalitions that sometimes include nonrelatives.

Male parental effort and paternity in a variable mating system

Recent theoretical models suggest that males may respond to changes in paternity by adjusting their parental effort. Male response will depend on the availability of reliable paternity cues and the relative costs and benefits of parental effort to the male (i.e. its effect on the survival of young and alternative mating opportunities). Males breeding in pairs may be constrained because reductions in male parental effort are unlikely to be compensated for by the female and thus the survival of both related and unrelated young may decrease. In contrast, males breeding in cooperative groups (i.e. with helpers or co-breeders) may not have this constraint if other individuals in the group compensate for reductions in male parental effort. White-browed scrubwrens,Sericornis frontalis, breed in pairs and cooperative groups, typically with one female and two males (alpha and beta). We found that male parental effort was related positively to paternity for beta males, but not for alpha or pair males. Alpha males had paternity in all broods and always fed young. In contrast, beta males often had no paternity and sometimes did not feed young. Time spent near the fertile female was not an accurate predictor of the percentage of young sired in a brood, but it was a good predictor of having sired young in a brood. Our results are consistent with the idea that male parental effort is allocated according to whether or not the male copulated with the female. We suggest that the relationship between male parental effort and paternity may vary among cooperatively breeding species depending on the type and availability of cues to a male's paternity.

Multiple mating and cooperative breeding in polygynandrous alpine accentors. II. Male mating tactics

I studied the timing and frequency of male copulatory behaviour in alpine accentors,Prunella collaris, in Japan, with respect to dominance status, age and development of the cloacal protuberance. Males used one of three mating tactics depending on their dominance status. Alpha males guarded several females in succession, but only during the females’ fertile period, while gamma males copulated rarely and only with unguarded females. The tactics of beta males were flexible: with unguarded females they usually adopted a frequent-copulation tactic, but when two females had synchronous egg-laying periods, beta males associated closely with whichever female the alpha male left unguarded. When alpha males closely guarded a female, beta males guarded this same female for short periods before and after the guarding period of the alpha male. Subordinate rank restricted a male's opportunities for mating but males of all dominance ranks were sexually active and had fully developed cloacal protuberances. Frequent copulation plus part-time mate guarding (as found in beta males) and opportunistic copulation (as found in gamma males) appears to be a conditional strategy whereby young, subordinate males are ‘making the best of a bad job’. A long-term study over 10 years showed that males moved up in social rank with increasing age but 78.9% of males remained subordinate because alpha males occupied the top rank for much of their lifetime.

Relatedness, polyandry and extra-group paternity in the cooperatively-breeding white-browed scrubwren ( Sericornis frontalis )

We used DNA fingerprinting to examine the genetic parentage and mating system of the cooperatively breeding white-browed scrubwren, Sericornis frontalis, in Canberra, Australia. Our analyses revealed a remarkable variety of mating tactics and social organization. Scrubwrens bred in pairs or multi-male groups that consisted of a female and two or more males. Females were always unrelated to the pair male or alpha (dominant) male. Among multi-male groups we found three different mating tactics. Firstly, when alpha and beta (subordinate) males were unrelated, they usually shared paternity in the brood. This resulted in both males gaining reproductive benefits directly. Secondly, when beta males were not related to the female but were related to the alpha males, beta males sired offspring in some broods. In this situation, beta males gained reproductive benefits both directly and potentially indirectly (through the related alpha male). Thirdly, when beta males were related to the female or both the female and alpha male, they remained on their natal territory and did not sire any offspring. Thus beta males gained only indirect reproductive benefits. Overall, when group members were related closely, the dominant male monopolized reproductive success, whereas when the members were not related closely the two males shared paternity equally. This positive association between monopolization of reproduction and relatedness is predicted by models of reproductive skew, but has not been reported previously within a single population of birds. Other cooperatively breeding birds with both closely related and unrelated helpers may show a similar variety of mating tactics. Finally, we found that extra-group paternity was more common in pairs (24% of young) than in multi-male groups (6%), and we discuss three possible reasons for this difference.

Rank and reproduction in cooperatively breeding African wild dogs: behavioral and endocrine correlates

African wild dogs (Lycaon pictus) live in cooperative packs with a clear-cut dominance hierarchy in each sex. Reproduction is largely monopolized by the dominant male and female. Alpha females produced 76% of all litters in the Selous Game Reserve and 81% in Kruger National Park. Only 6-17% of subordinate females gave birth each year, compared to 82% of dominant females. In nonmating periods, subordinate females had higher estrogen levels and higher estrogen/progestin ratios than alpha females, apparently preventing ovulation. During mating periods, subordinate females had lower estrogen levels than dominants, mated less often, and were less aggressive. Subordinate males mated at low rates, wore less aggressive than dominants, and had lower testosterone levels. Beta males were similar to alpha males behavioraDy and hormonaUy, suggesting that alpha males may share paternity with beta males. If paternity is more evenly shared than maternity, then subordinate males have a larger incentive than subordinate females to remain in the pack. Following this expectation, dispersal in Selous was female biased (49% versus 24% dispersing annually). Perhaps as a result of mortality associated with dispersal, the adult sex ratio was male biased, although the pup sex ratio was unbiased. In Kruger, neither dispersal nor the adult sex-ratio was biased. Reproductive suppression is widely thought to be caused by social stress in subordinates, but basal cortkosterone levels were higher in dominants than in subordinates

Relation between the longitudinal development of lipoprotein levels and biological parameters during adolescence and young adulthood in Amsterdam, The Netherlands.

To analyse the relation between the longitudinal development of total serum cholesterol (TC), high density lipoprotein cholesterol (HDL), and the TC/ HDL ratio and the longitudinal development of the biological parameters body fatness (SSF), lean body mass (LBM), and cardiopulmonary fitness (VO2-max). The relations were analysed with generalised estimating equations (GEE). The relations were investigated with data from the Amsterdam growth and health study, a longitudinal study in which six measurements were carried out within a period of 15 years. Altogether 98 females and 84 males aged 13 years at the start of the study. Adjusted for lifestyle and other biological parameters, the longitudinal development of TC was inversely related to the development of LBM (standardised regression coefficient beta = -0.27; p < or = 0.01) and positively to SSF (beta males = 0.32; p < or = 0.01 and beta females = 0.15; p < or = 0.01). HDL was inversely related to LBM (beta = -0.26; p < or = 0.01) and positively to VO2-max (beta = 0.08; p < or = 0.05). The TC/HDL ratio was positively related to SSF (beta males = 0.39; p < or = 0.01 and beta females = 0.13; p < or = 0.01) and inversely to VO2-max (beta = -0.09; p < or = 0.05). The longitudinal analyses showed that body fatness was related to a high risk profile with respect to hypercholesterolaemia, and cardiopulmonary fitness to a low risk profile. Furthermore, it was shown that using body mass index as an indicator of body fatness in relation to lipoprotein values, has some important drawbacks.

Breeding Ecology of the Short-tailed Bush Warbler Cettia squameiceps in Western Hokkaido

Breeding ecology of the Short-tailed Bush Warbler Cettia squarneiceps was investigated in western Hokkaido during five seasons (1990-1994). The first arrival and first egg-laying dates were similar among years. Clutch sizes varied between 4-6 eggs, but they decreased as the breeding season progressed. The mean incubation and nestling period was 12.9±0.5 days (SD, n=18) and 10.0±0.4 days (SD, n=17), respectively. Only females incubated eggs and brooded nestlings for a long period of time. Most of the feeding of the young was conducted by males. Different (beta or gamma) males from the resident (alpha) male appeared and sometimes fed the young in 48.1% of twenty five nests observed. Some males were captured at locations far from their own nests, while there were only few cases in which a female was captured at a place distant from her mate's song area. As it was often observed that a beta male was the neighboring territory holder and his own nest was in the incubation period, it is hypothesized that some males who are emancipated from the incubation, might visit other territories to seek extra-pair copulations (EPC). We have, however, not observed mating between a female and a beta male except in the case of a widow. Within the breeding season, the females usually selected the same partner for the second brood. Main reason why the divorce rate within the season is low for the warbler in our study area is probably the high success rate for the first brood.