Sex differences in the drivers of reproductive skew in a cooperative breeder

Many cooperatively breeding societies are characterized by high reproductive skew, such that some socially dominant individuals breed, while socially subordinate individuals provide help. Inbreeding avoidance serves as a source of reproductive skew in many high‐skew societies, but few empirical studies have examined sources of skew operating alongside inbreeding avoidance or compared individual attempts to reproduce (reproductive competition) with individual reproductive success. Here, we use long‐term genetic and observational data to examine factors affecting reproductive skew in the high‐skew cooperatively breeding southern pied babbler (Turdoides bicolor). When subordinates can breed, skew remains high, suggesting factors additional to inbreeding avoidance drive skew. Subordinate females are more likely to compete to breed when older or when ecological constraints on dispersal are high, but heavy subordinate females are more likely to successfully breed. Subordinate males are more likely to compete when they are older, during high ecological constraints, or when they are related to the dominant male, but only the presence of within‐group unrelated subordinate females predicts subordinate male breeding success. Reproductive skew is not driven by reproductive effort, but by forces such as intrinsic physical limitations and intrasexual conflict (for females) or female mate choice, male mate‐guarding and potentially reproductive restraint (for males). Ecological conditions or “outside options” affect the occurrence of reproductive conflict, supporting predictions of recent synthetic skew models. Inbreeding avoidance together with competition for access to reproduction may generate high skew in animal societies, and disparate processes may be operating to maintain male vs. female reproductive skew in the same species.     

Early growth,dominance acquisition and lifetime reproductive success in male and female cooperative meerkats

In polygynous species, variance in reproductive success is higher in males than females. There is consequently stronger selection for competitive traits in males and early growth can have a greater influence on later fitness in males than in females. As yet, little is known about sex differences in the effect of early growth on subsequent breeding success in species where variance in reproductive success is higher in females than males, and competitive traits are under stronger selection in females. Greater variance in reproductive success has been documented in several singular cooperative breeders. Here, we investigated consequences of early growth for later reproductive success in wild meerkats. We found that, despite the absence of dimorphism, females who exhibited faster growth until nutritional independence were more likely to become dominant, whereas early growth did not affect dominance acquisition in males. Among those individuals who attained dominance, there was no further influence of early growth on dominance tenure or lifetime reproductive success in males or females. These findings suggest that early growth effects on competitive abilities and fitness may reflect the intensity of intrasexual competition even in sexually monomorphic species.     

Lifetime patterns of pairing success in male Ortolan Buntings Emberiza hortulana

Analyses of lifetime fitness in birds are typically based on estimates of breeding success, in particular the number of offspring fledged. Small and isolated bird populations often have a male‐skewed adult sex ratio, so that male lifetime productivity depends to a large degree on pairing success, but few studies have focused on patterns of lifetime pairing success. The Norwegian population of Ortolan Buntings Emberiza hortulana is strongly male‐skewed, such that in any year about half of all males are unpaired. Pairing success of first‐year males (16–44%) was significantly lower than for older males (52–89%). Lifetime pairing success was correlated with lifespan and was strongly skewed, with a majority of males being paired only once or never, and only 11% paired three or more times despite a stable lifetime annual survival rate of 63%. Males that were paired in one year were more likely to be paired the next year than males that were unpaired in the previous year. The shortage of females caused even the older males to have a substantial probability of becoming unpaired, and 49% of long‐lived males (known as adults for at least 4 years) were unpaired after years in which they were paired. Pairing success in the Ortolan Bunting therefore follows similar age‐related and lifetime patterns in breeding success documented in other species. However, even the older males ran a high risk of not being paired, contrasting with earlier distinctions between pre‐breeding and breeding lifespans. I discuss the importance of knowledge of pairing success for the management of endangered and declining populations.     

Delayed breeding affects lifetime reproductive success differently in male and female green woodhoopoes

In cooperatively breeding species, many individuals only start breeding long after reaching physiological maturity [1], and this delay is expected to reduce lifetime reproductive success (LRS) [1-3]. Although many studies have investigated how nonbreeding helpers might mitigate the assumed cost of delayed breeding (reviewed in [3]), few have directly quantified the cost itself [4, 5] (but see [6, 7]). Moreover, although life-history tradeoffs frequently influence the sexes in profoundly different ways [8, 9], it has been generally assumed that males and females are similarly affected by a delayed start to breeding [7]. Here, we use 24 years of data to investigate the sex-specific cost of delayed breeding in the cooperatively breeding green woodhoopoe (Phoeniculus purpureus) and show that age at first breeding is related to LRS differently in males and females. As is traditionally expected, males that started to breed earlier in life had greater LRS than those that started later. However, females showed the opposite pattern: Those individuals that started to breed later in life actually had greater LRS than those that started earlier. In both sexes, the association between age at first breeding and LRS was driven by differences in breeding-career length, rather than per-season productivity. We hypothesize that the high mortality rate of young female breeders, and thus their short breeding careers, is related to a reduced ability to deal with the high physiological costs of reproduction in this species. These results demonstrate the importance of considering sex-specific reproductive costs when estimating the payoffs of life-history decisions and bring into question the long-held assumption that delayed breeding is necessarily costly.     

Variation in selection pressure acting on body size by age and sex in a reverse sexual size dimorphic raptor

Body size strongly influences fitness, with larger individuals benefiting in terms of both greater productivity and survivorship; for reverse sexual size dimorphic (RSD) species, this relationship may be more complex. We examined the selection pressures acting on body size in male and female Merlins Falco columbarius to assess whether larger or smaller individuals of this RSD species were favoured in terms of survival and breeding performance. For males and females there were clear links between body size and survival but the exact relationship varied by sex. Among males, birds that survived each year class were larger than those that died and yearlings were on average smaller than older birds, but there were no measurable differences among adult males (age 2+). Among females, larger individuals aged 1 and 2 years were more likely to survive, but this size‐based pattern was not apparent in older age classes. Size early in life predicted the lifespan in male Merlins but not as strongly as for females and not for the largest individuals. Reproductive performance based on brood size was not associated with body size in either males or females, but there was a weak positive relationship between female body size and lifetime reproductive success. Selection appears to favour larger males and females but there is no indication that the population is evolving towards bigger individuals, perhaps in part due to selection against the largest birds. Increased survival may allow larger and higher quality individuals to occupy higher quality territories as they age and thereby to accrue greater lifetime reproductive success in the process.     

Costly reproductive competition between females in a monogamous cooperatively breeding bird

In many cooperatively breeding societies, only a few socially dominant individuals in a group breed, reproductive skew is high, and reproductive conflict is common. Surprisingly, the effects of this conflict on dominant reproductive success in vertebrate societies have rarely been investigated, especially in high-skew societies. We examine how subordinate female competition for breeding opportunities affects the reproductive success of dominant females in a monogamous cooperatively breeding bird, the Southern pied babbler (Turdoides bicolor). In this species, successful subordinate reproduction is very rare, despite the fact that groups commonly contain sexually mature female subordinates that could mate with unrelated group males. However, we show that subordinate females compete with dominant females to breed, and do so far more often than expected, based on the infrequency of their success. Attempts by subordinates to obtain a share of breeding impose significant costs on dominant females: chicks fledge from fewer nests, more nests are abandoned before incubation begins, and more eggs are lost. Dominant females appear to attempt to reduce these costs by aggressively suppressing potentially competitive subordinate females. This empirical evidence provides rare insight into the nature of the conflicts between females and the resultant costs to reproductive success in cooperatively breeding societies.     

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.     

Effects of recruiting age on senescence, lifespan and lifetime reproductive success in a long-lived seabird

Theories of ageing predict that early reproduction should be associated with accelerated reproductive senescence and reduced longevity. Here, the influence of age of first reproduction on reproductive senescence and lifespan, and consequences for lifetime reproductive success (LRS), were examined using longitudinal reproductive records of male and female blue-footed boobies (Sula nebouxii) from two cohorts (1989 and 1991). The two sexes showed different relationships between age of first reproduction and rate of senescent decline: the earlier males recruited, the faster they experienced senescence in brood size and breeding success, whereas in females, recruiting age was unrelated to age-specific patterns of reproductive performance. Effects of recruiting age on lifespan, number of reproductive events and LRS were cohort- and/or sex-specific. Late-recruiting males of the 1989 cohort lived longer but performed as well over the lifetime as early recruits, suggesting the existence of a trade-off between early recruitment and long lifespan. In males of the 1991 cohort and females of both cohorts, recruiting age was apparently unrelated to lifespan, but early recruits reproduced more frequently and fledged more chicks over their lifetime than late recruits. Male boobies may be more likely than females to incur long-term costs of early reproduction, such as early reproductive senescence and diminished lifespan, because they probably invest more heavily than females. In the 1991 cohort, which faced the severe environmental challenge of an El Ni?o event in the first year of life, life-history trade-offs of males may have been masked by effects of individual quality.     

Male brood provisioning rates provide evidence for inter‐age competition for mates in female Cooper's Hawks Accipiter cooperii

Life history theory predicts that individuals should maximize lifetime reproductive success (LRS) by breeding as soon as they reach sexual maturity, yet many species delay breeding, either because there are insufficient available mates or breeding sites, or because delayed breeding yields higher LRS. Accipitriform species, such as Cooper's Hawk Accipiter cooperii, exhibit both delayed breeding and delayed plumage maturation. However, in certain circumstances, first‐year females in non‐definitive plumage do breed and apparently compete with older females for high‐quality breeding territories. We predicted that these young females are at a competitive disadvantage compared with older females and that older females would have both higher reproductive success and be able to acquire higher quality nesting territories. We conducted brood counts and measured prey delivery rates by male Cooper's Hawks in an expanding urban population located in Albuquerque, New Mexico (USA), to assess our prediction. We found that older females had higher reproductive success, fledging 1.6 more offspring than younger females, and that they occupied territories where males provisioned at higher rates of 0.37 more prey items per 2‐h period. Our results showed that older females fared better than first‐year females but it is unclear if this is the result of passive or active competition. Older females initiated nesting 14.3 days sooner than first‐year females and thus may have filled vacant, high‐quality territories before first‐year females began seeking mates. Additionally, first‐year females were never observed persistently to confront older females for breeding territories, but they did actively compete against each other. First‐year females may defer to older females who, in a direct competitive interaction, would be most likely to prevail. Thus, delayed plumage maturation in Cooper's Hawks may serve to focus competition for nesting territories within age classes.     

Large males have a mating advantage in a species of darter with smaller, allopaternal males Etheostoma olmstedi

Theory suggests that males that are larger than their competitors may have increased mating success, due to both greater competitive ability and increased attractiveness to females. We examined how male mating success varies with male size in the tessellated darter Etheostoma olmstedi. Previous work has shown that large males tend to move around and breed in vacant breeding sites, and consequently provide less care for their eggs, while smaller individuals can be allopaternal, caring for the eggs of other males as well as for their own. We studied female egg deposition in a natural breeding population using artificial breeding sites and in the laboratory, where female choice of spawning site was restricted to two breeding sites tended by two males of different sizes. In both the field and the laboratory, nests tended by larger males were more likely to receive new eggs. Additionally, the mean size of males associated with a nest was positively correlated with both the maximum coverage of eggs at the nest and the number of times new eggs were deposited. We discuss how the increased mating success of larger males, despite their decreased parental care, may help explain allopaternal care in this species [Current Zoology 56 (1): 1-5, 2010].     

Should I Stay or Should I Go Now: Late Establishment and Low Site Fidelity as Alternative Territorial Behaviors

In species in which males defend territories for breeding, males may differ in territorial behavior; alternative behaviors among territorial males are not well understood. In our long‐term study of partially‐migratory song sparrows, we have observed that most territorial males establish territories before females begin nesting and remain site‐faithful both within and between breeding seasons; however, some males establish territories later in the season (late establishers) and/or change territory locations either within or between seasons (movers). Whether late establishment or moving are equally successful strategies for territory defense, or best‐of‐bad‐job options, is not known. Here, we compare the frequencies of these behaviors to demographic variables over a 9‐yr period and compare lifetime tenure and early season nesting success for males who differ in site fidelity and timing of territory establishment. Across years, late establishing was negatively correlated with the return rate of previously territorial males; moving was positively correlated with the number of occupied territories at the start of the breeding season (territory density). While moving was independent of number of years on territory, late territory establishment only occurred in a male’s first year as a territory holder. Of 88 males, 25% established their first territory late, primarily in undefended space; 31% moved. Late and early establishers did not differ in lifetime tenure; movers, however, had longer lifetime tenure than site‐faithful males. Among early establishers, movers and non‐movers did not differ in the number of successful early nests/year or number of young fledged/year; among late establishers, however, movers had significantly higher early nesting success by both measures. Late establishers who moved had higher early season nesting success and higher early season nesting success/year than site‐faithful early establishers. Thus, individual variation in the timing of territory establishment and site fidelity may be facultative alternative territorial strategies.     

Male reproductive strategy and the importance of maternal status in the Antarctic fur seal Arctocephalus gazella

Abstract. Although mammalian mating systems are classically characterized in terms of male competition and polygyny, it is becoming increasingly apparent that alternative male strategies and female choice may play important roles. For example, females who mate with males from a dominant dynasty risk producing inbred offspring. Many pinnipeds are highly polygynous, but in some species alternative male strategies such as aquatic mating appear to be important, even when behavioral observations suggest strong polygyny. Here, we analyze male reproductive success in the Antarctic fur seal Arctocephalus gazella , an otariid described behaviorally as being highly polygynous, by combining a microsatellite paternity analysis spanning seven consecutive breeding seasons with detailed behavioral data on both sexes. Territorial males fathered 59% of 660 pups analyzed from our study colony. Male reproductive skew was considerable, with a quarter of all paternities assigned to just 12 top individuals on a beach where mean annual pup production was 635. Most males were successful for only a single season, but those able to return over successive years enjoyed rapidly increasing success with each additional season of tenure. We found no evidence of alternative male reproductive tactics such as aquatic or sneaky terrestrial mating. However, paternity was strongly influenced by maternal status. Females observed on the beach without a pup were significantly less likely to conceive to a sampled territorial male than equivalent females that did pup. In addition, their pups carried combinations of paternal alleles that were less likely to be found on the study beach and exhibited lower levels of shared paternity. Thus, from a territorial male's perspective, not all females offer equal opportunities for fertilization.     

Preliminary analysis of reproductive success in a large mammal with alternative mating tactics,the Northern chamois,Rupicapra rupicapra

In polygynous mating systems, reproductive skew depends on the ability of males to monopolize females, which in turn may promote the development of contrasting traits in the two sexes. Although dominant individuals normally enjoy a higher reproductive success (RS) than subordinates, the use of genetic markers has shown that behavioural observations of male mating success may not provide reliable clues of RS. We report the preliminary results of the first DNA‐based paternity analysis on the Northern chamois (Rupicapra rupicapra), a scarcely dimorphic mountain ungulate described as highly polygynous, in relation to mating tactic and age. Because of sampling difficulties, the success in parentage assignment was low, and the interpretation of results requires caution. Territorial males had a greater RS than nonterritorial ones but they were unable to monopolize mating events. Age had a weak effect on paternity outcome but only males ≥ 6 years showed siring success. Although future studies are needed to assess the opportunity for sexual selection in male chamois, the concurrence of limited sexual size dimorphism, compensatory growth, unbiased sex‐specific survival, RS of alternative mating tactics and, possibly, long breeding tenure, may hint at the adoption of a conservative mating strategy in this species.     

Lifetime mating success in the damselfly Coenagrion puella

Lifetime mating success of male azure damselflies (Coenagrion puella) was measured in a natural population. The major determinant of mating success is the number of days a male spends at the breeding site, which is mostly determined by a male's adult lifespan. Long-lived males have a higher mating rate than short-lived males, and daily mating rate increases with age up to 6 days, then falls. Large males live longer, but have a lower daily mating rate than small males. These effects of size are very weak, accounting for no more than 2% of the daily variance in mating success. The only overall effect of size on lifetime mating success is that males at both extremes of the size distribution are more likely to fail to mate. Chance differences in the number of females encountered are sufficient to account for the remaining variance in mating success. The weather is also shown to have a major effect on mating success. We draw attention to the ways in which it may be misleading to draw conclusions about the action of sexual selection from studies of daily, rather than lifetime, reproductive success. We provide evidence to support the view that variance in male reproductive success is neither evidence for sexual selection, nor a measure of its intensity.     

Coalitions of relatives and reproductive skew in cooperatively breeding white-winged choughs

We used DNA fingerprinting to examine reproductive skew in cooperatively breeding white-winged choughs, Corcorax melanorhamphos, which live in groups of up to 20 individuals. Before a severe drought, groups that had been stable for multiple years were characterized by long-term monogamy involving a single breeding pair (high skew). After the drought, new groups formed from the amalgamation of multiple individuals and coalitions of relatives. At most one member of each faction succeeded in breeding, such that skew was dependent on the number of unrelated factions, and not group size. In the new groups, dominant males and females with supporting relatives were always successful. Whereas most females without support also gained breeding positions, many males without family support failed to breed. Thus subordinates gain indirect fitness by first helping related males to secure a breeding position, and then helping to raise their young. Our study demonstrates the advantage of operating in coalitions, and suggests that the acquisition of future allies may be a major benefit of helping behaviour in this species.     

Male rank, female breeding synchrony, and patterns of paternity in the boat-tailed grackle

Species in which males directly defend groups of breeding femalesoften have extreme skew in observed male mating success. Inonly a few species, however, has a corresponding skew in fertilizationsuccess been confirmed. Furthermore, the ecological and socialfactors contributing to variation in fertilization success needinvestigation. This study examined competition for mates andpaternity in the boat-tailed grackle (Quiscalus major). Observationsat colonies of nesting females revealed that the toprankingor alpha males performed more than 70% of the copulations. DNAfingerprinting indicated that alpha males sired less than 40%of nestlings. Nevertheless, analysis of band-sharing scoresamong nestlings from different nests suggested that alpha malessired more than three times as many offspring as any other individualmale. Because few nestlings were sired by the nonalpha malesthat associated with colonies, females must have mated withother males while on trips away from colonies. Analysis of paternitywithin broods revealed that at least half of all females hadtheir brood fertilized by more than one male. Alpha males' successat fertilizing eggs did not vary with the number of simultaneouslyreceptive females within a colony. Our results suggest that maleand female behavior in female-defense polygyny results fromcomplex coevolution of the sexes.     

Inbreeding avoidance and female mate choice shape reproductive skew in capuchin monkeys (Cebus capucinus imitator)

Reproductive skew in multimale groups may be determined by the need for alpha males to offer reproductive opportunities as staying incentives to subordinate males (concessions), by the relative fighting ability of the alpha male (tug‐of‐war) or by how easily females can be monopolized (priority‐of‐access). These models have rarely been investigated in species with exceptionally long male tenures, such as white‐faced capuchins, where female mate choice for novel unrelated males may be important in shaping reproductive skew. We investigated reproductive skew in white‐faced capuchins at Sector Santa Rosa, Costa Rica, using 20 years of demographic, behavioural and genetic data. Infant survival and alpha male reproductive success were highest in small multimale groups, which suggests that the presence of subordinate males can be beneficial to the alpha male, in line with the concession model's assumptions. None of the skew models predicted the observed degree of reproductive sharing, and the probability of an alpha male producing offspring was not affected by his relatedness to subordinate males, whether he resided with older subordinate males, whether he was prime aged, the number of males or females in the group or the number of infants conceived within the same month. Instead, the alpha male's probability of producing offspring decreased when he was the sire of the mother, was weak and lacked a well‐established position and had a longer tenure. Because our data best supported the inbreeding avoidance hypothesis and female choice for strong novel mates, these hypotheses should be taken into account in future skew models.     

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

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

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.