Extrapair paternity, inclusive fitness, and within-group benefits of helping in western bluebirds

In central coastal California, USA, 3–16% of western bluebird ( Sialia mexicana ) pairs have adult male helpers at the nest. Demographic data on a colour-ringed population over a 13-year period indicate that helpers gain a small indirect fitness benefit through increases in the number of young fledged from nests of close kin. A small proportion of adult helpers (16%) that were able to breed and help simultaneously had higher annual inclusive fitness than males that only bred. These males comprised such a minor proportion of helpers that the mean fitness of helpers was still lower than the mean fitness of independent breeders. We used DNA fingerprinting to determine whether extrapair fertilizations alter within-group benefits enough to tip the balance in favour of helping behaviour. Overall, 19% of 207 offspring were sired by males other than their social father and extrapair fertilizations occurred in 45% of 51 nests. Intraspecific brood parasitism was rare so that mean mother-nestling relatedness approximated the expected value of 0.5. Extrapair paternity reduced putative father-offspring relatedness to 0.38. Mean helper-nestling relatedness was 0.41 for helpers assisting one or both parents and 0.28 for helpers aiding their brothers. Helpers rarely sired offspring in the nests at which they helped. Helping was not conditional on paternity and helpers were not significantly more closely related to offspring in their parents' nests than to offspring in their own nests. Although helpers may derive extracurricular benefits if helping increases their own or their father's opportunities for extrapair fertilizations, within-nest inclusive fitness benefits of helping do not compensate males for failing to breed. Breeding failure and constraints on breeding are the most likely explanations for why most helpers help.     

Shared parentage and incest avoidance in the cooperatively breeding acorn woodpecker

Social groups of acorn woodpeckers (Melanerpes formicivorus) range in size from unaided pairs to 15 adults. Behavioural indicators of mate guarding, assumed incest avoidance and observations of egg-laying indicate that social organization ranges from monogamous pairs to groups with up to seven male and three female putative cobreeders plus up to 10 nonbreeding helpers. In addition, groups occasionally lack a putative breeder throughout the breeding season. Here we report results from multilocus DNA fingerprinting of 372 nestlings from 123 nests in groups with putative cobreeders of one or both sexes. No extra-group fertilizations were found. Putative cobreeding males within social groups shared paternity. However, the most reproductively successful male was, on average, almost three times as successful as the next most successful and additional males only occasionally sired offspring. In contrast, cobreeding females shared parentage equally. Helpers never bred incestuously when their opposite-sex parent (or another relative, such as their uncle) held breeding status in the group. However, during breeding male vacancies, 14 nestlings were produced when helper males bred incestuously with their mother. Both male and female helpers usually became successful cobreeders with their same-sex parent following replacement of the opposite-sex breeder(s) by unrelated individuals.     

Reproductive roles in the cooperatively breeding acorn woodpecker: incest avoidance versus reproductive competition

Incest is rare in the cooperatively breeding acorn woodpecker (Melanerpes formicivorus) despite a polygynandrous mating system in which nearly all group members are close relatives. Here we test the relative importance of avoiding matings between close relatives (incest avoidance) and within-sex competition for breeding opportunities (reproductive competition) in determining the mating system of acorn woodpeckers by examining how reproductive roles change following breeding vacancies. In 83% of cases in which helpers of the same sex were present in the group, reproductive vacancies were resolved when new unrelated immigrants filled the vacancy to the exclusion of resident same-sex helpers, who generally emigrated or did not breed while they remained in the group. Helpers of the opposite sex, especially when male, were significantly more likely to remain in their natal group and in about half the cases inherited and bred following reproductive vacancies. This result was not explainable by reproductive competition, since the number of immigrants was often less than or equal to the number of same-sex helpers in the group. Apparent incest resulted in 5% of cases. The time required to resolve reproductive vacancies was significantly longer for groups with helpers of the same sex as the vacancy. These results confirm that both incest avoidance and reproductive competition are important factors determining reproductive roles within groups of this highly social species.     

Breeding Biology and Variable Mating System of a Population of Introduced Dunnocks (Prunella modularis) in New Zealand

Species with variable mating systems provide a unique opportunity to investigate whether females receive direct fitness benefits from additional male partners. The direct benefits provide an obvious explanation for why females would breed polyandrously, in a situation where males clearly do not attain their optimal reproductive success. Evidence for these direct benefits is, however, mixed. Here, we present a detailed study of the breeding biology of the dunnock, Prunella modularis, which inform an investigation into the effects of the social mating system on the reproductive success in a population of dunnocks in Southern New Zealand. We studied 80 different social groups over the course of three breeding seasons. Dunnocks in our population presented a variable mating system, with socially monogamous (45%), socially polyandrous (54%) and socially polygynandrous (1%) groups being observed in the same breeding season. We did not observe any polygynous social units in our study period although polygyny exists in the population. We found little difference in the numbers of eggs laid, and egg volume between monogamous and polyandrous nests. However, polyandrous groups had better hatching and fledging success than monogamous groups (composite d = 0.385, 95% CI: 0.307 to 0.463). Overall our results support the notion that polyandry is beneficial for females.     

Living with strangers: direct benefits favour non-kin cooperation in a communally nesting bird

The greater ani (Crotophaga major), a Neotropical cuckoo, exhibits an unusual breeding system in which several socially monogamous pairs lay eggs in a single nest and contribute care to the communal clutch. Cooperative nesting is costly-females compete for reproduction by ejecting each other's eggs-but the potential direct or indirect fitness benefits that might accrue to group members have not been identified. In this study, I used molecular genotyping to quantify patterns of genetic relatedness and individual reproductive success within social groups in a single colour-banded population. Microsatellite analysis of 122 individuals in 49 groups revealed that group members are not genetic relatives. Group size was strongly correlated with individual reproductive success: solitary pairs were extremely rare and never successful, and nests attended by two pairs were significantly more likely to be depredated than were nests attended by three pairs. Egg loss, a consequence of reproductive competition, was greater in large groups and disproportionately affected females that initiated laying. However, early-laying females compensated for egg losses by laying larger clutches, and female group members switched positions in the laying order across nesting attempts. The greater ani, therefore, appears to be one of the few species in which cooperative breeding among unrelated individuals is favoured by direct, shared benefits that outweigh the substantial costs of reproductive competition.     

Life histories and the evolution of cooperative breeding in mammals

While the evolution of cooperative breeding systems (where non-breeding helpers participate in rearing young produced by dominant females) has been restricted to lineages with socially monogamous mating systems where coefficients of relatedness between group members are usually high, not all monogamous lineages have produced species with cooperative breeding systems, suggesting that other factors constrain the evolution of cooperative breeding. Previous studies have suggested that life-history parameters, including longevity, may constrain the evolution of cooperative breeding. Here, we show that transitions to cooperative breeding across the mammalian phylogeny have been restricted to lineages where females produce multiple offspring per birth. We find no support for effects of longevity or of other life-history parameters. We suggest that the evolution of cooperative breeding has been restricted to monogamous lineages where helpers have the potential to increase the reproductive output of breeders.     

Long-term fitness benefits of egg sex modification by the Seychelles warbler

Sex-ratio theory states that if the fitness costs to the parents of producing one offspring's sex relative to the other are higher, parents should discount these costs by producing fewer individuals of the more costly sex. In the co-operatively breeding Seychelles warbler (Acrocephalus sechellensis) mothers adaptively modify the sex of their single egg toward daughters, the helping sex, when living on territories with rich resources where helpers increase parental reproductive success, but toward sons, the dispersing sex, when living on territories where resources are scarce and/or no helping benefits accrue. By modifying offspring sex ratio, parents maximize their inclusive fitness benefits. Pairs in high-quality territories gained significantly more inclusive fitness benefits (through helping and reproducing offspring) from the production of daughters than from sons, and vice versa in low-quality territories (through reproducing offspring). Experimental manipulation of the offspring's sex shows that the consequences of sex allocation are adaptive for parents on high-quality territories. On high-quality territories with female production, breeding pairs raising step-daughters gained significantly higher inclusive benefits (through indirect and direct fitness gains) than by raising step-sons.     

Genetic analysis reveals diverse kin‐directed routes to helping in the rifleman Acanthisitta chloris

The social organization of cooperatively breeding species is extremely variable, with diverse social group composition and patterns of relatedness. Species that exhibit alternative routes to helping within the same population are potentially useful systems to investigate the causes and fitness consequences of diverse evolutionary pathways to cooperative behaviour. In this study, we use microsatellite markers and field observations to describe helping behaviour and patterns of relatedness in the unusual cooperative breeding system of the rifleman Acanthisitta chloris. First, we show that rifleman helpers consist of a remarkably diverse demographic, including males and females, who may be adult or juvenile, failed breeders or nonbreeders, or even successful breeders that simultaneously feed their own brood. Adult helpers mostly helped at first‐brood nests, while first‐brood juveniles assisted their parents at second broods. Second, we show that rifleman pairs are strictly sexually monogamous, and helpers did not gain any current reproductive success through helping. Third, genotyping showed that contrary to previous assumptions, helpers were closely related to the recipients of their care and preferentially directed care towards relatives over contemporaneous nests of nonrelatives. Finally, we show that variation in helper provisioning effort was attributed to age: juvenile helpers provisioned less than adults and were less responsive to the demands of a growing brood. Overall, our results show that the diverse routes to helping in this unusual species are driven by the common theme of kinship between helper and recipients, resulting in a previously underestimated potential for helpers to gain indirect fitness benefits.     

Helpers benefit offspring in both the short and long-term in the cooperatively breeding banded mongoose

Helpers in cooperative and communal breeding species are thought to accrue fitness benefits through improving the condition and survival of the offspring that they care for, yet few studies have shown conclusively that helpers benefit the offspring they rear. Using a novel approach to control for potentially confounding group-specific variables, I compare banded mongoose (Mungos mungo) offspring within the same litter that differ in the amount of time they spend with a helper, and hence the amount of care they receive. I show that pups that spend more time in close proximity to a helper are fed more, grow faster and have a higher probability of survival to independence than their littermates. Moreover, high growth rates during development reduce the age at which females breed for the first time, suggesting that helpers can improve the future fecundity of the offspring for which they care. These results provide strong evidence that it is the amount of investment per se that benefits offspring, rather than some correlate such as territory quality, and validate the assumption that helpers improve the reproductive success of breeders, and hence may gain fitness benefits from their actions. Furthermore, the finding that helpers may benefit offspring in the long-term suggests that current studies underestimate the fitness benefits that helpers gain from rearing the offspring of others.     

Male Seychelles warblers use territory budding to maximize lifetime fitness in a saturated environment

In cooperatively breeding species, helping at the nest and buddingoff part of the natal territory have been advanced as strategiesto increase fitness in an environment that is saturated withterritories. The importance of helping or territory buddingas a determinant of lifetime reproductive success (LRS) hasbeen debated because the potential benefits of both strategiescould not be separated. Here we test the causes and the immediateand future fitness consequences of single dispersal decisionstaken by male Seychelles warblers (Acrocephalus sechellensis).Males breeding in high-quality territories (high food abundance)have significantly higher LRS than similar-aged males buddingoff part of the parental territory. Initially, budders havea low reproductive success (because of limited food resourcesor absence of a breeding partner). However, they have a longlife span and inherit high-quality territories through sitedominance, by which they gain higher LRS than breeders on low-qualityterritories, helpers, or floaters. Experimental creation ofmale breeding territory vacancies showed that most young malesbecame budders because of intense competition for high-quality territories. The translocation of warblers to the previouslyunoccupied Aride Island shows that males behave according tothe expected fitness benefits of each dispersal strategy. Inthe absence of competition for territories on Aride, all youngmales bred in high-quality territories. However, after saturationof high-quality habitat with territories, most males becamebudders rather than breeders on low-quality habitat, helpers,or floaters.     

Genotype and extra-pair paternity in the house wren: a rare-male effect?

Females in socially monogamous species may select extra-pair (EP) mates to increase the heterozygosity, and hence fitness, of their offspring. We tested this hypothesis in the house wren (Troglodytes aedon), a largely monogamous songbird in which EP young are common. We typed paired males and females, nestlings, and males on neighbouring territories, at five to seven microsatellite loci over 2 years in a Wyoming, USA, population. We identified EP sires at 20 nests with EP young. In pairwise comparisons, we found no significant differences between cuckolded within-pair (WP) males and EP sires in three measures of heterozygosity (mean d2, standardized heterozygosity and internal relatedness). However, EP sires had fewer alleles that were common within the population than did the WP males they cuckolded. Nearby males who were EP sires also had fewer common alleles than did nearby males who did not sire EP young. Females in our population may be more prone to accept copulations from males with rare genotypes than from males with common genotypes. Alternatively, selection of rare-male sperm may occur within the female reproductive tract. Because mating with rare males is likely to increase offspring heterozygosity, our data suggest that EP mating may provide genetic benefits to females.     

Fitness consequences of helping behavior in the western bluebird

We examined the fitness consequences of helping behavior inthe western bluebird (Sialia mexicana) at Hastings Reservationin Carmel Valley, California, USA, and tested hypotheses forhow helpers benefit from engaging in alloparental behavior.Both juvenile and adult western bluebirds occasionally helpat the nest During a 12 year period, all adult helpers and mostjuvenile helpers were male. Helpers usually fed at nests ofboth their parents and rarely helped when only one parent waspresent. The frequency of pairs with adult helpers was only7%, but nearly one-third of adult males helped among those withboth parents on the study area. At least 28% were breeders whosenests failed. The propensity to help appears to depend uponparental survival, male philopatry, and the breeding successof potential helpers. Feeding rates were not increased at nestswith juvenile helpers, apparendy because breeding males reducedtheir feeding rates. In contrast, adult helpers increased theoverall rates of food delivery to the nest in spite of a reductionin the number of feeding trips made by both male and femaleparents. Helpers did not derive any obvious direct fitness benefitsfrom helping, but they had greater indirect fitness than nonhelpersdue to increases in nestling growth rates and fledging successat their parents' nests. Helpers fledged fewer offspring intheir first nests than did nonhelpers, suggesting that theywere birds with reduced reproductive potential. Although wehave not yet measured the effect of extrapair fertilizationson the fitness benefits of helping, we calculated the differencein fitness between helpers and nonhelpers as a function of thepotential helper's paternity when breeding independently andhis father's paternity in the nest at which he might help. Inconjunction with constraints on breeding and indirect fitnessbenefits, we predict that relatedness of males to the youngin their own as well as their parents' nests will influencehelping behavior in western bluebirds.     

Mating system, philopatry and patterns of kinship in the cooperatively breeding subdesert mesite Monias benschi

In the first molecular study of a member of the threatened avian family, Mesitornithidae, we used nine polymorphic microsatellite loci to elucidate parentage, patterns of within-group kinship and occurrence of extra-group paternity in the subdesert mesite Monias benschi, of southwest Madagascar. We found this cooperatively breeding species to have a very fluid mating system. There was evidence of genetic monogamy and polygynandry: of the nine groups with multiple offspring, six contained one breeding pair with unrelated helpers and three contained multiple male and female breeders with related helpers. Although patterns of within-group kinship varied, there was a strong positive relationship between group size and relatedness, suggesting that groups form by natal philopatry. There was also a strong positive correlation between within-sex and between-sex relatedness, indicating that unlike most cooperatively breeding birds, philopatry involved both sexes. In contrast to predictions of kin selection and reproductive skew models, all monogamous groups contained unrelated individuals, while two of the three polygynandrous groups were families. Moreover, although between-group variation in seasonal reproductive success was related to within-group female relatedness, relatedness among males and between the sexes had no bearing on a group's reproductive output. While kin selection may underlie helping behaviour in females, factors such as direct long-term fitness benefits of group living probably determine helping in males. Of the 14 offspring produced by fully sampled groups, at least two were sired by males from neighbouring groups: one by a breeding male and one by a nonbreeding male, suggesting that males may augment their reproductive success through extra-group paternity.     

Nest helpers improve parental survival but not offspring production in a high‐elevation passerine,the Ground Tit Pseudopodoces humilis

The way in which breeders respond to helping, in terms of either offspring production or their own survival, may reflect the adaptive aspects of a cooperative breeding system. We explore this issue using a 5‐year study of the Ground Tit Pseudopodoces humilis, a facultative cooperative breeder in which 47% of socially monogamous pairs have between one and four close male relatives as helpers. We found that helped nests did not fledge more or heavier nestlings than unhelped nests, and male young from helped and unhelped nests were equally likely to recruit into the local breeding population. However, helped parents of both sexes had a higher probability of survival to the following year than did unhelped parents. These findings suggest that Ground Tit parents with helpers trade current reproduction for personal survival and future reproduction, a strategy favoured by selection to cope with harsh, unpredictable environments such as the Tibetan Plateau.     

Environmental mismatch results in emergence of cooperative behavior in a passerine bird

A major problem in the evolution of maternal effects is explaining the origin and persistence of maternally induced phenotypes that lower offspring fitness. Recent work focuses on the relative importance of maternal and offspring selective environments and the mismatch between them. However, an alternative approach is to directly study the origin and performance of offspring phenotypes resulting from mismatch. Here, we capitalize on a detailed understanding of the ecological contexts that provide both the cue and the functional context for expression of maternally induced offspring phenotypes to investigate the consequences of environmental mismatch. In western bluebirds, adaptive integration of offspring dispersal and aggression is induced by maternal competition over nest cavities. When nest cavities are locally abundant, mothers produce nonaggressive offspring that remain in their natal population, and when nest cavities are scarce, mothers produce aggressive dispersers. However, a few offspring neither disperse nor breed locally, instead helping at their parent’s nest, and as a result these offspring have unusually low fitness. Here, we investigate whether females produce helpers to increase their own fitness, or whether helpers result from a mismatch between the cues mothers experience during offspring production and the breeding environment that helpers later encounter. We found that producing helpers does not enhance maternal fitness. Instead, we show that helpers, which were the least aggressive of all returning sons in the population, were most common when population density increased from the time sons were produced to the time of their reproductive maturity, suggesting that the helper phenotype emerges when cues of resource competition during offspring development do not match the actual level of competition that offspring experience. Thus, environmental mismatch might explain the puzzling persistence of maternally induced phenotypes that decrease offspring fitness.     

Hormonal correlates of development and natal dispersal in wild female owl monkeys (Aotus azarae) of Argentina

Pair-living and socially monogamous primates typically do not reproduce before dispersing. It is currently unclear whether this reproductive suppression is due to endocrine or behavioral mechanisms. Cooperatively breeding taxa, like callitrichids, may forego reproduction in natal groups because they reap inclusive fitness benefits and/or they are avoiding inbreeding. However, neither of these benefits of delayed reproduction appear to adequately explain the lack of reproduction prior to leaving the natal group in pair-living monogamous species. In this study, we determined whether wild Azara's owl monkeys (Aotus azarae) in the Argentinean Chaco establish reproductive maturity prior to dispersing. We utilized 635 fecal extracts to characterize reproductive hormone profiles of 11 wild juvenile and subadult females using enzyme immunoassays. Subadult females showed hormone profiles indicative of ovulatory cycling and had mean PdG and E1G concentrations approximately five times higher than juveniles. Contrary to expectations from the inbreeding avoidance hypothesis, female owl monkeys do not delay puberty, but rather commence ovarian cycling while residing in their natal group. Still, subadults appear to have a period during which they experience irregular, non-conceptive cycles prior to reproducing. Commencing these irregular cycles in the natal group may allow them to develop a state of suspended readiness, which could be essential to securing a mate, while avoiding costs of ranging solitarily. Our results indicate that reproductive suppression in female owl monkeys is not due to endocrine suppression. We suggest that adults likely use behavioral mechanisms to prevent subadults from reproducing with unrelated adult males in their natal group.     

Family-based winter territoriality in western bluebirds, Sialia mexicana: the structure and dynamics of winter groups

Winter residency is characteristic of the majority of cooperatively breeding birds, but the composition and dynamics of winter groups have been examined in relatively few. In 1996-1998, we examined winter territoriality in the western bluebird, a year-round resident that shows a limited degree of helping behaviour in central coastal California, U.S.A. In spring, most western bluebirds breed as socially monogamous pairs, but a small proportion of pairs (3-16%) have additional breeding-age males helping at the nest, usually assisting parents or brothers. We found that year-round residents commonly wintered in family groups that defended territories similar to those used in spring. Winter groups had an even sex ratio and formed early in the autumn, when hatch-year birds dispersed. More females than males left their natal groups to be replaced by an influx of immigrant hatch-year birds. Winter groups typically consisted of breeders and one or two sons from the prior breeding season along with one or more immigrant females. A second period of dispersal occurred in spring when winter groups broke up and most birds other than the breeding pair left the winter territory. When they bred, yearling males and females often bred with unrelated individuals from their winter groups. Sons were more likely to remain on the study area as yearlings when they wintered with both parents than when they wintered with just one parent. We suggest that young males stay the winter due to benefits of remaining in family groups on mistletoe-based winter territories. Subsequent localized dispersal of sons then leads to opportunistic kin-based interactions later in life. Copyright 2001 The Association for the Study of Animal Behaviour.     

Reproductive success and helper effects in the cooperatively breeding grey-crowned babbler

Cooperative breeding, where some individuals help to raise offspring that are not their own, is a relatively rare social system in birds. We studied the breeding biology of a declining cooperative breeder, the grey-crowned babbler Pomatostomus temporalis , with the aim of isolating the social factors that affect its reproductive success. Most breeding pairs were assisted by philopatric offspring, although pairs could breed successfully without helpers. Females laid up to four clutches (usually three eggs per clutch) per season. Male (but not female) helpers increased the number of young fledged from individual nests and the likelihood of re-nesting, resulting in higher seasonal fledgling production. Helper effects on brood size and fledgling production were greater in the second year of the study, which was also characterized by higher nest failure. This suggests that helpers enhance reproduction more in poor conditions. Our study demonstrates the interacting effects of social and ecological factors on reproductive success, and that retention of offspring is not always beneficial for the breeders in cooperative species.     

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.     

Reproductive biology of captive male cottontop tamarin monkeys as a function of social environment

The cottontop tamarin, Saguinus oedipus oedipus, is a cooperatively breeding monkey in which mature male and female offspring serve as helpers to assist in rearing younger siblings. Generally, only one female per social group reproduces; breeding restriction is mediated in postpubertal female offspring through low and acyclic levels of reproductive hormones. We investigated (1) reproductive activity of postpubertal male offspring, and (2) whether aggression towards male offspring and a cortisol-mediated stress response might restrict breeding of male offspring in the natal group. We examined sexual behaviour, olfactory communication and urinary hormone levels (testosterone, dihydrotestosterone, luteinizing hormone, cortisol) of the subject males while we manipulated their social environment from housing in natal groups to pairing with a novel female, and after the production of their own offspring. Mounting and erection rates of the male subjects were as high in the natal group as when paired with a novel female. However, most mounts in the natal group were directed towards other males, and complete copulation sequences did not occur with natal-group females. Social environment had no significant effect on olfactory investigation of breeding females. Although hormone levels increased significantly after the subjects were removed from the natal group, the elevation was transient; the hormone levels of subjects in their natal groups did not differ from the levels shown by the same males when successfully producing their own offspring. Male offspring received more contact aggression in the natal group than when paired with the novel female. However, most of the aggression was received from siblings rather than the breeding pair, and levels of cortisol did not correspond with levels of aggression. Thus, at both a behavioural and endocrine level, mature male offspring in captive natal groups were potentially fertile, but sexual activity with natal-group females appeared to be behaviourally restricted and directed instead towards group males. In wild cottontop tamarin groups, this reproductive potential may allow male helpers flexibility to respond to breeding opportunities. Copyright 2001 The Association for the Study of Animal Behaviour.