Direct benefits and the evolution of female-biased cooperative breeding in Seychelles warblers

Abstract.— Inclusive fitness benefits have been suggested to be a major selective force behind the evolution of cooperative breeding. We investigated the fitness benefits selecting for cooperative breeding in the Seychelles warbler, Acrocephalus sechellensis . A microsatellite-based genotyping method was used to determine the relatedness of subordinates to group offspring in an isolated population of Seychelles warblers. The indirect and direct breeding benefits accruing to individual subordinates were then calculated for every successful breeding event over a three-year period. We show that female subordinates frequently gained parentage and that this, combined with high levels of extra group paternity, resulted in low levels of relatedness between subordinates and non descendent offspring within a territory. Direct breeding benefits were found to be significantly higher than indirect kin benefits for both female and male subordinates. As predicted, female subordinates gained significantly more direct breeding opportunities and therefore higher inclusive fitness benefits by being a subordinate within a group than did males. This may explain why most subordinates in the Seychelles warbler are female.     

Sex-specific associative learning cues and inclusive fitness benefits in the Seychelles warbler

In cooperative breeding vertebrates, indirect fitness benefits would be maximized by subordinates that accurately assess their relatedness to group offspring and preferentially help more closely related kin. In the Seychelles warbler (Acrocephalus sechellensis), we found a positive relationship between subordinate-nestling kinship (determined using microsatellite marker genotypes) and provisioning rates, but only for female subordinates. Female subordinates that helped were significantly more related to the nestlings than were nonhelpers, and the decision to help appears to be based on associative learning cues. High levels of female infidelity means that subordinates cannot trust their legitimacy through the male line, consequently they appear to use the continued presence of the primary female, but not the primary male, as a reliable cue to determine when to feed nestlings. By using effective discrimination, female subordinates are able to maximize the indirect benefits gained within a cooperative breeding system otherwise driven primarily by direct breeding benefits.     

Sex ratios when helpers stay at the nest

This study investigates the evolution of the sex ratio (parental investment in sons) when breeding adults are supported by help provided by nonbreeding individuals of one sex. The study also assumes that the helping sex remains on its natal site to compete for the opportunity to breed, whereas the nonhelping sex disperses. Two kin-selection models are presented, both of which incorporate the age structure found in many natural populations where such helping occurs. The first model assumes that helpers increase the survival of their parents. The second model assumes that helpers are indiscriminant: a helper chooses to increase the survival of a random pair of adults breeding on its natal patch. In both models, sex ratios are not always biased toward the sex that provides the most help. When helpers do not discriminate (second model), the direction of sex-ratio bias is determined solely by the size of the benefit of helping behavior. When this benefit is small, sex-ratio evolution is primarily influenced by local resource competition and sex ratios are biased toward the nonhelping (dispersive) sex. If the benefit of help is large enough, the effect of local resource competition is reduced and sex-ratio bias favors the helpful sex. When helpers help only their parents, the same qualitative relationship exists between the direction of sex-ratio bias and the benefit of helping. In this case, however, the direction of sex-ratio bias is also influenced by the size of the social group, mortality, and which individual (mother or father) controls the sex ratio. This study also investigates a sex-ratio conflict that exists between mates. Helping behavior of nonbreeders can act to alleviate the disparities between the optimal sex ratio from the perspective of a mother and that from the perspective of a father. This consequence of helping has not been previously recognized.     

Parent presence, delayed dispersal, and territory acquisition in the Seychelles warbler

The presence of parents in the natal territory may play an important,but often overlooked, role in natal dispersal and the consequentacquisition of a territory. Living with parents in a territorymay confer a fitness advantage to subordinates through, forexample, the nepotistic behavior of the parents or indirectbenefits gained by helping to raise nondescendent kin. Whena parent is replaced by a stepparent, such advantages are reducedor disappear and, as a result, subordinates may disperse. Subordinatesthat disperse after parent replacement may be constrained intheir timing of dispersal, which could have negative fitnessconsequences. In the cooperatively breeding Seychelles warbler,we show that when a parent was naturally replaced or experimentallyremoved and subsequently replaced by a stepparent from outsidethe territory, subordinates were more likely to disperse thanwhen both parents remained in the natal territory. Furthermore,subordinates dispersing from territories in which one or bothparents had been replaced were less likely to acquire a breederposition than subordinates dispersing when both parents werestill on the natal territory. Our findings suggest that thepresence of parents in the natal territory may promote delayeddispersal and facilitate the eventual acquisition of a breederposition outside the natal territory. Our results support theidea that the prolonged parental care, which long-lived speciesare able to provide, may have selected for family living.     

Parentage assignment and extra-group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus sechellensis)

We describe the development and initial application of a semiautomated parentage testing system in the Seychelles warbler (Acrocephalus sechellensis). This system used fluorescently labelled primers for 14 polymorphic microsatellite loci in two multiplex loading groups to genotype efficiently over 96% of the warbler population on Cousin island. When used in conjunction with the program CERVUS, this system provided sufficient power to assign maternity and paternity within the Seychelles warbler, despite the complications associated with its cooperative breeding system and a relatively low level of genetic variation. Parentage analyses showed that subordinate 'helper' females as well as the dominant 'primary' females laid eggs in communal nests, indicating that the Seychelles warbler has an intermediate level of female reproductive skew, in between the alternative extremes of helper-at-the-nest and joint nesting systems. Forty-four per cent of helpers bred successfully, accounting for 15% of all offspring. Forty per cent of young resulted from extra-group paternity.     

The significance of multiple mating in the social wasp Vespula maculifrons

The evolution of the complex societies displayed by social insects depended partly on high relatedness among interacting group members. Therefore, behaviors that depress group relatedness, such as multiple mating by reproductive females (polyandry), are unexpected in social insects. Nevertheless, the queens of several social insect species mate multiply, suggesting that polyandry provides some benefits that counteract the costs. However, few studies have obtained evidence for links between rates of polyandry and fitness in naturally occurring social insect populations. We investigated if polyandry was beneficial in the social wasp Vespula maculifrons. We used genetic markers to estimate queen mate number in V. maculifrons colonies and assessed colony fitness by counting the number of cells that colonies produced. Our results indicated that queen mate number was directly, strongly, and significantly correlated with the number of queen cells produced by colonies. Because V. maculifrons queens are necessarily reared in queen cells, our results demonstrate that high levels of polyandry are associated with colonies capable of producing many new queens. These data are consistent with the explanation that polyandry is adaptive in V. maculifrons because it provides a fitness advantage to queens. Our research may provide a rare example of an association between polyandry and fitness in a natural social insect population and help explain why queens in this taxon mate multiply.     

Pup escorting in the communal breeding banded mongoose: behavior, benefits, and maintenance

In cooperatively breeding species, helpers typically providefood to offspring, and distribute food throughout the broodor litter. However, in the communal breeding banded mongoose(Mungos mungo), some group members escort individual pups duringtheir period of dependence, and escorts consistently associatewith the same pup, although not all pups have an escort. Theaim of the present study was to determine whether group membersactively care for pups, pups benefit from association, and escortsor pups maintain association. Adult banded mongooses provision,protect, carry, groom, and play with pups. Although escortsfed pups more than did nonescorts, escorted pups were neitherlarger nor in better condition than were nonescorted pups atthe end of the association period. Nevertheless, escorted pupswere more likely to survive the association period than werenonescorted pups, providing evidence that carers confer beneficialeffects on their recipients. However, the recipients are unlikelyto be the genetic offspring of the escort because it is thepup that maintains the pup-escort association, and escorts,rather than showing a preference for provisioning their pairedpup, follow a "feed the closest pup" rule. Although carers gainindirect fitness benefits through increasing survival of relatedpups, the lack of kin discrimination means carers are unableto maximize their fitness by preferentially escorting theirown offspring or the offspring of closer relatives.     

The fitness consequences of kin-biased dispersal in a cooperatively breeding bird

Cooperative alliances among kin may not only lead to indirect fitness benefits for group-living species, but can also provide direct benefits through access to mates or higher social rank. However, the immigrant sex in most species loses any potential benefits of living with kin unless immigrants disperse together or recruit relatives into the group in subsequent years. To look for evidence of small subgroups of related immigrants within social groups (kin substructure), we used microsatellites to assess relatedness between immigrant females of the cooperatively breeding superb starling, Lamprotornis superbus. We determined how timing of immigration led to kin subgroup formation and if being part of one influenced female fitness. Although mean relatedness in groups was higher for males than females, 26% of immigrant females were part of a kin subgroup with a sister. These immigrant sibships formed through kin recruitment across years more often than through coalitions immigrating together in the same year. Furthermore, females were more likely to breed when part of a kin subgroup than when alone, suggesting that female siblings form alliances that may positively influence their fitness. Ultimately, kin substructure should be considered when determining the role of relatedness in the evolution of animal societies.     

Mother's little helpers: What we know (and don't know) about cooperative infant care in callitrichines

Since Darwin ( 1859 ), scientists have been puzzled by how behaviors that impose fitness costs on helpers while benefiting their competitors could evolve through natural selection. Hamilton's ( 1964 ) theory of inclusive fitness provided an explanation by showing how cooperative behaviors could be adaptive if directed at closely related kin. Recent studies, however, have begun to question whether kin selection is sufficient to explain cooperative behavior in some species (Bergmüller, Johnstone, Russell, & Bshary, 2007 ). Many researchers have instead emphasized the importance of direct fitness benefits for helpers in the evolution of cooperative breeding systems. Furthermore, individuals can vary in who, when, and how much they help, and the factors that affect this variation are poorly understood (Cockburn, 1998 ; Heinsohn, 2004 ). Cooperative breeders thus provide excellent models for the study of evolutionary theories of cooperation and conflict (Cant, 2012 ).     

The adaptive dynamics of altruism in spatially heterogeneous populations

Abstract.— We study the spatial adaptive dynamics of a continuous trait that measures individual investment in altruism. Our study is based on an ecological model of a spatially heterogeneous population from which we derive an appropriate measure of fitness. The analysis of this fitness measure uncovers three different selective processes controlling the evolution of altruism: the direct physiological cost, the indirect genetic benefits of cooperative interactions, and the indirect genetic costs of competition for space. In our model, habitat structure and a continuous life cycle makes the cost of competing for space with relatives negligible. Our study yields a classification of adaptive patterns of altruism according to the shape of the costs of altruism (with decelerating, linear, or accelerating dependence on the investment in altruism). The invasion of altruism occurs readily in species with accelerating costs, but large mutations are critical for altruism to evolve in selfish species with decelerating costs. Strict selfishness is maintained by natural selection only under very restricted conditions. In species with rapidly accelerating costs, adaptation leads to an evolutionarily stable rate of investment in altruism that decreases smoothly with the level of mobility. A rather different adaptive pattern emerges in species with slowly accelerating costs: high altruism evolves at low mobility, whereas a quasi-selfish state is promoted in more mobile species. The high adaptive level of altruism can be predicted solely from habitat connectedness and physiological parameters that characterize the pattern of cost. We also show that environmental changes that cause increased mobility in those highly altruistic species can beget selection-driven self-extinction, which may contribute to the rarity of social species.     

Influence of age on reproductive performance in the Seychelles warbler

I studied age-related breeding performance of the cooperativelybreeding Seychelles warbler (Acrocephalus sechellensis) on CousinIsland, Seychelles, during 14 years. The annual number of youngthat fledged is significantly related to territory quality andnumber of helpers in the breeding group. Accounting for thesefactors and for the partner's breeding experience, annual productionof fledglings by breeding birds increases from 2 to 5 yearsand decreases beyond 5 years of age. Age-related changes inreproductive success within breeding individuals, paired withthe same experienced partner and occupying the same breedingterritory with similar amount of food from 2 to 8 years of age,show that Seychelles warblers have higher hatching success andproduce more hatchlings and fledglings as they become older.This is probably not a response to decreasing residual reproductivevalue caused by decreasing life expectancy as they become older.Primiparous warblers produce the same number of fledglings asmultiparous warblers of the same age, have a similar life expectancyas multiparous warblers, and occupy territories with similaramounts of resources available for reproduction. As all warblershave similar access to food before reproduction and similarforaging efficiency, the low reproductive success in youngerwarblers cannot be ascribed to differences in environment butto the bird's ability to breed successfully (e.g., a resultof previous helping and/or breeding experience). Effects ofsenescence on reproduction begin to occur from age 6 for bothsexes. From that age, eggs have lower hatching success, butfledging success remains the same. Birds that start breedingat a young age on a given quality territory produce more fledglingsin their lifetime than birds that delay breeding. Many old birdsnever fledge young of their own. They have not been able tobreed because of a shortage of breeding territory vacancies.[BehavEcol 7: 417–425 (1996)]     

Queen–worker conflict over male production and the sex ratio in a facultatively polyandrous bumblebee, Bombus hypnorum: the consequences of nest usurpation

Evolutionary conflicts among social hymenopteran nestmates are theoretically likely to arise over the production of males and the sex ratio. Analysis of these conflicts has become an important focus of research into the role of kin selection in shaping social traits of hymenopteran colonies. We employ microsatellite analysis of nestmates of one social hymenopteran, the primitively eusocial and monogynous bumblebee Bombus hypnorum, to evaluate these conflicts. In our 14 study colonies, B. hypnorum queens mated between one and six times (arithmetic mean 2.5). One male generally predominated, fathering most of the offspring, thus the effective number of matings was substantially lower (1-3.13; harmonic mean 1.26). In addition, microsatellite analysis allowed the detection of alien workers, those who could not have been the offspring of the queen, in approximately half the colonies. Alien workers within the same colony were probably sisters. Polyandry and alien workers resulted in high variation among colonies in their sociogenetic organization. Genetic data were consistent with the view that all males (n = 233 examined) were produced by a colony's queen. Male parentage was therefore independent of the sociogenetic organization of the colony, suggesting that the queen, and not the workers, was in control of the laying of male-destined eggs. The population-wide sex ratio (fresh weight investment ratio) was weakly female biased. No evidence for colony-level adaptive sex ratio biasing could be detected.     

Care for kin: within-group relatedness and allomaternal care are positively correlated and conserved throughout the mammalian phylogeny

With an increasing amount of data becoming available, comparative analyses have called attention to the associations between cooperative breeding, monogamy and relatedness. We focus here upon the association between allomaternal care and relatedness among females within a social unit. Previous studies found a positive association, but such results date back to before molecular tools were in common use, they considered only a few mammalian orders, neglected phylogenetic clustering and/or did not correct for group sizes. Here, we use molecular data on relatedness from 44 species of mammals to investigate the phylogenetic clustering of, and the association between, allomaternal care and relatedness among females within a social unit. We find (i) a strong phylogenetic signal for allomaternal care and a moderate one for relatedness and group size, and (ii) a positive association between relatedness and allomaternal care, even when correcting for the smaller than average group sizes in species with allomaternal care. We also find that, in species without allomaternal care, adult females often live with unrelated females even when groups are small. We discuss these results in the light of recent evidence for the role of kin selection and the monogamy hypothesis in cooperative breeding.     

Inclusive fitness of 'kissing cousins': new evidence of a role for kin selection in the evolution of extra-pair mating in birds

Social monogamy is nearly ubiquitous across avian taxa,but evidence from a proliferation of studies utilizing molecular paternity analysis suggests that sexual monogamy is the rare exception rather than the rule (Griffith et al. 2002). Efforts to explain the prevalence of extra-pair paternity (EPP) have largely focused on the potential fitness benefits for offspring genetic quality, as females are less likely to benefit directly from seeking extra-pair mates. In particular, there has been considerable interest in the degree to which EPP may represent an adaptive female strategy to avoid inbreeding (or outbreeding)depression when paired with a highly related (or unrelated)social mate (Kempenaers 2007). Others have argued that, because relatives share many genes identical by descent,females might increase their own inclusive fitness by providing additional breeding opportunities to genetically related males (Waser et al. 1986; Kokko & Ots 2006). Thus, in the absence of significant inbreeding depression, pursuing EPP with relatives should be favoured by kin selection, although there exist few unambiguous empirical examples of such preferences in the literature. In this issue of Molecular Ecology, Wang &Lu (2011) present an analysis of mating patterns with respect to genetic relatedness of social and extra-pair partners in the ground tit (Parus humilis), a facultative cooperative breeder in which socially monogamous pairs occasionally form cooperative groups with unpaired helper males (Fig. 1). Consistent with the predictions of the kin-selection hypothesis, females in both bi-parental and cooperative groups preferentially engaged in extra-pair matings with relatives, irrespective of relatedness to their social mates, and while suffering no apparent costs of inbreeding depression in their progeny. These finding shave several exciting implications for our understanding of avian mating system diversity and the evolution of cooperative breeding.     

MHC diversity in two Acrocephalus species: the outbred Great reed warbler and the inbred Seychelles warbler

The Great reed warbler (GRW) and the Seychelles warbler (SW) are congeners with markedly different demographic histories. The GRW is a normal outbred bird species while the SW population remains isolated and inbred after undergoing a severe population bottleneck. We examined variation at Major Histocompatibility Complex (MHC) class I exon 3 using restriction fragment length polymorphism, denaturing gradient gel electrophoresis and DNA sequencing. Although genetic variation was higher in the GRW, considerable variation has been maintained in the SW. The ten exon 3 sequences found in the SW were as diverged from each other as were a random sub-sample of the 67 sequences from the GRW. There was evidence for balancing selection in both species, and the phylogenetic analysis showing that the exon 3 sequences did not separate according to species, was consistent with transspecies evolution of the MHC.     

Positive effects of helpers on reproductive success in the brown treecreeper and the general importance of future benefits

1. Numerous studies of cooperatively breeding species have tested for effects of helpers on reproductive success to evaluate hypotheses for the evolution of cooperation, but relatively few have used experimental or statistical approaches that control for the confounding effects of breeder and territory quality. 2. In the brown treecreeper Climacteris picumnus, most helpers are male offspring of the breeding pair that have delayed dispersal. We analysed 5 years of data (97 territory-years) using hierarchical linear modelling to test for effects of helpers on reproductive success while controlling for confounding factors. 3. The number of helpers was related positively to reproductive success even after controlling for differences between territories and breeders. A threshold effect was observed, with success increasing most with the presence of a second helper (i.e. at group size of four). 4. Feeding at the nest was one mechanism responsible for this effect, as larger groups had higher total feeding rates at all nesting stages. Higher total feeding rates, as well as higher feeding rates by helpers, were correlated in turn with greater reproductive success. 5. An analysis of the effects of helper feeding rate on reproductive success in groups with just one helper produced only weak support for a positive effect of helpers. Controlled comparisons of this kind utilize only a small fraction of the total data available and thus have limited statistical power compared to hierarchical or mixed-modelling. 6. A number of hypotheses to explain the evolution and maintenance of helping behaviour are consistent with our results for brown treecreepers including kin selection and hypotheses based on future direct benefits. 7. A previous synthesis of studies of helper effects that controlled for confounding factors suggested a pattern in which male helpers rarely have positive effects on reproductive success. However, revising that synthesis to include recent hierarchical or mixed-modelling studies suggests that helpers of both sexes usually have positive effects, and that the relative importance of future direct benefits may have been underestimated.