Causes and consequences of incest avoidance in the cooperatively breeding mole-rat, Cryptomys darlingi (Bathyergidae)

A number of social mole-rat species maintain a strong reproductive skew (only one breeding pair in the group) solely through incest avoidance. Incest avoidance probably evolved for one of two reasons, namely for actually maintaining a reproductive skew or, alternatively, to avoid high inbreeding depression. In the latter case a strong reproductive skew would result as a fortuitous by-product of the combination of a cloistral family life style of mole-rats and incest avoidance. We undertook breeding experiments in which the fertility of pairs of unrelated individuals were compared with that of pairs of double first cousins. Inbreeding depression was remarkably high and an accompanying model suggests that it may be sufficient to support the idea that strong incest avoidance evolved primarily to eliminate the costs of inbreeding and subsequently facilitated the evolution of reproductive skew.     

Reproductive suppression in female cooperatively breeding cichlids

Suppression by dominants of female subordinate reproduction has been found in many vertebrate social groups, but has rarely been shown experimentally. Here experimental evidence is provided for reproductive suppression in the group-living Lake Tanganyika cichlid Neolamprologus pulcher. Within groups of three unrelated females, suppression was due to medium- and small-sized females laying less frequently compared with large females, and compared with medium females in control pairs. Clutch size and average egg mass of all females depended on body size, but not on rank. In a second step, a large female was removed from the group and a very small female was added to keep the group size constant. The medium females immediately seized the dominant breeding position in the group and started to reproduce as frequently as control pairs, whereas clutch size and egg mass did not change. These results show that female subordinate cichlids are reproductively capable, but apparently suppressed with respect to egg laying. Nevertheless, some reproduction is tolerated, possibly to ensure continued alloparental care by subordinate females.     

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.     

Experimental evaluation of sex differences in territory acquisition in a cooperatively breeding bird

In many species, territory ownership is a prerequisite for reproduction;consequently, factors that affect success in territory acquisitioncan have a large impact on fitness. When competing for territories,some individuals may have an advantage if, for example, theyare phenotypically superior or more familiar with the site thanothers. The relative importance of the many factors involvedin territory acquisition is, at present, unclear. We studiedpatterns of natural territory acquisition in a closed and saturatedpopulation of Seychelles warblers. Furthermore, by removingbreeders, we experimentally investigated the relative importance,to territory acquisition, of a range of factors and assessedwhether this differed between the sexes. In both sexes, themain route to natural territory acquisition was to dispersefrom the natal territory to immediately claim a vacant dominantposition. Males were older than females when acquiring a territoryfor the first time. In the removal experiment, for both sexes,the proximity of an individual's natal territory to a vacantdominant position was positively related to the individual'schance of claiming the vacancy. Older males were more likelyto gain an experimental vacant dominant position than were youngmales, whereas age did not affect territory acquisition in females.In the Seychelles warbler, the degree of intrasexual competitionfor territory ownership may be stronger for males than for femalesbecause territory ownership is a prerequisite for male reproduction,whereas females can reproduce on their natal territory. In suchcompetition, young males subsequently lose out to older ones.     

Reproductive parasitism of broodcare helpers in a cooperatively breeding fish

Large male helpers in the cooperatively breeding cichlid Neolamprologuspulchergain reproductive success by parasitizing the reproductive effortofmale territory owners. Under controlled, experimental conditionsweexamined the genetic relatedness between the members of broodpairs(n = 14), their male helpers (n = 8), and offspring(n= 292) in seven families. We used multilocus DNA fingerprintingtocheck for potential reproductive parasitism by male helpersand to assesstheir fertilization success. Of offspring producedin these families, 10.3%were sired by helpers. In parasitizedbroods, helper fertilization successvaried between 12.5% and35.8%. Male helpers parasitized parental reproductionwhen theirbody size exceeded 4.5 cm standard length (SL), even thoughsexualmaturity may be reached much earlier (3.5 cm SL). Twoof three parasitichelpers were punished by severe aggressiveattacks when parasitizing thereproduction of breeders, whichled to their expulsion from the territory.This study demonstratesa potential fitness benefit to broodcare helpers thatis oftenneglected. It also points to the delicate balance that may existbetweencooperative and competitive behavior in cooperatively breedingspecies.     

Reproductive senescence in a cooperatively breeding mammal

1. Senescence (or 'ageing') is a widespread and important process in wild animal populations, but variation in ageing patterns within and between species is poorly understood.
2. In cooperatively breeding species, the costs of reproduction are shared between breeders and one or more helpers. The effects of ageing in breeders may therefore be moderated by the presence of helpers, but there have been very few studies of senescence patterns in natural populations of cooperative breeders.
3. Here, we use 13 years of data from a long-term study population of wild meerkats ( Suricata suricatta ) to investigate age-related changes in several traits known to be key components of reproductive success in females of this species.
4. Four of the six traits studied exhibited significant declines with age, indicating senescence. Litter size, the number of litters produced per year and the number of pups that survived to emergence from the natal burrow per year all increased with female age up to a peak at c. 4 years, and declined steeply thereafter; the mean pup weight at emergence in a given litter declined steadily from age zero.
5. These results provide the first evidence of reproductive senescence in a wild population of a cooperatively breeding vertebrate. Breeding success declined with age despite the sharing of reproductive costs in this species, but further study is needed to investigate whether helping affects other aspects of senescence, including survival.     

Experimental evidence for helper effects in a cooperatively breeding cichlid

Neolamprologus pulcher is a cooperatively breeding cichlid fish,in which helpers stay in their natal territory and help withbrood care, territory defense, and maintenance. In this studywe investigated helper effects by an experimental group sizereduction in the field. After this manipulation, focal helpersin reduced groups tended to feed less, and small helpers visitedthe breeding shelter significantly more often than same-sizedhelpers in control groups. No evidence was found that remaininghelpers compensated for the removed helpers by increasing territorydefense and maintenance behavior. Breeders, however, did showa lower defense rate, possibly caused by an increase in broodcare effort. Survival of fry was significantly lower in removalthan control groups, which provides the first experimental proofin a natural population of fish that brood care helpers do effectivelyhelp. The data suggest that in small, generally younger, helpers,kin selection may be an important evolutionary cause of cooperation.Large helpers, however, who are generally older and less relatedto the breeders than small helpers are suggested to pay to beallowed to stay in the territory by helping. All group membersbenefit from group augmentation.     

A comparative analysis of some life-history traits between cooperatively and non-cooperatively breeding Australian passerines

Summary Comparative analyses were carried out for some life-history traits of cooperatively and non-cooperatively breeding Australian Corvida (i.e. old-endemic passerines). Multivariate statistical analyses at the family and genus levels revealed no significant differences between cooperative and non-cooperative breeders. A matched-pairs analysis between congeneric species showed that cooperatively breeding species lay smaller clutches than non-cooperatively breeding congenerics. Preliminary results also suggest that cooperative breeders have higher probabilities of rearing a second brood in the season and lower probabilities of survival than do non-cooperative breeders. However, the result for survival was significant in only one out of three tests. We conclude that cooperatively and non-cooperatively breeding Australian Corvida cannot be separated into distinct groups showingK- andr-selected life-history traits, respectively. Some life-history traits follow the prediction of ther-K selection model, others show evidence of co-adaptation instead, whereas still others show evidence of trade-offs.     

Demography of male reproductive queues in cooperatively breeding superb fairy-wrens Malurus cyaneus

1. Subordinate helpers in cooperative societies may gain both immediate and future benefits, including paternity and territorial inheritance. However, if such opportunities correlate with rank in the queue, it is unclear why such queues should be stable. 2. In cooperatively breeding superb fairy-wrens Malurus cyaneus, only males are generally philopatric, and form stable hierarchical queues for the dominant position. 3. Male opportunities for reproduction are influenced both by their dominance status within the group, and their relatedness to the breeding female. For young queuing subordinates, the breeding female is typically their mother. Because of incest avoidance, reproduction is possible only through extra-group mating, even if the dominant position is achieved while the mother is still on the territory. If the mother dies while the helper is still a subordinate, he can seek matings both outside the group, and with the unrelated replacement female within the group. Finally, males can achieve the dominant position and pair with an unrelated female by inheritance, dispersal to a neighbouring vacancy, or by forming a liaison with an immigrant subordinate female that causes fission of the natal territory. 4. On average males spent more time living with unrelated females than with their mother. Subordinate males gained no survival advantages when living with their mother rather than an unrelated female, contrary to the prediction that parents facilitate the survival of their offspring. 5. Dominants and subordinates also had similar survival. Mortality accelerated over time, probably because older males invest more in extra-group courtship display. 6. Fairy-wren queues are likely to be stable because older birds are superior, and because extra-pair mating provides direct benefits to subordinates.     

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.     

Brood sex ratio variation in a cooperatively breeding bird

In cooperatively breeding species, the fitness consequences of producing sons or daughters depend upon the fitness impacts of positive (repayment hypothesis) and negative (local competition hypothesis) social interactions among relatives. In this study, we examine brood sex allocation in relation to the predictions of both the repayment and the local competition hypotheses in the cooperatively breeding long-tailed tit Aegithalos caudatus. At the population level, we found that annual brood sex ratio was negatively related to the number of male survivors across years, as predicted by the local competition hypothesis. At an individual level, in contrast to predictions of the repayment hypothesis, there was no evidence for facultative control of brood sex ratio. However, immigrant females produced a greater proportion of sons than resident females, a result consistent with both hypotheses. We conclude that female long-tailed tits make adaptive decisions about brood sex allocation.     

Higher reproductive skew among birds than mammals in cooperatively breeding species

While competition for limited breeding positions is a common feature of group life, species vary widely in the extent to which reproduction is shared among females (‘reproductive skew’). In recent years, there has been considerable debate over the mechanisms that generate variation in reproductive skew, with most evidence suggesting that subordinates breed when dominants are unable to prevent them from doing so. Here, we suggest that viviparity reduces the ability of dominant females to control subordinate reproduction and that, as a result, dominant female birds are more able than their mammal counterparts to prevent subordinates from breeding. Empirical data support this assertion. This perspective may increase our understanding of how cooperative groups form and are stabilized in nature.     

Restricted mating dispersal and strong breeding group structure in a mid-sized marsupial mammal (Petrogale penicillata)

Ecological genetic studies have demonstrated that spatial patterns of mating dispersal, the dispersal of gametes through mating behaviour, can facilitate inbreeding avoidance and strongly influence the structure of populations, particularly in highly philopatric species. Elements of breeding group dynamics, such as strong structuring and sex-biased dispersal among groups, can also minimize inbreeding and positively influence levels of genetic diversity within populations. Rock-wallabies are highly philopatric mid-sized mammals whose strong dependence on rocky terrain has resulted in series of discreet, small colonies in the landscape. Populations show no signs of inbreeding and maintain high levels of genetic diversity despite strong patterns of limited gene flow within and among colonies. We used this species to investigate the importance of mating dispersal and breeding group structure to inbreeding avoidance within a 'small' population. We examined the spatial patterns of mating dispersal, the extent of kinship within breeding groups, and the degree of relatedness among brush-tailed rock-wallaby breeding pairs within a colony in southeast Queensland. Parentage data revealed remarkably restricted mating dispersal and strong breeding group structuring for a mid-sized mammal. Breeding groups showed significant levels of female kinship with evidence of male dispersal among groups. We found no evidence for inbreeding avoidance through mate choice; however, anecdotal data suggest the importance of life history traits to inbreeding avoidance between first-degree relatives. We suggest that the restricted pattern of mating dispersal and strong breeding group structuring facilitates inbreeding avoidance within colonies. These results provide insight into the population structure and maintenance of genetic diversity within colonies of the threatened brush-tailed rock-wallaby.     

Mothers adjust egg size to helper number in a cooperatively breeding cichlid

Mothers should adjust the size of propagules to the selectiveforces to which these offspring will be exposed. Usually, alarger propagule size is favored when young are exposed to highmortality risk or conspecific competition. Here we test 2 predictionson how egg size should vary with these selective agents. Whenoffspring are cared for by parents and/or alloparents, protectionmay reduce the predation risk to young, which may allow mothersto invest less per single offspring. In the cooperatively breedingcichlid Neolamprologus pulcher, brood care helpers protect groupoffspring and reduce the latters' mortality rate. Therefore,females are expected to reduce their investment per egg whenmore helpers are present. In a first experiment, we tested thisprediction by manipulating the helper number. In N. pulcher,helpers compete for dispersal opportunities with similar-sizedindividuals of neighboring groups. If the expected future competitionpressure on young is high, females should increase their investmentper offspring to give them a head start. In a second experiment,we tested whether females produce larger eggs when perceivedneighbor density is high. Females indeed reduced egg size withincreasing helper number. However, we did not detect an effectof local density on egg size, although females took longer toproduce the next clutch when local density was high. We arguethat females can use the energy saved by adjusting egg sizeto reduced predation risk to enhance future reproductive output.Adaptive adjustment of offspring size to helper number may bean important, as yet unrecognized, strategy of cooperative breeders.     

Dispersal of sibling coalitions promotes helping among immigrants in a cooperatively breeding bird

Kin selection is a major force in social evolution, but dispersal is often assumed to reduce its impact by diluting kinship. In most cooperatively breeding vertebrates, in which more than two individuals care for young, juveniles delay dispersal and become helpers in family groups. In long-tailed tits (Aegithalos caudatus), however, offspring disperse to breed and helpers are failed breeders that preferentially aid kin. Helping also occurs among immigrants, but their origins are unknown and cooperation in these cases is poorly understood. Here, we combine long-term demographic and genetic data from our study population to investigate immigration and helping in this species. We first used a novel application of parentage analysis to discriminate between immigrants and unknown philopatric recruits. We then cross-checked sibship reconstruction with pairwise relatedness estimates to show that immigrants disperse in sibling coalitions and helping among them is kin biased. These results indicate that dispersal need not preclude sociality, and dispersal of kin coalitions may help maintain kin-selected cooperation in the absence of delayed dispersal.