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.     

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.     

Age-dependent reproductive costs and the role of breeding skills in the Collared flycatcher

This study addressed whether there are any age‐related differences in reproductive costs. Of especial interest was whether young individuals increased their reproductive effort, and thereby their reproductive cost, as much as older birds when brood size was enlarged. To address these questions, a brood‐size manipulation experiment with reciprocal cross‐fostering of nestlings of young and middle‐aged female Collared flycatchers, Ficedula albicollis, was performed on the Swedish island of Gotland. Nestlings’ body mass, tarsus length and survival were recorded to estimate the parental ability and parental effort of the experimental female birds. Female survival and clutch size were recorded in the following years to estimate reproductive costs. We found that middle‐aged female flycatchers coped better with enlarged broods than younger females or invested more in reproduction. In the following year, young female birds that had raised enlarged broods laid smaller clutches than the females from all the other experimental groups. This result shows that the young female birds pay higher reproductive costs than the middle‐aged females. Both young and middle‐aged female flycatchers seemed to increase their reproductive effort when brood size was increased. However, such an increase resulted in higher reproductive costs for the young females. The difference in reproductive costs between birds of different ages is most likely a result of insufficient breeding skills of the young individuals.     

Stable group size in cooperative breeders: the role of inheritance and reproductive skew

Recent studies of reproductive skew have revealed great variationin the distribution of direct fitness among group members, yetthere have been surprisingly few attempts to explore the consequencesof such variation for stable group size, and none that takeinto account the future benefits of group membership to nonbreeders.This means that the existing theory is not suited to explainthe group size of most cooperatively breeding vertebrates andprimitively social insects in which group membership involvessubstantial future benefits. Here we model the group size ofsuch species as social queues in which nonbreeders can inherita breeding position if they outlive those ahead of them in thequeue. We demonstrate, however, that the results can be generalizedto systems in which inheritance occurs via scramble competition,rather than via a strict queue. The model predicts that stablegroup size will depend on the number of breeding positions inthe group and the mortality rates of breeders and nonbreeders,but not on the distribution of reproduction among the pool ofbreeders. This is because deaths occur at random, so that eachindividual has the same chance of surviving to reach each breedingposition. We tested a specific prediction of the model usingdata on ovarian development in the paper wasp, Polistes dominulus.We found a positive correlation between group size and the proportionof females with fully developed eggs, as predicted. Our resultsclarify the interaction between the dominance structure andsize of animal groups and add to the growing recognition ofthe potential for inheritance as a major determinant of bothindividual behavior and group-level characteristics of animalsocieties.     

Reproductive skew and group size: an N-person staying incentive model

Transactional models of social evolution emphasize that dominantbreeders may donate parcels of reproduction to subordinatesin return for peaceful cooperation. We develop a general transactionalmodel of reproductive partitioning and group size for N-persongroups when (1) expected group output is a concave (decelerating)functiong[N] of the number N of group members, and (2) thesubordinates may receive fractions of total group reproduction("staying incentives") just sufficient to induce them to stayand help the dominant instead of breeding solitarily. We focusespecially on "saturated" groups, that is, groups that havegrown in size just up to the point where subsequent joining by subordinates is no longer beneficial either to them (in parent-offspring groups) or to the dominant (in symmetric-relatedness groups).Decreased expected output for solitary breeding increases thesaturated group size and decreases the staying incentives.Increased relatedness decreases both the saturated group sizeand the staying incentives. However, in saturated groups withsymmetric relatedness, an individual subordinate's staying incentive converges to 1 — g[N^* — 1]/g[N^*]) regardless ofrelatedness, where N^* is the size of a saturated group, providedthat the g[N] function near the saturated group size N^* isapproximately linear. Thus, staying incentives can be insensitiveto relatedness in saturated groups, although the dominant's total fraction of reproduction (total skew) will be more sensitive.The predicted ordering for saturated group size is: Parent-fullsibling offspring = non-relatives > symmetrically relatedrelatives. Strikingly, stable groups of non-relatives can formfor concaveg[N] functions in our model but not in previousmodels of group size lacking skew manipulation by the dominant.Finally, symmetrical relatedness groups should tend to breakup by threatened ejections of subordinates by dominants, whereas parent-offspring groups should tend to breakup via unforceddepartures by subordinates.     

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.     

Effects of clutch size manipulations on reproductive behaviour and nesting success in the cooperatively breeding Bell Miner (Manorina melanophrys)

Summary An experimental manipulation of clutch size was carried out on a wild population of the cooperatively breeding Bell Miner (Manorina melanophrys, Meliphagidae) to assess which factor(s) limit clutch size in this species. Results provide some support for the trade-off hypothesis since there is a cost of reproduction for the breeding female in terms of loss of body mass. The breeding female performs most of the nestling care. Clutches of three eggs are also laid during the mid-breeding season which is the period most favourable for breeding (i.e. nestlings grow faster). This evidence also supports the intrabrood competition hypothesis. Clutches that have lost an egg were more likely to be deserted; this may be an antipredator strategy since partial clutch predation has been recorded in the field. Nest predation was high in this study (64.9%), suggesting that many small clutches may be a strategy to decrease the effect of nest predation on reproductive success over the whole breeding season (nest predation hypothesis). Both the trade-off hypothesis and the nest predation hypothesis may apply in this case since they are not mutually exclusive. The size of the attending group did not greatly affect reproductive success in the short term, although if both age structure and size of the group are taken into account, reproductive success can be better predicted.     

Reproductive skew, costs, and benefits of cooperative breeding in female wood mice (Apodemus sylvaticus)

Two current models seek to explain reproduction of subordinatesin social groups: incentives given by dominants for peacefullyremaining in the group (reproductive skew model) or incompletecontrol by dominants. These models make different predictionsconcerning genetic relatedness between individuals for thedistribution of reproduction and the stability of cooperativebreeding associations. To test these models and to furtherexplore the relationships between reproductive skew, geneticrelatedness, and investment of each participant, we performedbehavioral observations of female wood mice (Apodemus sylvaticus)raising pups communally. Our results do not support previousmodels. Differences in lifetime reproductive success were significantlygreater within mother—daughter pairs than within pairsof sisters or unrelated females. Subordinate females of eitherbreeding unit did not differ in their direct reproduction.Calculations of inclusive fitness based on our results leadto the following predictions: (1) Communal nests should occuronly when ecological circumstances prevent solitary breeding.(2) Subordinate females gain the highest inclusive fitnessjoining their mothers; they also show the highest nursing investment.(3) Mothers should accept daughters, who have no opportunityfor solitary breeding. (4) Dominant sisters and unrelated femalesshould reject subordinate females because cooperative breedingreduces their reproductive success. However, breeding unitsof dominant sisters and unrelated females nevertheless occurand can be explained by our finding that such females significantlyreduce nursing time, which may help them save energy for futurebreeding cycles. Our data demonstrate that both genetic relatednessand investment skew are important in the complex evolutionof reproductive skew in cooperative breeding.     

Cooperative breeding in birds: the role of ecology

Theory predicts that cooperative breeding should only occurin species in which certain individuals are constrained frombreeding independently by some peculiarity of the species' ecology.Here, we use comparative methods to examine the role of variationin ecology in explaining differences between taxa in the frequencyof cooperative breeding. We address three questions. First,does the frequency of cooperative breeding vary at just one phylogeneticlevel, or across several levels? Second, are differences inthe frequency of cooperative breeding among closely-relatedspecies correlated with ecology? Last, are ecological differencesbetween ancient lineages important in predisposing certain lineagesto cooperative breeding? We find that variation in the frequencyof cooperative breeding occurs across all phylogenetic levels,with 40% among families and 60% within families. Also, variationin the frequency of cooperative breeding between closely related speciesis associated with ecological differences. However, differencesin the frequency of cooperative breeding among more ancientlineages are not correlated with differences in ecology. Together,our results suggest that cooperative breeding is not due toany single factor, but is a two step-process: life-history predispositionand ecological facilitation. Low annual mortality predisposescertain lineages to cooperative breeding. Subsequently, changesin ecology facilitate the evolution of cooperative breedingwithin these predisposed lineages. The key ecological changesappear to be sedentariness and living in a relatively invariableand warm climate. Thus, although ecological variation is notthe most important factor in predisposing lineages to cooperativebreeding, it is important in determining exactly which speciesor populations in a predisposed lineage will adopt cooperativebreeding.