Effects of maternal stress on egg characteristics in a cooperatively breeding fish

Elevated stress experienced by a mother can compromise both her own reproductive success and that of her offspring. In this study, we investigated whether chronically stressed mothers experienced such effects in cooperatively breeding species, in which helpers at the nest potentially compound the negative effects of maternal stress. Using Neolamprologus pulcher, a group-living cichlid fish from Lake Tanganyika, we observed the effects of experimentally increased stress on female reproductive success (measured as inter-spawn interval, and number of eggs) as well as egg characteristics including egg size and cortisol concentrations. Stress levels were manipulated by repeated exposure to the acute stresses of chasing and netting. Stressed females had longer inter-spawn intervals and laid fewer, smaller eggs. Although no significant differences in egg cortisol concentrations were detected between control and stressed females, egg cortisol concentration fell between spawns in control but not in stressed fish. No effect of helper number was detected for any parameter examined, except there appeared to be less change in egg cortisol content in groups with helpers present. Our results suggest that stress imposes fitness costs on breeding females, and social regulation of a dominance hierarchy does not appear to exacerbate or alleviate the negative effects of maternal stress.     

Experimental evidence for kin-biased helping in a cooperatively breeding vertebrate

The widespread belief that kin selection is necessary for the evolution of cooperative breeding in vertebrates has recently been questioned. These doubts have primarily arisen because of the paucity of unequivocal evidence for kin preferences in cooperative behaviour. Using the cooperative breeding system of long-tailed tits (Aegithalos caudatus) in which kin and non-kin breed within each social unit and helpers are failed breeders, we investigated whether helpers preferentially direct their care towards kin following breeding failure. First, using observational data, we show that not all failed breeders actually become helpers, but that those that do help usually do so at the nest of a close relative. Second, we confirm the importance of kinship for helping in this species by conducting a choice experiment. We show that potential helpers do not become helpers in the absence of close kin and, when given a choice between helping equidistant broods belonging to kin and non-kin within the same social unit, virtually all helped at the nest of kin. This study provides strong evidence that kinship plays an essential role in the maintenance of cooperative breeding in this species.     

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.     

Evidence for size and sex-specific dispersal in a cooperatively breeding cichlid fish

African Great Lake cichlid populations are divided into thousands of genetic subpopulations. The low gene flow between these subpopulations is thought to result from high degrees of natal philopatry, heavy predation pressure, and a patchy distribution of preferred habitats. While predation pressure and habitat distribution are fairly straightforward to assess, data on dispersal distances and rates are scarce. In fishes, direct observations of dispersal events are unlikely, but dispersal can be studied using molecular markers. Using seven microsatellite loci, we examined dispersal in the cooperatively breeding cichlid fish, Neolamprologus pulcher. As this species is found in well-defined groups clustered into subpopulations, we could assess dispersal on a narrow (within subpopulation) and broad (between subpopulation) scale. While fish were generally more related to others in their own subpopulation than they were to fish from other subpopulations, large males diverged from this pattern. Large males were more related to other large males from different subpopulations than they were to large males from their own subpopulation, suggesting more frequent dispersal by large males. Across subpopulations, relatedness between large males was higher than the relatedness among large females; this pattern was not detected in small males and small females. Within a subpopulation, individuals appeared to be preferentially moving away from relatives, and movement was unrestricted by the physical distance between groups. Our results highlight the importance of examining multiple spatial scales when studying individual dispersal biases.     

Reproductive parasitism of broodcare helpers in a cooperatively breeding fish

Large male helpers in the cooperatively breeding cichlid Neolamprologus pulchergain reproductive success by parasitizing the reproductive effort ofmale territory owners. Under controlled, experimental conditionswe examined 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 fingerprintingto check for potential reproductive parasitism by male helpersand to assess their fertilization success. Of offspring producedin these families, 10.3% were sired by helpers. In parasitizedbroods, helper fertilization success varied between 12.5% and35.8%. Male helpers parasitized parental reproduction when theirbody size exceeded 4.5 cm standard length (SL), even thoughsexual maturity may be reached much earlier (3.5 cm SL). Twoof three parasitic helpers were punished by severe aggressiveattacks when parasitizing the reproduction of breeders, whichled to their expulsion from the territory. This study demonstratesa potential fitness benefit to broodcare helpers that is oftenneglected. It also points to the delicate balance that may exist betweencooperative and competitive behavior in cooperatively breeding species.     

Male reproductive suppression in the cooperatively breeding fish Neolamprologus pulcher

In most cooperative breeders, dominants suppress the reproductionof subordinates. However, two previous studies of Neolamprologuspulcher, a cooperatively breeding cichlid fish, have suggestedthat socially subordinate helper males sneak fertilizationsfrom dominant breeding males. If such sneaking does occur, boththeoretical work and empirical studies of other fish speciessuggest that sperm competition will select for increased reproductiveinvestment by sneaker males, relative to more dominant males.To address these issues, we quantified gonadal investment andsperm characteristics of 41 N. pulcher male breeders and 62male helpers from 55 groups in Lake Tanganyika. Gonadal investmentfollowed patterns consistent with reproductive suppression,with breeders having considerably larger testes masses thanhelpers. Breeders also had faster and longer swimming spermand a higher percentage of motile sperm compared to helpers.However, sperm characteristics of large helpers were similarto those of breeders, but these same helpers had lower testesmasses. Thus, large helpers had sperm that were physiologicallyequivalent to that of breeders, but their relatively small gonadsimply that they were reproductively suppressed.     

Sex-biased preferential care in the cooperatively breeding Arabian babbler

In many social birds there are sex differences in dispersal patterns, with males commonly remaining in their natal group whereas females typically disperse at adolescence. Group members may therefore increase their fitness by preferentially caring for offspring of a particular sex according to social circumstances. Although previous studies have focussed on intragroup social factors that may affect preferential care, we propose that the relative size of neighbouring groups is of primary importance. Here we show that in the cooperatively breeding Arabian babbler (Turdoides squamiceps), parents preferentially feed male offspring when relative group size is small, and female offspring when group size is large. Unlike parents, helpers consistently favour young of the opposite sex to themselves, suggesting the risk of competition with members of the same sex for future breeding opportunities may override other considerations. These results emphasize the complexity of investment strategies in relation to social circumstances and the variable benefits of raising males vs. females in a species with sex-biased philopatry.     

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.     

The role of prolactin in the regulation of brood care in the cooperatively breeding fish Neolamprologus pulcher

The hormone prolactin (PRL) is important for the regulation of parental care in many species of mammals, birds and fish, and for alloparental care (care directed at nondescendant young) in some mammals and birds. Its significance in alloparental brood care of cooperatively breeding fish has not yet been assessed. Here, we test the role of PRL in brood care behavior of the cooperatively breeding cichlid Neolamprologus pulcher. The expression of PRL mRNA was determined in the pituitary glands of breeders of both sexes, helpers that showed brood care behavior and nonbreeding fish as controls. In addition, PRL levels were experimentally manipulated in male breeders and helpers by intraperitoneal injections of ovine PRL, and the behavior of these test fish was recorded toward standardized clutches. Adult females had higher levels of PRL mRNA than adult males, which was true both for breeders and nonbreeders. Contrary to expectation, there was no positive correlation between PRL and brood care behavior in any category of test fish, and the experimental application of PRL did not change brood care propensity. Interestingly, brood-caring adult females had significantly lower levels of PRL mRNA than adult female nonbreeders, whereas there was no difference between helpers and similar-sized nonbreeding group members. PRL mRNA levels increased with body mass in juveniles, but decreased with body mass in adults. In conclusion, we found no evidence that elevated levels of PRL are directly involved in the regulation of brood care behavior in this species.     

Explaining variation in maternal care in a cooperatively breeding mammal

Because of the necessity of lactation, mammalian mothers must perform at least a minimum amount of infant care. In cooperatively breeding species, other group members aid in all other aspects of infant care. However, some mothers continue to carry and nurse their infants more than others. The golden lion tamarin, Leontopithecus rosalia, is a small, communally breeding primate in the family Callitrichidae. We studied hormonal, individual, historical and social factors hypothesized to contribute to variation in levels of maternal care. We used neonatal weight as a measure of prenatal care, and carrying and nursing as measures of postnatal care. Greater neonatal weight was associated with smaller litter size, lower prepartum levels of oestrogen conjugates, and higher prepartum cortisol levels. Higher rates of carrying during weeks 2 and 3 were associated with higher maternal weight, larger litter size and smaller numbers of helpers per infant. Higher rates of nursing in weeks 2 and 3 were predicted by smaller group size and provisioning of the mother. The most important factors affecting postnatal maternal care were maternal weight, group size, litter size and provisioning status of the mother. Thus, females that display higher levels of maternal care do so either because they have to (they have fewer helpers) or because they can (they are in better condition).     

Lateralization in response to social stimuli in a cooperatively breeding cichlid fish

Cerebral lateralization, an evolutionarily ancient and widespread phenomenon among vertebrates, is thought to bestow cognitive advantages. The advantages of lateralization at the individual-level do not necessarily require that the entire population share the same pattern of lateralization. In fact, directional bias in lateralization may lead to behavioural predictability and enhanced predator success or prey evasion. Recent theory has suggested that population-level lateralization may be favored if individuals are better able to perform coordinated behaviours, providing a distinct advantage in cooperative contexts. Here we test whether the highly social, cooperatively breeding cichlid fish Neolamprologus pulcher shows lateralized responses to a social stimulus. We found population-level biases in males; on average male N. pulcher use their right eye/left hemisphere to view their mirror image. Individual females had a preferred hemisphere, but these preferences appeared not to be directionally aligned among females. We discuss these results in the context of coordinated social behaviour and suggest future research directions.     

First evidence for heritable variation in cooperative breeding behaviour

Understanding the evolution of complex social behaviours, such as cooperative breeding, is a fundamental problem in evolutionary biology, which has attracted much theoretical and empirical interest. Variation within and between species in the frequency of helping behaviour has been typically associated with variation in direct costs and benefits due to ecological constraints, or with indirect fitness payoffs (i.e. kin selection). Here, we provide the first evidence that individual variation in cooperative behaviour within a natural population also has a heritable component. Using a seven-generation pedigree in a wild population of western bluebirds (Sialia mexicana), we show significant heritable variation for the propensity to help rather than breed, as well as for the probability of having a helper at the nest. We also document a strong positive relationship between a bird's lifespan and its prospect of receiving help when breeding, in accordance with earlier comparative studies across species. These findings provide useful insights into the possible mechanisms which have led to the evolution of cooperative breeding and other social systems.     

Long-term brood division and exclusive parental care in a cooperatively breeding passerine

In some species of birds, individual adults feed different subsets of the brood after the young have left the nest. However, few studies have shown that such ‘brood division’ represents long-term separation into subfamilies, rather than short-term biases in care, and the function of brood division is unknown. Most functional hypotheses assume that brood division is an adult adaptation to increase reproductive success; others suggest that fledglings are responsible for brood division, or that brood division is the outcome of conflicts of interest within families. We tested for long-term brood division in the white-browed scrubwren, Sericornis frontalis, a cooperatively breeding passerine, and assessed functional hypotheses, using behavioural, morphological and molecular evidence. We found that 71% of scrubwren broods became divided in the second week after fledging, and remained divided for the following 4-5 weeks of care. Furthermore, most individual young were fed almost exclusively by a single adult, even in undivided broods and broods of one. Brood division did not arise through adults caring for young of a specific sex, nor did genetic paternity explain division. Tests of other hypotheses were indirect, relying for example on testing mechanisms rather than predictions. We rejected the hypotheses that brood division was primarily an adaptation to reduce the mean or variance in predation, or that it was likely to increase the rate at which young were provisioned. Fledglings probably had an active role in maintaining brood division, with fledglings that had been biggest in the nest tending to be fed by adults that had fed nestlings at the greatest rate. This suggests that the most dominant fledgling may sequester the care of the best feeder. We also found evidence that brood division might be an adult adaptation to reduce the effects of sibling competition, or that it might arise through conflicts of interest among adults. We further suggest that social specialization, resulting from learning about a particular individual, might bring additional advantages to long-term brood division. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Variable infant care contributions in cooperatively breeding groups of wild saddleback tamarins

Among non-human primates, alloparental infant care is most extensive in callitrichines, and is thought to be particularly costly for tamarins whose helpers may suffer increased energy expenditure, weight loss, and reduced feeding time and mobility. The costs and benefits of infant care likely vary among group members yet very few wild studies have investigated variable infant care contributions. We studied infant care over an 8-month period in four wild groups of saddleback tamarins in Bolivia to evaluate: (a) what forms of infant care are provided, by whom, and when, (b) how individuals adjust their behavior (activity, vigilance, height) while caring for infants, and (c) whether individuals differ in their infant care contributions. We found that infant carrying, food sharing, and grooming varied among groups, and immigrant males—those who joined the group after infants were conceived—participated less in infant care compared to resident males. Adult tamarins fed less, rested more, and increased vigilance while carrying infants. Although we did not detect changes in overall activity budgets between prepartum and postpartum periods, tamarins spent more time scanning their environments postpartum, potentially reflecting increased predation risk to both carriers and infants during this period. Our study provides the first quantitative data on the timing and amount of infant carrying, grooming, and food transfer contributed by all individuals within and among multiple wild groups, filling a critical knowledge gap about the factors affecting infant care, and highlighting evolutionary hypotheses for cooperative breeding in tamarins.     

Intragroup social dynamics vary with the presence of neighbors in a cooperatively breeding fish

Conflict is an in here nt part of social life in group-living species. Group members may mediate conflict through submissive and affiliative behaviors, which can reduce aggression, stabilize dominance hierarchies, and foster group cohesion. The frequency and resolution of within-group conflict may vary with the presenee of neighboring groups. Neighbors can threaten the territory or resources of the whole group, promoting behaviors that foster within-group cohesion. However, neighbors may also foster conflict of interests among group members: opportunities for subordinate dispersal may alter conflict among dominants and subordinates while opportunities for extrapair reproduction may increase conflict between mates. To understand how neighbors mediate within-group conflict in the cooperatively breeding fish Neolamprologus pulcher, we measured behavioral dynamics and social network structure in isolated groups, groups recently exposed to neighbors, and groups with established neighbors. Aggression and submission between the dominant male and female pair were high in isolated groups, but dominant aggression was directly primarily at subordinates when groups had neighbors. This suggests that neighbors attenuate conflict between mates and foster conflict between dominants and subordinates. Further, aggression and submission between similarly sized group members were most frequent when groups had neighbors, suggesting that neighbors induce rank-related conflict. We found relatively little change in within-group affiliative networks across treatments, suggesting that the presence of neighbors does not alter behaviors associated with promoting group cohesion. Collectively, these results provide some of the first empirical insights into the extent to which intragroup behavioral networks are mediated by intergroup interactions and the broader social context.     

First report of alloparental care in the Key Largo woodrat (Neotoma floridana smalli)

Here we report the first observation of alloparental care in a subadult female Key Largo woodrat. Maternal and other behaviors were scored for the subject dam and her subadult daughter at the birth of the dam’s second litter and the following 30 days. After assisting with birth, the subadult exhibited maternal behaviors and remained in close proximity to the pups. The rate of maternal care behaviors observed in the subject dam was lower than in solitary dams without an alloparent present. However, the total maternal care score for the dam and subadult combined approached the average score for single dams.     

Evidence for frequent incest in a cooperatively breeding mammal

As breeding between relatives often results in inbreeding depression, inbreeding avoidance is widespread in the animal kingdom. However, inbreeding avoidance may entail fitness costs. For example, dispersal away from relatives may reduce survival. How these conflicting selection pressures are resolved is challenging to investigate, but theoretical models predict that inbreeding should occur frequently in some systems. Despite this, few studies have found evidence of regular incest in mammals, even in social species where relatives are spatio-temporally clustered and opportunities for inbreeding frequently arise. We used genetic parentage assignments together with relatedness data to quantify inbreeding rates in a wild population of banded mongooses, a cooperatively breeding carnivore. We show that females regularly conceive to close relatives, including fathers and brothers. We suggest that the costs of inbreeding avoidance may sometimes outweigh the benefits, even in cooperatively breeding species where strong within-group incest avoidance is considered to be the norm.