Sexual conflict and parental care in magnificent frigatebirds: full compensation by deserted females

Parental care is a cooperative venture between a male and a female in many socially monogamous birds. Care is costly, and thus, sexual conflict arises between the parents about how much effort they should invest into rearing their young. The sexual conflict over care is most apparent when one parent abandons the brood before the offspring are independent. The deserted parent has three options: (1) desert the brood because a single parent is unable to raise the young on its own; (2) continue care provision at the same level as during biparental care, and thus do not compensate for the absence of mate; or (3) increase care and compensate partially or totally. We investigated these options in the magnificent frigatebird, Fregata magnificens, a species in which the male deserts his mate and brood before the chick is independent. During biparental care, females fed the chick more often than the males. After their mate deserted, the females nearly doubled their feeding rate and thus, fully compensated for the lost care. Consistent with these observations, growth rates of chicks provided with biparental and female-only care did not differ. These results support recent theoretical models of parental care, and suggest that females may withhold care during biparental care to manoeuvre their mates into prolonged care provision. A female only provides at her full capacity once her mate has deserted.     

The manipulation of food resources reveals sex-specific trade-offs between parental self-feeding and offspring care

Parent Palestine sunbirds (Nectarinia osea) feed on flower nectar that is not fed to their nestlings. This phenomenon provided a unique opportunity to manipulate self-feeding rates of parent birds independently of the rate at which they feed arthropod prey to their offspring. Based on provisioning models, we predicted that parents would invest more in their young as the energy content of their own food increased. From our earlier work, we also predicted that the levels of sex-specific activities of males and females would differ as the energy content of their food increased. Sunbird pairs with two or three nestlings were provided with feeders containing a low-, medium- or high-concentration sucrose solution. As the sugar concentration increased, the females delivered arthropods at a greater rate to their nestlings, removed proportionally more faecal sacs and spent longer at the nest, while the males increased their mobbing effort. Nestling food intake and body mass, but not tarsus length or bill size, were larger in small broods than in large broods, and increased with increasing feeder sugar concentration. These results imply that increasing the energy content of food consumed by parent sunbirds allows them to increase the rate at which other foods are delivered to their young and to increase other parental care activities as well. The results also add credence to the idea that behavioural decisions reflect life-history trade-offs between parental self-feeding and investment in current young.     

Model parents: is full compensation for reduced partner nest attendance compatible with stable biparental care?

Previous models have suggested that biparental care will beevolutionarily stable when each parent only partially compensatesfor decreases in effort by their partner. We investigated asystem where breeding success is an accelerating function ofparental effort. This could occur in species with a high predationlevel—for example, in a dense sea-bird colony or in specieswhere eggs or young are very prone to cooling. In these caseswe found that parents will fully compensate for decreased partnereffort, or else they will abandon the breeding attempt altogether.We use a second graphical model to show that biparental carecan exist under a situation of full compensation for reducedpartner effort if neither parent can do all the care alone.Each parent will abandon the breeding attempt if his or hercondition falls below a certain threshold. If the participationof both parents is necessary for the breeding attempt to besuccessful, then neither parent will want to force their partnerto abandon by making them work so hard that they fall belowthe condition threshold. Because abandonment by oen partnermeans the failure of the breeding attempt, each individualwill do at least enough work so that the partner will not abandon,resulting in biparental care. There will be a region of conflictbetween the parents, within which the conflict can be resolvedin various ways. Possible resolutions of this conflict, andthe consequences and applications of the model, are discussed.     

Should young ever be better off with one parent than with two?

We analyze models of parental care, providing the first systematiccomparison of the care given to young by one parent versus bytwo parents. In the Houston-Davies model of care, young alwaysdo better with two parents rather than with one parent. Whenone parent decides about its level of care before the other,then the young may do better with one parent when the costsof care for the parents are asymmetric. When the level of parentaleffort is reached by negotiation, there are cases in which youngdo better with one parent, even when costs are symmetric. Theanalysis suggests empirical ways to differentiate between differentresponse rules.     

Negotiation over offspring care--how should parents respond to each other's efforts?

Models of biparental care predict that parents should compensateincompletely for any change in their partner's investment. Experimentaltests have, however, yielded results that range from full compensation,through a lack of any reaction, to a matching response. Herewe suggest a new, adaptive explanation for such variation. Buildingon an approach developed by McNamara et al., we incorporateuncertainty regarding brood need or value into a game-theoreticalmodel of biparental negotiation over offspring care. We showthat when each parent has only partial information, greatereffort invested by one serves as a signal to the other of broodneed. This favors a matching response by the focal parent'smate, whereas the impact of increased effort on the marginalvalue of investment favors a compensatory response. The netoutcome depends on the relative strength of these two effects.The greater the variation in brood need compared with parentalstate, the weaker the predicted level of compensation, and themore likely matching is to occur. Our model also suggests whymales and females might respond differently to each other. Ifthere is an informational asymmetry between them, then the parentthat is better informed about brood need should work harder,respond more strongly to changes in brood need, be less sensitiveto changes in the cost of feeding, and compensate more stronglyfor changes in partner effort. If the asymmetry is very great,the poorly informed parent may even match changes in its partner'swork rate.     

To Compensate or Not? Caring Parents Respond Differentially to Mate Removal and Mate Handicapping in the Burying Beetle,Nicrophorus quadripunctatus

Game theoretical models predict that when one parent reduces its care, the mate should adjust its care facultatively to compensate partially. To test these models, mate-removal and mate-handicapping techniques have been used. However, there have been few experimental studies comparing results from mate removal and mate handicapping, and there has been no study on insects employing handicapping. Male and female burying beetles both maintain the nest and regurgitate to young. We examined how burying beetle parents adjust their level of care when their mates are removed or handicapped. Males increased their frequency of provisioning significantly after female removal, whereas females showed no response to male removal. However, neither sex showed a response to the handicapping of its partner, although handicapped mates decreased the frequency of their care. This result showed that burying beetle parents respond differentially to mate removal and handicapping, and suggests that parents do not respond to a change in the behavior of their mates.     

Parentally biased favouritism: why should parents specialize in caring for different offspring?

'Parentally biased favouritism' occurs when the two parents differentially care for individual offspring or kinds of offspring. Examples in birds include brood division and differential investment by the two parents in relation to the size or sex of the offspring. This paper uses mathematical models to investigate which ideas can, in theory, explain parentally biased favouritism. One previous explanation is that the parents differ in their cost of reproduction and that the parent who consequently invests least concentrates its care on the more valuable offspring. However, a mathematical model predicts the total care given by each parent and received by each offspring, not how much each parent cares for each offspring, and hence does not explain parentally biased favouritism. Parentally biased favouritism towards particular types of offspring can be explained by a difference between the parents in the benefits of caring for a given type of offspring or in the effort incurred in providing care to a given type of offspring, but then it is extreme, with at least one of the parents providing care to only one type of offspring. Parentally biased favouritism towards particular individual offspring (brood division) can be explained by parent-offspring conflict or sexual conflict.     

Parental Self-Feeding Effects on Parental Care Levels and Time Allocation in Palestine Sunbirds

The trade-off between parents feeding themselves and their young is an important life history problem that can be considered in terms of optimal behavioral strategies. Recent studies on birds have tested how parents allocate the food between themselves and their young. Until now the effect of food consumption by parent birds on their food delivery to their young as well as other parental activities has rarely been studied. I have previously shown that parent Palestine sunbirds (Nectarinia osea) will consume nectar and liquidized arthropods from artificial feeders. However, they will only feed their young with whole arthropods. This provided a unique opportunity to experimentally manipulate the food eaten by parents independent of that fed to their offspring. Here, I hypothesized that parents invest in their current young according to the quality of food that they themselves consume. Breeding pairs with two or three nestlings were provided with feeders containing water (control), sucrose solution (0.75 mol) or liquidized mealworms mixed with sucrose solution (0.75 mol). As food quality in feeders increased (from water up to liquidized mealworms mixed with sucrose solution): 1) Parents (especially females) increased their food delivery of whole arthropod prey to their young. 2) Only males increased their nest guarding effort. Nestling food intake and growth rate increased with increasing food quality of parents and decreasing brood size. These results imply that increasing the nutrient content of foods consumed by parent sunbirds allow them to increase the rate at which other foods are delivered to their young and to increase the time spent on other parental care activities.     

Relative influence of male and female care in determining nestling mass in a migratory songbird

Biparental care is common in birds, with the allocation of effort being highly variable between the sexes. In most songbird species, the female typically provides the most care early in the breeding cycle with both parents providing care when provisioning young. Food provisioning should be directly related to offspring quality; however, the relative influence each parent has on offspring quality has rarely been assessed at the nest level. Consequently, we were interested in assessing the relative influence male and female provisioning has on one measurement of offspring quality, nestling mass, in the black‐throated blue warbler Dendroica caerulescens. Over a six year period, 2003–2008, we collected information on average nestling mass per brood on day 6 of the nestling cycle and parental provisioning rates on day 7 of the nestling cycle from 182 first brood nests on three different study plots. We found that average nestling mass was directly related to male provisioning rate, while it was not related to female provisioning rate. On the other hand, estimated biomass provisioned had little influence on average nestling mass, calling into question its utility in assessing parental quality. Finally, there was some indication that parental influence on average nestling mass was dependent on the other parent's provisioning rate, suggesting that parents work in concert to influence nestling quality.     

How is sexual conflict over parental care resolved? A meta‐analysis

Biparental care of offspring is both a form of cooperation and a source of conflict. Parents face a trade‐off between current and future reproduction: caring less for the current brood allows individuals to maintain energy reserves and increase their chances of remating. How can selection maintain biparental care, given this temptation to defect? The answer lies in how parents respond to changes in each other’s effort. Game‐theoretical models predict that biparental care is evolutionarily stable when reduced care by one parent leads its partner to increase care, but not so much that it completely compensates for the lost input. Experiments designed to reveal responses to reduced partner effort have mainly focused on birds. We present a meta‐analysis of 54 such studies, and conclude that the mean response was indeed partial compensation. Males and females responded differently and this was in part mediated by the type of manipulation used.     

Differential response by males and females to manipulation of partner contribution in the great tit (Parus major)

1.  In birds with bi-parental care, handicapping is often assumed to decrease the amount of parental care of the handicapped partner. We discuss how handicapping could alter the shape of the handicapped bird's survival–effort curve (theoretical curve relating the survival of a parent to its effort) and show that the optimal response could yield a decrease, no response or even an increase in effort of the handicapped bird.
2.  Male or female great tits Parus major (L.) were handicapped during the nestling period by clipping a number of feathers in order to study the effects on parental care and body condition.
3.  Handicapped males significantly decreased their feeding rates, while handicapped females did not. Condition of handicapped females significantly deteriorated, while condition of handicapped males did not change during the experiment. Females with a handicapped partner fully compensated for their partner's decrease in work rate, while males with a handicapped partner did not show any compensation and even tended to decrease their feeding rates.
4.  Using an inverse optimality approach, we reconstructed the theoretical curve relating the survival of a parent to its effort on the basis of the experimental effects. The handicapped male's survival–effort curve appeared to be slightly steeper than that of handicapped females. This suggests that handicapped males suffer more from an increase in effort than handicapped females.     

Sex differences in biparental care as offspring develop: a field study of convict cichlids (<Emphasis Type="Italic">Amatitlania siquia</Emphasis>)

Parental investment theory states that parents should contribute more to older offspring. Differences between the sexes also influence how each parent contributes to offspring in biparental species. Here, we examined a naturally occurring population of biparental convict cichlids in Costa Rica to determine how each parent cared for offspring during two distinct offspring development stages. Consistent with the predictions of the reproductive value hypothesis, we hypothesized that the levels of parental contribution would be relative to the value that each parent places on a brood. We predicted that female parents would contribute more than male parents because female convict cichlids have lower future reproductive success than males. Additionally, we predicted that both parents should contribute more to older offspring, either due to the young’s increased susceptibility to predation (i.e., the vulnerability hypothesis) or because of the longer period of time parents have been interacting with older offspring (i.e., feedback hypotheses). This increase in investment by males should coincide with a change in the coordination of care between parents. Detailed observations of parental pairs in their natural habitat supported these predictions. Females contributed more to broods than males and were relatively unaffected by offspring age while males spent significantly more time with older, free-swimming fry. Additionally, males tended to leave younger offspring more than females did, and were more likely to do so consecutively with younger offspring. This suggests that the coordination of duties between parents changes as parental investment changes. Overall, these data support both the reproductive value and the vulnerability hypotheses, but not necessarily the feedback hypothesis.     

Negotiation over offspring care?--a positive response to partner-provisioning rate in great tits

Game theoretical models of biparental care predict that a changein work rate by one parent should be met by incomplete compensationby its partner. However, in empirical studies on biparentalbirds, there has been some inconsistency in the direction andextent of the response, and the mechanism behind it has so farbeen unclear. Parents could be responding directly to partnerwork rate or indirectly via chick begging. In this study ofgreat tits (Parus major), the work rate of one parent was increasedexperimentally by augmenting the begging of the chicks withplayback of extra begging calls whenever the parent visitedthe nest. The playback had no effect on the chicks' beggingbehavior, so any change in the focal parent's behavior was adirect response to its partner's work rate over a short timescale.An experimental increase in care by either male or female parentled to an increase (to a lesser extent) in the work rate ofits partner, which is counter to the decrease predicted by partialcompensation models. This seemingly paradoxical result may reflectdecisions made exclusively over a short timescale and is inkeeping with new theoretical work, which takes into accountthe information content of partner work rates.     

Association studies of QTL for multi-allele markers by mixed models

In this paper, we extend association study methods of both Fan et al. [Hum Hered 2002;53:130-145], in which a quantitative trait locus (QTL) and a multi-allele marker are considered for trio families, and Fan and Xiong [Biostatistics 2003, in press], in which a QTL and a bi-allelic marker are considered for nuclear families. The objective is to build mixed models for association study between a QTL and a multi-allelic marker for nuclear families with any number of offspring. Two types of nuclear family data are considered: the first is genetic data of offspring from at least one heterozygous parents, and the second is genetic data of offspring of nuclear family. (1) For the data of offspring from at least one heterozygous parents, we assume that at least one parent is heterozygous at the marker locus, and we may infer clearly the transmission of parental marker alleles to the offspring. We show that it can be used in association study in the presence of linkage. The theoretical basis is the difference between the conditional mean of trait value given an allele is transmitted and the conditional mean of trait value given the allele is not transmitted from a heterozygous parent. To build valid models, we calculate the variance covariance structure of trait values of offspring. Besides, the reduction of the number of parameters is discussed under an assumption of tight linkage between the trait locus and the marker. (2) For the data of offspring of nuclear family, we show that it can be used in general association study. In this case, the theoretical basis is the difference between the conditional mean of trait values given an allele is transmitted from a parent and the population mean. Then, we calculate variance-covariance structure of trait values of offspring. (3) Based on the theoretical analysis, mixed models are built for each type of the data, and related test statistics are proposed for association study. By power calculation and comparison, we show that, in some instances, the proposed test statistics have higher power than that by collapsing alleles to be new ones. The proposed models are used to analyze chromosomes 4 and chromosome 16 data of the Oxford asthma data, Genetic Analysis Workshop 12.     

Begging the question: are offspring solicitation behaviours signals of need?

Throughout the animal kingdom, distinctive behaviour by offspring commonly precedes and accompanies their provisioning by parents. Here, we assess empirical support for the recent theory that begging advertises offspring need, that parents provision young in relation to begging intensity, and that the apparently costly nature of begging ensures the reliability of the signal. While there is some support for the predictions of honest signalling models, empirical work has also revealed a host of complexities (such as the use of multiple signals) that existing theoretical analyses have only begun to address.     

The effect of clutch cooling rate on starling, Sturnus vulgaris, incubation strategy

In avian species where only one parent incubates, that parent must divide its time between the mutually exclusive activities of incubation and foraging in such a way as to maintain both body condition and clutch temperature within certain limits. In a uniparental incubator, the starling, we experimentally reduced the rate at which unattended clutches of eggs cooled down and monitored the resulting changes in the parent's incubation strategy. Opposite to the predictions of standard models of time allocation during incubation, parents spent a much greater percentage of each 24-h period incubating when the rate of clutch cooling was reduced. Incubation bouts lasted significantly longer on experimental nests than on control nests, both during the daytime and overnight. Mean foraging bout duration did not differ between the two groups of nests. These results are consistent with the hypotheses that parental foraging success cues the end of a foraging bout, and that parental energy level cues the end of an incubation bout. However, most previous studies suggest that parents spend less time incubating when the rate of clutch cooling is slow. If parental energy level cues departure, these results can be explained only if the amount of time available for incubation is constrained in these cases by the time a parent must spend foraging in order to maintain body condition. Such parents should take more time away from incubation when the unattended clutch cools slowly, as this is when the cost of being absent is minimized. Copyright 1999 The Association for the Study of Animal Behaviour.     

Can low-quality parents exploit their high-quality partners to gain higher fitness?

An individual's optimal investment in parental care potentially depends on many variables, including its future fitness prospects, the expected costs of providing care and its partner's expected or observed parental behaviour. Previous models suggested that low-quality parents could evolve to exploit their high-quality partners by reducing care, leading to the paradoxical prediction that low-quality parents could have higher fitness than their high-quality partners. However, these studies lacked a complete and consistent life-history model. Here, we challenge this result, developing a consistent analytical model of parental care strategies given individual variation in quality, and checking our results using agent-based simulations. In contrast to previous models, we predict that high-quality individuals always outcompete low-quality individuals in fitness terms. However, care effort may differ between high- and low-quality parents in either direction: low-quality individuals care more than high-quality individuals if their baseline mortality is higher, but less if their mortality increases more steeply with increasing care. We also highlight the ambiguity of the term ‘quality’ and stress the need for ‘genealogical consistency’ in evolutionary models.     

Brood defence and parental roles in a biparental cichlid fishLamprologus toae in Lake Tanganyika

Brood defence of a cichlid fish,Lamprologus toae, was investigated in its natural habitat in Lake Tanganyika. Both parents guarding a brood attacked both conspecific and heterospecific intruder fishes at different locations. The heterospecific intruder fishes could be classified into three groups on the basis of the locations at which the attacks against each species took place. The distinction of groups by the parents seemed to be primarily based on food habits and feeding behaviour of the intruder fishes. The piscivorous species which were more dangerous for the brood were attacked by both parents at more distant locations from the brood. Parental defence of breeding territory changed with the development of the young. The frequency of attacks against each group decreased after the young reached the size too large for the fishes of the group to prey on. Division of labour in the territorial defence was recognized between male and female. The male parent mainly defended the peripheral region of the territory and the female parent defended the inner region. Significance of the selective attack against intruders and the division of labour between the two sexes in brood defence is discussed.     

Biparental care: short-term manipulation of partner contribution and brood size in the starling, Sturnus vulgaris

In species with biparental care, the evolutionarily stable investmentstrategy depends, among other factors, on the reproductive valueof the brood and on the contribution of one's partner. A shortfallin work rate by one parent should be partially compensated forby its partner, while both parents should invest more effortwhen there are more young. We simultaneously tested these predictionsby attaching weights to one member of pairs of European starlings(Sturnus vulgaris), thus reducing one partner's nest visitationrate, and by daily manipulation of brood sizes (between threeand seven chicks). Both sexes compensated to an equivalent degreefor their partner's lower work rate, while at the same timeadjusting flexibly to the daily brood size changes by increasingvisit rates to larger broods. However, this ability to compensatewas limited in the larger brood sizes, perhaps due to an upperlimit on provisioning rate. Weighted birds and their partnersshowed differences in prey types delivered, relative to controls,taking a lower proportion of leatherjackets. With regard tothe proximate cues affecting parental provisioning rate, beggingnoise levels (automatically recorded by computer from microphonesin the nest-box) increased with brood size, but average lengthof begging bout did not. As expected, visit rates per chickdecreased as brood size increased, and this was reflected inlower weight gains per day by chicks in larger broods. Theseresults agree in general with games theory models but revealimportant departures from our previous work with respect to(1) parents reaching an apparent ceiling to nest visitationrate at high brood sizes and (2) the ability to track thesebrood demands with short-term adjustments.     

The vigilance components of begging and sibling competition

The conflict between siblings over how parental resources are divided has promoted the evolution of specific behaviour to outcompete each other. Young animals look out for parents’ arrival in order to start begging as quickly as possible, since a rapid begging reaction increases the likelihood of being fed before nestmates. If the young can physically intercept the parents, selection might be operating on the offspring ability to monitor parent arrival (vigilance towards parents) and any sudden modifications in siblings’ behaviour (vigilance towards siblings). To investigate the adaptive value of nestling vigilance in the context of family interactions, we recorded which direction barn owl Tyto alba siblings were facing in 89 two‐chick broods before the first parental feeding visit of the night. Nestlings were more vigilant towards nest entrance than expected by chance suggesting that vigilance towards parents is an important component of sibling competition. When positioned near the nest‐box entrance where parents predictably deliver food, the younger individual (i.e. junior) looked more towards the entrance than its older sibling. Thus, when the likelihood of obtaining a food item is relatively high, juniors are more vigilant than seniors to detect the incoming parent. When positioned at the back of the nest, the senior looked relatively more frequently towards its sibling than the junior did in the same situation. This suggests that when the likelihood of obtaining a food item is relatively low, seniors are more vigilant than juniors to observe their sibling. Because vigilance was not related to hunger level and prey obtaining, we propose the hypothesis that vigilance towards parents and siblings only indirectly influences the outcome of sibling competition.