The effect of parental quality and malaria infection on nestling performance in the Collared Flycatcher (Ficedula albicollis)

Plumage ornamentation often signals the quality of males and, therefore, female birds may choose elaborately ornamented mates to increase their fitness. Such mate choice may confer both direct and indirect benefits to the offspring. Males with elaborate ornaments may provide good genes, which can result in better nestling growth, survival or resistance against parasitic infections. However, these males may also provision their offspring with more food or food of better quality, resulting in nestlings growing at a higher rate or fledging in better condition. In this study, we examined if there was an association between male ornamentation and malaria infection in Collared Flycatchers (Ficedula albicollis). We also investigated offspring performance in relation to malaria infection in the parents and the quality of the genetic and rearing fathers (assessed by the size of two secondary sexual characters) under simulated good and bad conditions (using brood size manipulation). We found that secondary sexual characters did not signal the ability of males to avoid parasitic infections, and malaria infection in the genetic and the rearing parents had no effect on nestling growth and fledging size. Our results do show, however, that it may be beneficial for the females to mate with males with a large forehead patch because wing feathers of nestlings reared by large-patched males grew at a higher rate. Fast feather growth can result in earlier fledging which, in turn, could improve nestling survival in highly variable environments or under strong nest predation.     

Context-dependent effects of parental effort on malaria infection in a wild bird population, and their role in reproductive trade-offs

Although trade-offs between reproductive effort and other fitness components are frequently documented in wild populations, the underlying physiological mechanisms remain poorly understood. Parasitism has been suggested to mediate reproductive trade-offs, yet only a limited number of parasite taxa have been studied, and reproductive effort-induced changes in parasitism are rarely linked to trade-offs observed in the same population. We conducted a brood size manipulation experiment in blue tits (Cyanistes caeruleus) infected with malaria (Plasmodium) parasites, and used quantitative PCR to measure changes in parasitaemia. In one of two years investigated, parasitaemia increased as a result of brood enlargement, and was also positively associated with two other indicators of reproductive effort: clutch size and single parenthood. These associations between both experimental and naturally varying reproductive effort and parasitaemia suggest that immune control of chronic malaria infections can be compromised when parents are working hard. Brood size manipulation significantly affected the number of independent offspring produced, which was maximised when brood size was unchanged. Moreover, when parents were infected with one of two common Plasmodium species, the shape of this trade-off curve was more pronounced, suggesting that parasitic infection may exacerbate the trade-off between quantity and quality of offspring. Although the involvement of parasites in survival costs of reproduction has received much attention, these results suggest their role in other commonly documented reproductive trade-offs, such as that between number and quality of offspring, warrants further study.     

Avian malaria is associated with increased reproductive investment in the blue tit

Haemosporidians causing avian malaria are very common parasites among bird species. Their negative effects have been repeatedly reported in terms of deterioration in survival prospects or reproductive success. However, a positive association between blood parasites and avian fitness has also been reported. Here, we studied a relationship between presence of malaria parasites and reproductive performance of the host, a hole‐breeding passerine – the blue tit Cyanistes caeruleus. Since the malaria parasites might affect their hosts differently depending on environmental conditions, we performed brood size manipulation experiment to differentiate parental reproductive effort and study the potential interaction between infection status and brood rearing conditions on reproductive performance. We found individuals infected with malaria parasites to breed later in the season in comparison with uninfected birds, but no differences were detected in clutch size. Interestingly, infected parents produced heavier and larger offspring with stronger reaction to phytohemagglutinin. More importantly, we found a significant interaction between infection status and brood size manipulation in offspring tarsus length and reaction to phytohemagglutinin: presence of parasites had stronger positive effect among birds caring for experimentally enlarged broods. Our results might be interpreted either in the light of the parasite‐mediated selection or terminal investment hypothesis.     

Do females adjust brood sex ratio according to males’ genetic structures in a gregarious passerine,the vinous‐throated parrotbill Paradoxornis webbianus?

A growing number of bird species are known to have fine‐scale genetic structure during the breeding season, with relatives breeding in close vicinity. Such genetic structure often has fitness consequences for parents, and sex ratio theory predicts that females should respond adaptively when they determine offspring sex. We examined whether or not females allocate offspring sex adaptively in response to the local genetic structures as well as other biotic and abiotic factors in a population of the vinous‐throated parrotbill Paradoxornis webbianus, a small passerine with strong flocking habit and various genetic structures among neighbouring males during the breeding season. The average brood sex ratio of hatchlings (secondary sex ratio) did not deviate from parity. In addition, the observed brood sex ratio was independent of the fine‐scale genetic structure and other factors including breeding density, clutch size, laying date, parents’ quality, and the presence of extrapair paternity. Accordingly, we reject the hypothesis of adaptive sex allocation by female parrotbills in association with local genetic structure and other factors. Instead we conclude that despite the plausible benefits of biased sex allocation, this species determines brood sex ratio via random sex allocation with equal probability of male and female offspring.     

Offspring dynamics affect food provisioning,growth and mortality in a brood-caring spider

In brood-caring species, family members are faced with a conflict over resource distribution. While parents are selected to adapt the amount of care according to their offspring''s needs, offspring might be selected to demand more care than optimal for parents. Recent studies on birds have shown that the social network structure of offspring affects the amount of care and thus the fitness of families. Such a network structure of repeated interactions is probably influenced by within-brood relatedness. We experimentally manipulated the group composition in a brood-caring spider to test how the presence of unrelated spiderlings affects the dynamics between female and brood as well as within broods. Broods consisting of siblings grew better and had a lower mortality compared with mixed broods, no matter whether the caring female was a genetic or foster mother. Interestingly, we found that foster mothers lost weight when caring for sibling broods, whereas females caring for mixed broods gained weight. This indicates that females may be willing to share more prey when the brood contains exclusively siblings even if the entire brood is unrelated to the female. Resource distribution may thus be negotiated by offspring dynamics that could have a signalling function to females.     

Asynchronous hatching in the burying beetle,Nicrophorus quadripunctatus,maxmizes parental fitness

Life history theory predicts that natural selection favours parents who balance investment across offspring to maximize fitness. Theoretical studies have shown that the optimal level of parental investment from the offspring's perspective exceeds that of its parents, and the disparity between the two generates evolutionary conflict for the allocation of parental investment. In various species, the offspring hatch asynchronously. The age hierarchy of the offspring usually establishes competitive asymmetries within the brood and determines the allocation of parental investment among offspring. However, it is not clear whether the allocation of parental investment determined by hatching pattern is optimal for parent or offspring. Here, we manipulated the hatching pattern of the burying beetle Nicrophorus quadripunctatus to demonstrate the influence of hatching pattern on the allocation of parental investment. We found that the total weight of a brood was largest in the group that mimicked the natural hatching pattern, with the offspring skewed towards early hatchers. This increases parental fitness. However, hatching patterns with more later hatchers had heavier individual offspring weights, which increases offspring fitness, but this hatching pattern is not observed in the wild. Thus, our study suggests that the natural hatching pattern optimizes parental fitness, rather than offspring fitness.     

EVOLUTION OF OBLIGATE SIBLICIDE IN BOOBIES. 2: FOOD LIMITATION AND PARENT–OFFSPRING CONFLICT

Proximate limitation on parental food delivery has long been invoked to explain the evolution of single-chick broods of pelagic seabirds such as masked boobies (Sula dactylatra). A second possible proximate limit on brood size is siblicide driven by genetic parent–offspring conflict (POC) over brood size, if siblicidal offspring can reduce brood size to one even if the parents' optimal brood size is greater than one. I tested these two hypotheses by experimentally suppressing obligate siblicide in masked booby broods and comparing breeding parameters of these broods with unmanipulated single-chick control broods. Per capita mortality rate of experimental nestlings was higher than that of controls, but this deficit was more than made up by larger brood size. Parents of experimental broods brought more food to offspring, had higher fledging success, and apparently incurred no additional major short-term cost of reproduction, relative to parents of control broods, thus refuting the food limitation hypothesis. Estimates of inclusive fitness of chicks in experimental broods were higher than were those of control nestlings, a result inconsistent with the POC hypothesis that the siblicidal offspring's optimal brood size is one while the parents' optimum is greater than one. This discrepency between natural brood size and apparent brood size optima might be resolved in several ways: experimental artifacts may give misleading estimates of optimal brood size; experimental and control offspring may have different reproductive values at the time of fledging; nestling masked boobies may face a special frequency-dependent case of POC in which the high risk of sharing a nest with a siblicidal sibling makes invasion of other behavioral genotypes difficult even when offspring and parent inclusive fitnesses are higher from a nonsiblicidal brood of two than from a brood of one.     

Parental care and adaptive brood sex ratio manipulation in birds

Under many circumstances, it might be adaptive for parents to bias the investment in offspring in relation to sex. Recently developed molecular techniques that allow sex determination of newly hatched offspring have caused a surge in studies of avian sex allocation. Whether females bias the primary brood sex ratio in relation to factors such as environmental and parental quality is debated. Progress is hampered because the mechanisms for primary sex ratio manipulation are unknown. Moreover, publication bias against non-significant results may distort our view of adaptive sex ratio manipulation. Despite this, there is recent experimental evidence for adaptive brood sex ratio manipulation in birds. Parental care is a particularly likely candidate to affect the brood sex ratio because it can have strong direct effects on the fitness of both parents and their offspring. We investigate and make predictions of factors that can be important for adaptive brood sex ratio manipulation under different patterns of parental care. We encourage correlational studies based on sufficiently large datasets to ensure high statistical power, studies identifying and experimentally altering factors with sex-differential fitness effects that may cause brood sex ratio skew, and studies that experimentally manipulate brood sex ratio and investigate fitness effects.     

Evaluation of Darwin's fecundity advantage hypothesis in Parthenium beetle,Zygogramma bicolorata

In the Parthenium beetle, Zygogramma bicolorata Pallister (Coleoptera: Chrysomelidae), variation in body size exists between and within the sexes. The females are larger than the males. Darwin (1874) proposed the fecundity advantage hypothesis, that is, large‐sized females produce more progeny, with subsequent studies supporting, as well as, refuting the hypothesis. Thus, in order to evaluate whether this hypothesis stands in Z. bicolorata we performed experiments to investigate the role of body size in influencing: (i) assortative mating; (ii) reproductive attributes; and (iii) growth, development and survival of offspring. It is the first attempt in this beetle. We found that size influenced assortative mating, reproductive output and offspring fitness. Larger males and females were preferred as mates over smaller ones. The pairs, having larger adults as mates, had higher fecundity, while the egg viability was influenced by the male size only. The offspring of larger parents had fast development and higher survival, indicating thereby possible better nutrient allotment by the female and supply of accessory gland proteins by the male in addition to better quality of genes.     

Spatial structure and parental aggression in eider broods

The spatial position of young animals within a brood affects their survival, so that marginal individuals are at greater risk of predation. Spatial brood structuring may be caused by differences in offspring size, age, hunger, or active parental manipulation through aggression. Nepotistic manipulation of brood structure would confer fitness benefits for parents accepting nondescendant young. However, insufficient kin recognition has often been considered to preclude such nepotism in birds, particularly in precocial waterfowl. We explored the spatial structure of ducklings within broods of eiders, Somateria mollissima, a seaduck with frequent brood amalgamation. We compared the distribution of ducklings of different origin relative to reference females whose kinship to the ducklings was known. We also observed female aggression towards ducklings, to evaluate the role of parental manipulation of brood structure. We found a nonrandom distribution of ducklings within broods; a female's own young were on average closer to her than unrelated young were. We also found evidence for parental nepotism: whether the brood contained unrelated young was the strongest predictor of female aggression towards ducklings. The spatial position, hatch weight and relative size of ducklings showed no significant correlations with each other, suggesting that active parental manipulation may be needed to explain the observed spatial structure. Our study conflicts with previous anecdotal evidence suggesting that brood amalgamation in eiders results in the disintegration of parent-offspring bonds, preventing parental exploitation of nondescendant young. It also opens up the possibility that the spatial position of ducklings depends on their mother's status in the female dominance hierarchy. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Relationships between brood size and offspring body size in an ovoviviparous fish: maternal effects and genetic trade-off

Maternal effects can form an important source of variation in offspring fitness and have important evolutionary and ecological consequences. To explore genetic control for body size of newborn offspring, the present study examined maternal brood size and offspring body size in 14 strains and performed cross experiments in an ovoviviparous fish, guppy. Correlation analyses among the strains indicated that the strains with larger brood size have smaller offspring body size. Diallel and reciprocal crosses among four strains revealed a large maternal, but no paternal, contribution to offspring body size. To examine whether offspring body size is determined by maternal genotypes and whether offspring body size correlates with albinism, backcrosses were performed between a wild-type strain with large offspring body size and an albino strain. Offspring body size differed from both the parental strains in one generation of backcrossing but was not significantly different from the paternal strains after three generations. In the backcross generations, the offspring yielded by albino individuals showed significantly smaller body size than those yielded by normal individuals. These results indicated that offspring body size is determined by maternal genotypes, suggesting that offspring body size is influenced by the maternal albinism gene or the maternal locus linked with the albinism locus. The significant negative correlation between maternal brood size and offspring body size detected through our experiments showed that the maternal genetic character of brood size strongly correlated with offspring body size, indicating genetic trade-off between maternal brood size and offspring body size in the guppy.     

Interaction between parental care and sibling competition: parents enhance offspring growth and exacerbate sibling competition

Species with elaborate parental care often also show intense sibling competition over resources provided by parents, suggesting joint evolution of these two traits. Despite this, the evolution of elaborate parental care and the evolution of intense sibling competition are often studied separately. Here, we examine the interaction between parental food provisioning and sibling competition for resources through the joint manipulation of the presence or absence of parents and brood size in a species with facultative parental care: the burying beetle Nicrophorus vespilloides. The effect of the interaction between the presence or absence of parents and brood size was strong; brood size had a strong effect on growth when parents provided care, but no effect when parents were absent. As in previous studies, offspring grew faster when parents were present than when parents were absent, and offspring grew faster in smaller broods than in larger broods. Our behavioral observations showed that brood size had a negative effect on both the amount of time parents spent providing resources to individual offspring and the offspring's effectiveness of begging, confirming that the level of sibling competition increased with brood size. Furthermore, offspring in larger broods shifted more from begging toward self-feeding as they grew older compared to offspring in small broods. Our study provides novel insights into the joint evolution of parental care and sibling competition, and the evolution of offspring begging signals. We discuss the implications of our results in light of recent theoretical work on the evolution of parental care, sibling competition, and offspring begging signals.     

Inbreeding depression in an insect with maternal care: influences of family interactions,life stage and offspring sex

Although inbreeding is commonly known to depress individual fitness, the severity of inbreeding depression varies considerably across species. Among the factors contributing to this variation, family interactions, life stage and sex of offspring have been proposed, but their joint influence on inbreeding depression remains poorly understood. Here, we demonstrate that these three factors jointly shape inbreeding depression in the European earwig, Forficula auricularia. Using a series of cross‐breeding, split‐clutch and brood size manipulation experiments conducted over two generations, we first showed that sib mating (leading to inbred offspring) did not influence the reproductive success of earwig parents. Second, the presence of tending mothers and the strength of sibling competition (i.e. brood size) did not influence the expression of inbreeding depression in the inbred offspring. By contrast, our results revealed that inbreeding dramatically depressed the reproductive success of inbred adult male offspring, but only had little effect on the reproductive success of inbred adult female offspring. Overall, this study demonstrates limited effects of family interactions on inbreeding depression in this species and emphasizes the importance of disentangling effects of sib mating early and late during development to better understand the evolution of mating systems and population dynamics.     

Mating strategies in dominant meerkats: evidence for extra‐pair paternity in relation to genetic relatedness between pair mates

Rates of extra‐pair paternity (EPP) have frequently been associated with genetic relatedness between social mates in socially monogamous birds. However, evidence is limited in mammals. Here, we investigate whether dominant females use divorce or extra‐pair paternity as a strategy to avoid the negative effects of inbreeding when paired with a related male in meerkats Suricata suricatta, a species where inbreeding depression is evident for several traits. We show that dominant breeding pairs seldom divorce, but that rates of EPP are associated with genetic similarity between mates. Although extra‐pair males are no more distantly related to the female than social males, they are more heterozygous. Nevertheless, extra‐pair pups are not more heterozygous than within‐pair pups. Whether females benefit from EPP in terms of increased fitness of the offspring, such as enhanced survival or growth, requires further investigations.     

An integrated approach to life-cycle evolution using selective landscapes

A model which defines fitness in terms of the intrinsic rate of increase of phenotypes is used to analyse which life cycles are appropriate to which ecological circumstances. The following predictions are made for asexual animals and those sexual animals producing on average more than one daughter per brood. If there are no behavioural or physiological interactions between variables, then number of offspring per breeding should be maximized, survival until first/next breeding should be maximized, and time to first/next breeding should be minimized. If interactions occur such that altering one life-cycle variable affects another, then there are trade-offs between variables and the optimum trade-off will maximize fitness.Number of offspring per breeding will generally affect adult survivorship until next breeding. Given certain reasonable assumptions about this trade-off, high juvenile survivorship selects towards semelparity (many offspring per brood), low juvenile survivorship selects towards iteroparity (few offspring per brood). If juvenile survival depends on adult feeding, as in altricial birds, then juvenile survivorship declines as clutch size is increased. Optimal clutch size maximizes the number of surviving offspring per brood.Two trade-offs involve parental care. If parents guard their offspring they should take more risks if brood size is larger. The amount that parents feed their offspring should depend on how effective feeding is in enhancing growth. Growth may also be enhanced by taking risks, in juveniles or adults. The extent of risk-taking should depend on how effective risk-taking is in enhancing growth.If the number of offspring per brood is related to growing conditions for offspring, the prediction is that more offspring per brood should be produced if growing conditions for offspring are better. If the adult can protect the offspring, for example by encapsulating them, the amount of protection provided should depend on how effective the protection is in increasing offspring survivorship.     

Sexual dimorphism,survival, and parental investment in relation to offspring sex in a precocial bird

Differential growth rate between males and females, owing to a sexual size dimorphism, has been proposed as a mechanism driving sex‐biased survival. How parents respond to this selection pressure through sex ratio manipulation and sex‐biased parental investment can have a dramatic influence on fitness. We determined how differential growth rates during early life resulting from sexual size dimorphism affected survival of young and how parents may respond in a precocial bird, the black brant Branta bernicla nigricans. We hypothesized that more rapidly growing male goslings would suffer greater mortality than females during brood rearing and that parents would respond to this by manipulating their primary sex ratio and parental investment. Male brant goslings suffered a 19.5% reduction in survival relative to female goslings and, based on simulation, we determined that a female biased population sex ratio at fledging was never overcome even though previous work demonstrated a slight male‐biased post‐fledging survival rate. Contrary to the Fisherian sex ratio adjustment hypothesis we found that individual adult female brant did not manipulate their primary sex ratio (50.39% male, n = 645), in response to the sex‐biased population level sex ratio. However, female condition at the start of the parental care period was a good predictor of their primary sex ratio. Finally, we examined how females changed their behavior in response to primary sex ratio of their broods. We hypothesized that parents would take male biased broods to areas with increased growth rates. Parents with male biased primary sex ratios took broods to areas with higher growth rates. These factors together suggest that sex‐biased growth rates during early life can dramatically affect population dynamics through sex‐biased survival and recruitment which in turn affects decisions parents make about sex allocation and sex‐biased parental investment in offspring to maximize fitness.     

Offspring fitness and individual optimization of clutch size

Within-year variation in clutch size has been claimed to be an adaptation to variation in the individual capacity to raise offspring. We tested this hypothesis by manipulating brood size to one common size, and predicted that if clutch size is individually optimized, then birds with originally large clutches have a higher fitness than birds with originally small clutches. No evidence was found that fitness was related to the original clutch size, and in this population clutch size is thus not related to the parental capacity to raise offspring. However, offspring from larger original clutches recruited better than their nest mates that came from smaller original clutches. This suggests that early maternal or genetic variation in viability is related to clutch size.     

Should mothers provision their offspring equally? A manipulative field test

Within‐brood variation in offspring size is universal, but its causes are unclear. Theoretical explanations for within‐brood variation commonly invoke bet‐hedging, although alternatives consider the role of sibling competition. Despite abundant theory, empirical manipulations of within‐brood variation in offspring size are rare. Using a field experiment, we investigate the consequences of unequal maternal provisioning for both maternal and offspring fitness in a marine invertebrate. We create experimental broods of siblings with identical mean, but different variance, in offspring size, and different sibling densities. Overall, more‐variable broods had higher mean performance than less‐variable broods, suggesting benefits of unequal provisioning that arise independently of bet‐hedging. Complementarity effects drove these benefits, apparently because offspring‐size variation promotes resource partitioning. We suggest that when siblings compete for the same resources, and offspring size affects niche usage, the production of more‐variable broods can provide greater fitness returns given the same maternal investment; a process unanticipated by the current theory.     

Adjustment of parental expenditure in sympatric <Emphasis Type="Italic">Onthophagus</Emphasis> beetles (Coleoptera: Scarabaeidae)

Many organisms adjust their parental expenditure to offspring in response to resource quality. However, the mechanisms underlying the adjustment in parental expenditure are not well understood. We examined the adjustments in parental expenditure and subsequent offspring performance in two sympatric, closely related dung beetles, Onthophagus ater and O. fodiens, that were provided either monkey, deer, horse, or cow dung. The egg contained within each dung brood mass provisioned by the parent beetles develops to adulthood underground. Thus, the size of the brood mass roughly represents the amount of parental expenditure. The brood mass size differed between the two species and among the four dung types. Results of offspring performance suggested that O. ater parents optimally adjusted the brood mass size in response to dung quality, whereas O. fodiens parents did not. We hypothesized that brood mass size in O. ater may increase with prolonged egg maturation caused by the lower nutrition level of cow dung. In addition, our complex results may be explained in part by the specific threshold concept of dung quality (i.e., water content and nutritional level).     

Is the small clutch size of a Corsican blue tit population optimal?

In an attempt to test predictions of the optimisation hypothesis of life history traits in birds, we estimated fitness consequences of brood size manipulations. Experiments were carried out over a period of 4 years in a Mediterranean population of blue tits Parus caeruleus which is confronted with a particular set of environmental constraints. Effects of brood size manipulation were investigated in relation to year-to-year variation in environmental conditions, especially caterpillar abundance. There was a strong variation in the effects of brood size manipulation depending on year. Most effects were on offspring quality (fledging mass, tarsus length). The absolute number of recruits did not significantly differ among categories (reduced, control, enlarged broods) but varied considerably among years. Females recruited from enlarged broods were of lower quality, started to breed later and laid fewer eggs than those recruited from control and reduced broods. Neither parental survival nor reproductive performances of adults in year n + 1 was affected by brood size manipulation in year n. Thus there was no evidence for a cost of reproduction in this population. Since the number of recruits did not depend on brood size manipulation (recruitment rates were higher in reduced broods), but recruits from reduced broods were of better quality compared with other groups, we conclude that adults lay a clutch that is larger than that which is predicted by the optimisation hypothesis. Producing more young could incur some penalties because offspring from large broods are of lower quality and less likely to recruit in the population. Two possible reasons why decision rules in this population seem to be suboptimal are discussed. Received: 10 March 1998 / Accepted: 1 July 1998