Post-hatching parental care masks the effects of egg size on offspring fitness: a removal experiment on burying beetles

Parents can increase the fitness of their offspring by allocating nutrients to eggs and/or providing care for eggs and offspring. Although we have a good understanding of the adaptive significance of both egg size and parental care, remarkably little is known about the co-evolution of these two mechanisms for increasing offspring fitness. Here, we report a parental removal experiment on the burying beetle Nicrophorus vespilloides in which we test whether post-hatching parental care masks the effect of egg size on offspring fitness. As predicted, we found that the parent's presence or absence had a strong main effect on larval body mass, whereas there was no detectable effect of egg size. Furthermore, egg size had a strong and positive effect on offspring body mass in the parent's absence, whereas it had no effect on offspring body mass in the parent's presence. These results support the suggestion that the stronger effect of post-hatching parental care on offspring growth masks the weaker effect of egg size. We found no correlation between the number and size of eggs. However, there was a negative correlation between larval body mass and brood size in the parent's presence, but not in its absence. These findings suggest that the trade-off between number and size of offspring is shifted from the egg stage towards the end of the parental care period and that post-hatching parental care somehow moderates this trade-off.     

Parental care masks a density‐dependent shift from cooperation to competition among burying beetle larvae

Studies of siblings have focused mainly on their competitive interactions and to a lesser extent on their cooperation. However, competition and cooperation are at opposite ends on a continuum of possible interactions and the nature of these interactions may be flexible with ecological factors tipping the balance toward competition in some environments and cooperation in others. Here we show that the presence of parental care and the density of larvae on the breeding carcass change the outcome of sibling interactions in burying beetle broods. With full parental care there was a strong negative relationship between larval density and larval mass, consistent with sibling competition for resources. In the absence of care, initial increases in larval density had beneficial effects on larval mass but further increases in larval density reduced larval mass. This likely reflects a density‐dependent shift between cooperation and competition. In a second experiment, we manipulated larval density and removed parental care. We found that the ability of larvae to penetrate the breeding carcass increased with larval density and that feeding within the carcass resulted in heavier larvae than feeding outside the carcass. However, larval density did not influence carcass decay.     

Individual variation in parental tradeoffs between the number and size of offspring at the pre- and post-natal stages

Life-history theory predicts that parents refer to the resources they hold to determine their breeding strategy. In multi-brooded species, it is hypothesized that single-brooded parents produce larger clutches and raise offspring with a brood survival strategy, whereas multi-brooded parents only do this under good breeding conditions. Under poor conditions, they produce smaller clutches and raise offspring with a brood reduction strategy. We tested this hypothesis in the Brown-cheeked Laughing Thrush Trochalopteron henrici, which can breed twice a year on the Tibetan Plateau, by investigating the life-history traits and provisioning behaviours of single- and double-brooded parents. Single-brooded parents laid larger clutches of smaller eggs and produced more and larger fledglings than double-brooded parents in their first brood. Double-brooded parents produced smaller clutches of larger eggs but fledged larger nestlings in their first brood than in their second brood. As single-brooded parents only need to raise one brood a year, then producing and raising as many offspring as possible (i.e. the brood survival strategy in a large brood) can maximize their reproductive success. For double-brooded parents, producing and raising fewer offspring in the first brood (i.e. the brood survival strategy in a small brood) can ensure their nesting success during a short breeding cycle. Additionally, producing more offspring but raising larger nestlings in the second brood (i.e. the brood reduction strategy in a large brood) can select for offspring of higher quality within the brood. Our findings indicate that different tradeoffs between single- and double-brooded parents in egg-laying and nestling-raising may be an adaptation to the seasonal variation in environmental conditions.     

Burying beetles: intraspecific interactions and reproductive success in the field

Abstract. 1. The discovery and utilization of small carcasses by burying beetles (Silphidae, Nicrophorus ) was studied by placing dead mice at random points on large grids at two Iocations in Michigan, U.S.A.
2. The majority of mice are found within 24 h by more beetles than ultimately will utilize the carcass. If a carcass is likely to be usurped by a larger species of beetle or by a vertebrate, then intraspecific competition may be postponed until the carcass is concealed and buried.
3. Both males and females practice parental care. Maturing broods are tended by no adults, a single female, a single male, or a male—female pair. No differences in brood success were observed among these categories.
4. The female lays a larger clutch than ultimately will survive. Brood size is regulated after the egg stage, such that offspring number varies, but individual offspring size does not.
5. A large amount of unexplained variation exists in brood size, in both the laboratory and the field. This variation is probably caused by the environment, and not the reproductive physiology of the beetles. Competition with microbes is a likely candidate.
6. Differences exist not only between Nicrophorus species, but also between localities for a single species, suggesting adaptation to local environments.     

A double-edged sword: parental care increases risk of offspring infection by a maternally vectored parasite

Parental care can protect offspring from predators but can also create opportunities for parents to vector parasites to their offspring. We hypothesized that the risk of infection by maternally vectored parasites would increase with the frequency of mother–offspring contact. Ammophila spp. wasps (Hymenoptera: Sphecidae) build nests in which they rear a single offspring. Ammophila species exhibit varied offspring provisioning behaviours: some species enter the nest once to provision a single, large caterpillar, whereas others enter the nest repeatedly to provision with many smaller caterpillars. We hypothesized that each nest visit increases the risk of offspring parasitism by Paraxenos lugubris (Strepsiptera: Xenidae), whose infectious stages ride on the mother wasp (phoresy) to reach the vulnerable Ammophila offspring. We quantified parasitism risk by external examination of museum-curated Ammophila specimens—the anterior portion of P. lugubris protrudes between the adult host''s abdominal sclerites and reflects infection during the larval stage. As predicted, Ammophila species that receive larger numbers of provisions incur greater risks of parasitism, with nest provisioning behaviour explaining ca 90% of the interspecific variation in mean parasitism. These findings demonstrate that parental care can augment, rather than reduce, the risk of parasite transmission to offspring.     

Seasonal variation in parental care, offspring development, and reproductive success in the burying beetle, Nicrophorus vespillo

1. Beetles of the genus Nicrophorus reproduce on small vertebrate carcasses that they bury in the soil to provide the larvae with food. Usually, both parents cooperate in brood care by feeding and guarding their progeny. 2. In pairs of the common European species N. vespillo, the duration of care depended on the time of year when the beetles reproduced. Both in 1990 and in 1991, male and female parents stayed longer with their broods when reproduction started in spring than when reproduction started in early or late summer. This was probably due to the longer development time of the larvae caused by lower temperatures in spring, because laboratory experiments suggested a strong influence of temperature on both the duration of brood care and offspring development. 3. The number of adult offspring produced by a beetle pair did not vary among different times of the year. 4. The median time required for offspring development, measured as time from burial of the carcass to emergence of young adults, was between 62 and 84 days. When the beetles reproduced in late summer, only about three-quarters of the offspring left the soil and hibernated as adults. The remaining offspring stayed underground and adults appeared on the soil surface the following spring. They still showed the flexible cuticle typical of newly-hatched beetles, suggesting that they may have overwintered in a pre-adult stage.     

Parasites and parental care in male upland bullies (Eleotridae)

Parental care of eggs by male upland bullies Gobiomorphus breviceps was studied in the field and in the laboratory, with special emphasis on the effect of infection by trematode cysts. In the field, the proportion of old eggs in the nest affected the time taken by males to return to their nest after being chased away, but only in one year of the study. No effects of male size, male parasite load, number of eggs per nest or nest characteristics were observed. In the laboratory, heavily-infected males spent more time fanning their eggs than lightly-infected ones. Smaller males also tended to spend more time fanning than large males. Male size, parasite load and number of eggs per nest had no measurable effect on the aggressiveness of guarding males towards intruders, weight loss in males or egg incubation time. Parental investments did not vary as a function of age of the eggs. All males cannibalized some of their eggs, and there appeared to be a threshold brood size below which males consumed their entire brood. Overall, results were not consistent with those of studies on other fish species, and indicate that rules of investment in parental care may be different for fish inhabiting harsh, unpredictable environments.     

Flexible parents: joint effects of handicapping and brood size manipulation on female parental care in Nicrophorus vespilloides

Parental care is highly variable, reflecting that parents make flexible decisions in response to variation in the cost of care to themselves and the benefit to their offspring. Much of the evidence that parents respond to such variation derives from handicapping and brood size manipulations, the separate effects of which are well understood. However, little is known about their joint effects. Here, we fill this gap by conducting a joint handicapping and brood size manipulation in the burying beetle Nicrophorus vespilloides. We handicapped half of the females by attaching a lead weight to their pronotum, leaving the remaining females as controls. We also manipulated brood size by providing each female with 5, 20 or 40 larvae. In contrast to what we predicted, handicapped females spent more time provisioning food than controls. We also found that handicapped females spent more time consuming carrion. Furthermore, handicapped females spent a similar amount of time consuming carrion regardless of brood size, whereas controls spent more time consuming carrion as brood increased. Females spent more time provisioning food towards larger broods, and females were more likely to engage in carrion consumption when caring for larger broods. We conclude that females respond to both handicapping and brood size manipulations, but these responses are largely independent of each other. Overall, our results suggest that handicapping might lead to a higher investment into current reproduction and that it might be associated with compensatory responses that negate the detrimental impact of higher cost of care in handicapped parents.     

The frequency and fitness consequences of communal breeding in a natural population of burying beetles: a test of reproductive skew

Abstract.  1. Reproductive cooperation occurs in diverse taxa and a defining characteristic of these social systems is how reproduction is shared. Both male and female burying beetles ( Nicrophorus spp.) facultatively form associations to bury a carcass and rear a single brood, making burying beetles a model system for testing skew theory.
2. In this study, 50% of 40–45 g carcasses and 75% of 55–60 g ones were buried by more than one male and/or female Nicrophorus tomentosus .
3. Females were significantly more likely to cooperate on 55–60 g carcasses than on 40–45 g ones.
4. Analysis of parentage of 13 broods using microsatellite loci as genetic markers showed that maternity analysis of only 2% of the young excluded all females captured leaving the brood chamber after burial. Males previously mated with resident females or displaced by resident males fathered 7% of the young.
5. The male and female remaining the longest were usually the parents of the most offspring, and reproductively dominant individuals also tended to be the largest.
6. Although all but two or three individuals that helped to bury the carcass produced some offspring, reproduction was often not shared equitably. Reproduction of females was significantly skewed on six of nine 40–45 g carcasses but shared fairly equitably on all three 55–60 g ones. Reproduction was skewed among males on 7 of 10 broods.
7. Both males and females relinquished a greater proportion of the brood as the days of assistance from all consexuals increased.     

State‐dependent cooperation in burying beetles: parents adjust their contribution towards care based on both their own and their partner's size

Handicapping experiments on species with biparental care show that a focal parent increases its contribution when its partner is handicapped. Such results are interpreted as evidence for negotiation, whereby each parent adjusts its amount of care to that of its partner. However, it is currently unclear whether the focal parent responds to a change in its handicapped partner's behaviour or state. To address this gap, we conducted an experiment on the burying beetle Nicrophorus vespilloides where we first generated different‐sized males and females by varying the duration of larval development. We then used a 2 × 2 factorial design in which a small or large male was paired with a small or large female. Small females provided less direct care (food provisioning and interactions with larvae) than large females, and both males and females provided less direct care when paired with a small partner. Thus, the focal parent adjusted its contribution towards care based on both its own state and that of its partner. There was also evidence for negotiation between the two parents as the focal parent adjusted its contribution based on the amount of care by its partner. However, there was no evidence that negotiation accounted for how the focal parent responded to its partner's size. Our results have important implications for our understanding of biparental cooperation as they show that each parent adjusts its contribution not only based on the amount of care provided by its partner but also based on its own state and its partner's state.     

Family dynamics through time: brood reduction followed by parental compensation with aggression and favouritism

Parental food allocation in birds has long been a focal point for life history and parent–offspring conflict theories. In asynchronously hatching species, parents are thought to either adjust brood size through death of marginal offspring (brood reduction), or feed the disadvantaged chicks to reduce the competitive hierarchy (parental compensation). Here, we show that parent American coots (Fulica americana) practice both strategies by switching from brood reduction to compensation across time. Late‐hatching chicks suffer higher mortality only for the first few days after hatching. Later, parents begin to exhibit parental aggression towards older chicks and each parent favours a single chick, both of which are typically the youngest of the surviving offspring. The late‐hatched survivors can equal or exceed their older siblings in size prior to independence. A mixed allocation strategy allows parents to compensate for the costs of competitive hierarchies while gaining the benefits of hatching asynchrony.     

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.     

Energy expenditure, nestling age, and brood size: an experimental study of parental behavior in the great tit Parus major

A brood manipulation experiment on great tits Parus major was performedto study the effects of nestling age and brood size on parentalcare and offspring survival. Daily energy expenditure (DEE)of females feeding nestlings of 6 and 12 days of age was measuredusing the doubly-labeled water technique. Females adjusted theirbrooding behavior to the age of the young. The data are consistentwith the idea that brooding behavior was determined primarilyby the thermoregulatory requirements of the brood. Female DEEdid not differ with nestling age; when differences in body masswere controlled for, it was lower during the brooding periodthan later. In enlarged broods, both parents showed significantlyhigher rates of food provisioning to the brood. Female DEE wasaffected by brood size manipulation, and it did not level offwith brood size. There was no significant effect of nestlingage on the relation between DEE and manipulation. Birds wereable to raise a larger brood than the natural brood size, althoughlarger broods suffered from increased nestling mortality ratesduring the peak demand period of the nestlings. Offspring conditionat fledging was negatively affected by brood size manipulation,but recruitment rate per brood was positively related to broodsize, suggesting that the optimal brood size exceeds the naturalbrood size in this population.     

Growth rate variation among passerine species in tropical and temperate sites: an antagonistic interaction between parental food provisioning and nest predation risk

Causes of interspecific variation in growth rates within and among geographic regions remain poorly understood. Passerine birds represent an intriguing case because differing theories yield the possibility of an antagonistic interaction between nest predation risk and food delivery rates on evolution of growth rates. We test this possibility among 64 Passerine species studied on three continents, including tropical and north and south temperate latitudes. Growth rates increased strongly with nestling predation rates within, but not between, sites. The importance of nest predation was further emphasized by revealing hidden allometric scaling effects. Nestling predation risk also was associated with reduced total feeding rates and per-nestling feeding rates within each site. Consequently, faster growth rates were associated with decreased per-nestling food delivery rates across species, both within and among regions. These relationships suggest that Passerines can evolve growth strategies in response to predation risk whereby food resources are not the primary limit on growth rate differences among species. In contrast, reaction norms of growth rate relative to brood size suggest that food may limit growth rates within species in temperate, but not tropical, regions. Results here provide new insight into evolution of growth strategies relative to predation risk and food within and among species.