Major benefits of guarding behavior in subsocial bees: implications for social evolution

Parental care is a behavior that increases the growth and survival of offspring, often at a cost to the parents' own survival and/or future reproduction. In this study, we focused on nest guarding, which is one of the most important types of extended parental care; we studied this behavior in two solitary bee species of the genus Ceratina with social ancestors. We performed the experiment of removing the laying female, who usually guards the nest after completing its provisioning, to test the effects of nest guarding on the offspring survival and nest fate. By dissecting natural nests, we found that Ceratina cucurbitina females always guarded their offspring until the offspring reached adulthood. In addition, the females of this species were able to crawl across the nest partitions and inspect the offspring in the brood cells. In contrast, several Ceratina chalybea females guarded their nests until the offspring reached adulthood, but others closed the nest entrance with a plug and deserted the nest. Nests with a low number of provisioned cells were more likely to be plugged and abandoned than nests with a higher number of cells. The female removal experiment had a significantly negative effect on offspring survival in both species. These nests frequently failed due to the attacks of natural enemies (e.g., ants, chalcidoid wasps, and other competing Ceratina bees). Increased offspring survival is the most important benefit of the guarding strategy. The abandonment of a potentially unsuccessful brood might constitute a benefit of the nest plugging behavior. The facultative nest desertion strategy is a derived behavior in the studied bees and constitutes an example of an evolutionary reduction in the extent of parental care.     

Social Experience During Development and Female Offspring Aggression in Peromyscus Mice

Cross‐fostering between the highly aggressive, biparental California mouse (Peromyscus californicus) and the less aggressive, less parental white‐footed mouse (P. leucopus) influences female offspring attack latency in California mice, but not in white‐footed mice. Adult female California mice raised by white‐footed mice expressed longer attack latencies in a neutral‐arena test but not in a resident‐intruder test. One social cue that may be used by offspring to develop environmentally appropriate levels of aggression is the type of parental care during development. In California mice, a composite score of maternal behavior was positively associated with neutral‐arena aggression as indicated by decreased attack latency. In both species, paternal nest‐building was positively associated with neutral‐arena aggression and higher maternal retrieval behavior predicted higher offspring resident‐intruder aggression as indicated by decreased attack latency. Together, these results indicate that parental behavior has the potential to shape the development of attack latency in female offspring.     

Feathers,suspicions, and infidelities: an experimental study on parental care and certainty of paternity in the blue tit

Theoretical models on parental care predict that males should decrease their parental effort when paternity is in doubt. Males may use some cues to assess their certainty of paternity, and try to avoid rearing offspring sired by extra‐pair males. We have previously reported in a socially monogamous passerine, the blue tit (Cyanistes caeruleus), that males decorate their nests with feathers, and that when this ornament is manipulated, males appear to have suspicions about the presence of an intruder male. Here, we decrease the male's certainty of paternity through experimental feather supplementation to analyse whether the outcome of our experiment supports the assumptions of the parental care theory. Male C. caeruleus responded to the feather supplementation experiment by reducing their parental investment (feeding frequency and nest defence) in comparison with control males. The occurrence of extra‐pair offspring in experimental nests was double than that in controls. This suggests that the manipulation was successful not only in altering males' perceived paternity, but also, indirectly, the actual paternity. Furthermore, males that gained extra‐pair young also had a higher than average probability to lose paternity in their nest, which may imply that male C. caeruleus faced a trade‐off between obtaining extra‐pair fertilizations and maintaining paternity in their own nest. Overall, this study supports the idea that males are prone to decrease their parental effort when they perceive that the risk of losing paternity is high. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 552–561.     

Contribution of males to brood care can compensate for their food consumption from a shared resource

The sharing of the same food source among parents and offspring can be a driver of the evolution of family life and parental care. However, if all family members desire the same meal, competitive situations can arise, especially if resource depletion is likely. When food is shared for reproduction and the raising of offspring, parents have to decide whether they should invest in self‐maintenance or in their offspring and it is not entirely clear how these two strategies are balanced. In the burying beetle Nicrophorus vespilloides, parents care for their offspring either bi‐ or uniparentally at a vertebrate carcass as the sole food source. The question of whether biparental care in this species offers the offspring a better environment for development compared with uniparental care has been the subject of some debate. We tested the hypothesis that male contribution to biparental brood care has a beneficial effect on offspring fitness but that this effect can be masked because the male also feeds from the shared resource. We show that a mouse carcass prepared by two Nicrophorus beetles is lighter compared with a carcass prepared by a single female beetle at the start of larval hatching and provisioning. This difference in carcass mass can influence offspring fitness when food availability is limited, supporting our hypothesis. Our results provide new insights into the possible evolutionary pathway of biparental care in this species of burying beetles.     

Flexible communication within bird families—The consequences of behavioral plasticity for parent–offspring coadaptation

Offspring are selected to demand more resources than what is optimal for their parents to provide, which results in a complex and dynamic interplay during parental care. Parent–offspring communication often involves conspicuous begging by the offspring which triggers a parental response, typically the transfer of food. So begging and parental provisioning reciprocally influence each other and are therefore expected to coevolve. There is indeed empirical evidence for covariation of offspring begging and parental provisioning at the phenotypic level. However, whether this reflects genetic correlations of mean levels of behaviors or a covariation of the slopes of offspring demand and parental supply functions (= behavioral plasticity) is not known. The latter has gone rather unnoticed—despite the obvious dynamics of parent–offspring communication. In this study, we measured parental provisioning and begging behavior at two different hunger levels using canaries (Serinus canaria) as a model species. This enabled us to simultaneously study the plastic responses of the parents and the offspring to changes in offspring need. We first tested whether parent and offspring behaviors covary phenotypically. Then, using a covariance partitioning approach, we estimated whether the covariance predominantly occurred at a between‐nest level (i.e., indicating a fixed strategy) or at a within‐nest level (i.e., reflecting a flexible strategy). We found positive phenotypic covariation of offspring begging and parental provisioning, confirming previous evidence. Yet, this phenotypic covariation was mainly driven by a covariance at the within‐nest level. That is parental and offspring behaviors covary because of a plastic behavioral coadjustment, indicating that behavioral plasticity could be a main driver of parent–offspring coadaptation.     

Do Brooding Pythons Recognize their Clutches? Investigating External Cues for Offspring Recognition in the Children's Python,Antaresia childreni

Parental care provides substantial benefits to offspring but exacts a high cost to parents, necessitating the evolution of offspring recognition systems when the risk of misdirected care is high. In species that nest, parents can use cues associated with the offspring (direct offspring recognition) or the nest (indirect offspring recognition) to reduce the risk of misdirected care. Pythons have complex parental care, but a low risk of misdirected care. Thus, we hypothesized that female Children's pythons (Antaresia childreni) use indirect cues to induce and maintain brooding behavior. To test this, we used a series of five clutch manipulations to test the importance of various external brooding cues. Contrary to our hypothesis, we found that female A. childreni are heavily internally motivated to brood, needing only minimal external cues to induce and maintain egg‐brooding behavior. Females were no more likely to brood their own clutch in the original nest as they were to brood a clutch from a conspecific, a pseudoclutch made from only the shells of a conspecific, or their clutch in a novel nest. The only scenario where brooding was reduced, but even then not eliminated, was when the natural clutch was replaced with similarly sized stones. These results suggest that egg recognition in pythons is similar to that of solitary‐nesting birds, which have similar nesting dynamics.     

The post‐fledging period in a tropical bird: patterns of parental care and survival

How environmental conditions affect the timing and extent of parental care is a fundamental question in comparative studies of life histories. The post‐fledging period is deemed critical for offspring fitness, yet few studies have examined this period, particularly in tropical birds. Tropical birds are predicted to have extended parental care during the post‐fledging period and this period may be key to understanding geographic variation in avian reproductive strategies. We studied a neotropical passerine, the western slaty‐antshrike Thamnophilus atrinucha, and predicted greater care and higher survival during the post‐fledging period compared to earlier stages. Furthermore, we predicted that duration of post‐fledging parental care and survival would be at the upper end of the distribution for Northern Hemisphere passerines. Correspondingly, we observed that provisioning continued for 6–12 weeks after fledging. In addition, provisioning rate was greater after fledging and offspring survival from fledging to independence was 75%, greater than all estimates from north‐temperate passerines. Intervals between nesting attempts were longer when the first brood produced successful fledglings compared to nests where offspring died either in the nest or upon fledging. Parents delayed initiating second nests after the first successful brood until fledglings were near independence. Our results indicate that parents provide greater care after fledging and this extended care likely increased offspring survival. Moreover, our findings of extended post‐fledging parental care and higher post‐fledging survival compared to Northern Hemisphere species have implications for understanding latitudinal variation in reproductive effort and parental investment strategies.     

Biparental care is predominant and beneficial to parents in the burying beetle Nicrophorus orbicollis (Coleoptera: Silphidae)

Parenting strategies can be flexible within a species and may have varying fitness effects. Understanding this flexibility and its fitness consequences is important for understanding why parenting strategies evolve. In the present study, we investigate the fitness consequences of flexible parenting in the burying beetle Nicrophorus orbicollis, a species known for its advanced provisioning behaviour of regurgitated vertebrate carrion to offspring by both sexes. We show that, even when a parent is freely allowed to abandon the carcass at any point in time, biparental post‐hatching care is the most common pattern of care adopted in N. orbicollis. Furthermore, two parents together raised more offspring than single parents of either sex, showing that the presence of the male can directly influence parental fitness even in the absence of competitors. This contrasts with studies in other species of burying beetle, where biparental families do not differ in offspring number. This may explain why biparental care is more common in N. orbicollis than in other burying beetles. We suggest how the fitness benefits of two parents may play a role in the evolution and maintenance of flexible biparental care in N. orbicollis.     

Nest visit synchrony is high and correlates with reproductive success in the wild Zebra finch Taeniopygia guttata

Nest visit synchrony, whereby adults coordinate their visits to the nest, has been documented in several species of cooperative breeders. Visit synchrony may reduce nest predation rate or sibling competition, or instead follow from synchronisation of other behaviours, such as foraging. However, nest visit synchrony has rarely been considered in species with bi‐parental care, even though it could conceivably bring similar fitness benefits to that seen in cooperative breeders. In addition, in species with bi‐parental care, we might expect nest visit synchrony to reflect the quality of the pair or the overall coordination of breeding activity between partners. Here, we tested whether nest visit synchrony occurs in a classic avian model for the study of bi‐parental care, the zebra finch Taeniopygia guttata. We found that in the wild, both zebra finch parents visited the nest very infrequently during nestling provisioning, with only one visit per hour, and that nest visits were highly synchronised with parents visiting the nest together on 78% of the visits. In addition, we found that nest visit synchrony was correlated with hatching rate, brood size at hatching and the number of offspring in the nest a few days prior to fledging. Our results suggest that, while more work is required to understand the benefits of nest visit synchrony in this species, considering behavioural synchrony and cooperation between mated partners may offer new insight into the study of parental investment, including in species with bi‐parental care.     

Individual Consistency in Parental Effort Across Multiple Stages of Care in the House Sparrow, Passer domesticus

In many avian species in which biparental care is provided to offspring, substantial variation exists within members of each sex in the level of effort contributed to various forms of parental care. Questions remain as to whether individuals that contribute more toward one parental activity also contribute more toward other activities in which they participate. We examined the contributions of male and female house sparrows (Passer domesticus) to three forms of parental care: incubation, nestling provisioning, and nest defense, and compared the investments made by individuals at each stage of care relative to other same‐sexed parents. In both males and females, nestling feeding rates were positively associated with time spent incubating, but no relationships were found between measures of nestling feeding and nest defense. The predictability of an individual's feeding behavior based on earlier incubation efforts may make incubation a good stage for individuals to evaluate the parental abilities of their partners.     

Females compensate for moult‐associated male nest desertion in Hooded Warblers

Uniparental offspring desertion occurs in a wide variety of avian taxa and usually reflects sexual conflict over parental care. In many species, desertion yields immediate reproductive benefits for deserters if they can re‐mate and breed again during the same nesting season; in such cases desertion may be selectively advantageous even if it significantly reduces the fitness of the current brood. However, in many other species, parents desert late‐season offspring when opportunities to re‐nest are absent. In these cases, any reproductive benefits of desertion are delayed, and desertion is unlikely to be advantageous unless the deserted parent can compensate for the loss of its partner and minimize costs to the current brood. We tested this parental compensation hypothesis in Hooded Warblers Setophaga citrina, a species in which males regularly desert late‐season nestlings and fledglings during moult. Females from deserted nests effectively doubled their provisioning efforts, and nestlings from deserted nests received just as much food, gained mass at the same rate, and were no more likely to die from either complete nest predation or brood reduction as young from biparental nests. The female provisioning response, however, was significantly related to nestling age; females undercompensated for male desertion when the nestlings were young, but overcompensated as nestlings approached fledging age, probably because of time constraints that brooding imposed on females with young nestlings. Overall, our results indicate that female Hooded Warblers completely compensate for male moult‐associated nest desertion, and that deserting males pay no reproductive cost for desertion, at least up to the point of fledging. Along with other studies, our findings support the general conclusion that late‐season offspring desertion is likely to evolve only when parental compensation by the deserted partner can minimize costs to the current brood.     

Are species differences in maternal effects arising from maternal care adaptive?

Parental care benefits offspring through maternal effects influencing their development, growth and survival. However, although parental care in general is likely the result of adaptive evolution, it does not follow that specific differences in the maternal effects that arise from care are also adaptive. Here, we used an interspecific cross‐fostering design in the burying beetle species Nicrophorus orbicollis and N. vespilloides, both of which have elaborate parental care involving direct feeding of regurgitated food to offspring, to test whether maternal effects are optimized within a species and therefore adaptive. Using a full‐factorial design, we first demonstrated that N. orbicollis care for offspring longer regardless of recipient species. We then examined offspring development and mass in offspring reared by hetero‐ or conspecific parents. As expected, there were species‐specific direct effects independent of the maternal effects, as N. orbicollis larvae were larger and took longer to develop than N. vespilloides regardless of caregiver. We also found significant differences in maternal effects: N. vespilloides maternal care caused more rapid development of offspring of either species. Contrary to expectations if maternal effects were species‐specific, there were no significant interactions between caretaker and recipient species for either development time or mass, suggesting that these maternal effects are general rather than optimized within species. We suggest that rather than coadaptation between parents and offspring performance, the species differences in maternal effects may be correlated with direct effects, and that their evolution is driven by selection on those direct effects.     

Subsocial behaviour in Oniticellus cinctus (Coleoptera, Scarabaeidae): effect of the brood on parental care and oviposition

ABSTRACT. In Oniticellus cinctus (F.) the nest chambers each contain about twenty brood balls. Females enlarge the brood balls during the egg and larval stages and remain in the chamber for the whole period of brood development (1 month); they then make a new nest after 1 week. The presence of the brood releases parental care and ensures that the mother remains in the nest: she repairs defects in the brood balls and the nest, and expels other O. cinctus females. A new ball is formed around a naked O. cinctus larva, but larvae of other species are killed. In addition, the brood inhibits oviposition: removal (or addition) of brood balls stimulates (or inhibits) egg laying. In inhibited ovarioles, existing follicles are resorbed and production of new ones ceases. Control of clutch size by the brood is an adaptation to the nest structure and life history of O. cinctus. It may have an important role in the reproductive strategy of other insects with parental care.     

Darwin's Finch Begging Intensity Does Not Honestly Signal Need in Parasitised Nests

Parental care should be selected to respond to honest cues that increase offspring survival. When offspring are parasitised, the parental food compensation hypothesis predicts that parents can provision extra food to compensate for energy loss due to parasitism. Chick begging behaviour is a possible mechanism to solicit increased feeding from attending parents. We experimentally manipulated parasite intensity from Philornis downsi in nests of Darwin's small ground finch (Geospiza fuliginosa) to test its effects on chick begging intensity and parental food provisioning. We used in‐nest video recordings of individually marked chicks to quantify nocturnal parasite feeding on chicks, subsequent diurnal chick begging intensity and parental feeding care. Our video analysis showed that one chick per brood had the highest parasite intensity during the night (supporting the tasty chick hypothesis) and weakest begging intensity during the day, which correlated with low parental care and rapid death. We observed sequential chick death on different days rather than total brood loss on a given day. Our within‐nest video images showed that (1) high nocturnal larval feeding correlated with low diurnal begging intensity and (2) parent birds ignored weakly begging chicks and provisioned strongly begging chicks. Excluding predation, all parasite‐free chicks survived (100% survival) and all parasitised chicks died in the nest (100% mortality). Weak begging intensity in parasitised chicks, which honestly signalled recent parasite attack, was not used as a cue for parental provisioning. Parents consistently responded to the strongest chick in both parasitised and parasite‐free nests.     

Patient Parents: Do Offspring Decide on the Timing of Fledging in Zebra Finches?

Parent–offspring conflict over parental care is predicted to become most pronounced during offspring transition to independence when offspring are predicted to attempt to extend care for longer than parents are selected to provide it. However, on the proximate level, it is difficult to determine who plays the most important role in this process, parents or offspring. For several vertebrate taxa, it has been documented that parents end brood care by abandoning offspring after a fixed period or else show high flexibility in the duration of care, but teasing apart the role of offspring and parents underlying this flexibility has been difficult. Here, we studied the decision to fledge in captive zebra finches (Taeniopygia guttata), an altricial songbird. We experimentally delayed the time of fledging to determine who decides about the end of feeding inside the nest, parents or offspring. The experiment indicates that parents do not primarily rely on phenotypic offspring traits in their decision to feed offspring in the nest, but appear to adjust the duration of parental care as long as offspring are in the nest which parents may take as an indicator of offspring need and locomotor abilities. Delayed‐fledging offspring appeared not to suffer a disadvantage in terms of age at the onset of independent feeding. Our study suggests that, in zebra finches, offspring play a major role in determining the time of fledging and leave the nest on their own, possibly to reduce the risk of nest predation, or to evade sibling competition in the nest.     

Parental Care Syndromes in House Sparrows: Positive Covariance Between Provisioning and Defense Linked to Parent Identity

Parents of many species provide multiple forms of care to their offspring. In many birds, parents often provision offspring with food and defend them from predators and/or nest‐site competitors. We tested how these two forms of parental care covary in a wild population of house sparrows (Passer domesticus). Using a behavioral reaction norm approach, we found that nestling provisioning exhibited between individual differences and positively covaried with a measure of nest defense: the propensity to attack a heterospecific nest box competitor, the European starling (Sturnis vulgaris). This result would seem to support parental investment theory and suggests that high‐provisioning parents have high‐value offspring, which they will defend more vigorously than low‐provisioning parents. In addition, we found that parents with nestlings that hatched earlier in the season and grew faster approached a model starling more frequently and tended to be more likely to strike the starling. However, we also found that although brood value explained significant variation in both nestling provisioning and nest defense, it did not eliminate the positive, between‐individual relationship between provisioning and defense. This suggests that some of the correlation between provisioning and defense is tied to individual identity and hence may be a behavioral syndrome in which differences between individuals in underlying attributes produce correlated behaviors.     

A comparison of life‐history and parental care in temperate and tropical wrens

Comparing closely related species that live in different environments is a powerful way to understand selective pressures that influence life‐history evolution. We examined a suite of life‐history traits and parental care in neotropical buff‐breasted wrens Cantorchilus leucotis and north‐temperate Carolina wrens Thryothorus ludovicianus (Family Troglodytidae), to test hypotheses about life‐history evolution. As expected, buff‐breasted wrens exhibited smaller clutch sizes and higher annual adult survival than Carolina wrens. We found minimal support for the nest predation hypothesis, as nest survival and age‐corrected provisioning rates to whole broods were similar between species, and number of breeding attempts and breeding season length were greater in temperate wrens. Critical predictions of the food limitation hypothesis were not supported; in particular age‐corrected provisioning rates per nestling were higher in the tropical than temperate species. The adult survival and offspring quality hypothesis garnered the most support, as buff‐breasted wrens exhibited greater age‐corrected provisioning rates per nestling, a longer nestling period, longer re‐nesting intervals following nest success, and lower annual fecundity than Carolina wrens. Despite similarly prolonged breeding seasons, reproductive strategies differ between species with buff‐breasted wrens investing considerably in single broods to optimize first‐year survival and Carolina wrens investing in multiple small broods to optimize annual fecundity.     

Parental care influences social immunity in burying beetle larvae

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Asynchronous hatching provides females with a means for increasing male care but incurs a cost by reducing offspring fitness

In species with biparental care, sexual conflict occurs because the benefit of care depends on the total amount of care provided by the two parents while the cost of care depends on each parent's own contribution. Asynchronous hatching may play a role in mediating the resolution of this conflict over parental care. The sexual conflict hypothesis for the evolution of asynchronous hatching suggests that females adjust hatching patterns in order to increase male parental effort relative to female effort. We tested this hypothesis in the burying beetle Nicrophorus vespilloides by setting up experimental broods with three different hatching patterns: synchronous, asynchronous and highly asynchronous broods. As predicted, we found that males provided care for longer in asynchronous broods whereas the opposite was true of females. However, we did not find any benefit to females of reducing their duration of care in terms of increased lifespan or reduced mass loss during breeding. We found substantial negative effects of hatching asynchrony on offspring fitness as larval mass was lower and fewer larvae survived to dispersal in highly asynchronous broods compared to synchronous or asynchronous broods. Our results suggest that, even though females can increase male parental effort by hatching their broods more asynchronously, females pay a substantial cost from doing so in terms of reducing offspring growth and survival. Thus, females should be under selection to produce a hatching pattern that provides the best possible trade‐off between the benefits of increased male parental effort and the costs due to reduced offspring fitness.