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.     

Guppies control offspring size at birth in response to differences in population sex ratio

Females that invest adaptively in their offspring are predicted to channel more resources to the sex that will be at an advantage in the prevailing environmental conditions. Here, we report, for the first time, that female Trinidadian guppy, Poecilia reticulata, respond in reproductively distinct ways when faced with differences in operational sex ratio. We show that females assigned to a female‐biased sex ratio produce larger male offspring than females in an environment in which males predominate. Given the link between size at birth and fitness, and the marked reproductive skew in this species, larger male offspring are expected to have reproductive advantages in guppy populations with an excess of females. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 414–419.     

Seasonal change in offspring sex and size in Dawson's burrowing bees (Amegilla dawsoni) (Hymenoptera: Anthophorini)

Abstract.  1. Nesting females of Dawson's burrowing bees, Amegilla dawsoni , produce a large size class of offspring, which includes daughters and major sons, and a small size class, which consists entirely of minor sons averaging half the weight of their larger siblings. Female allocation patterns change over the flight season such that the initial pattern of producing daughters shifts toward the production of both daughters and major sons in the middle of the season, and then the production of primarily minor sons in the latter part of the nesting season.
2. In Dawson's burrowing bees, this pattern is correlated with declines in pollen and nectar availability as the nesting season progresses as well as a heightened risk of dying before the final brood cell is completed. Here, the relation between these factors and the provisioning tactics of nesting Dawson's burrowing bees is discussed.     

When mothers make sons sexy: maternal effects contribute to the increased sexual attractiveness of extra-pair offspring

Quality differences between offspring sired by the social and by an extra-pair partner are usually assumed to have a genetic basis, reflecting genetic benefits of female extra-pair mate choice. In the zebra finch (Taeniopygia guttata), we identified a colour ornament that is under sexual selection and appears to have a heritable basis. Hence, by engaging in extra-pair copulations with highly ornamented males, females could, in theory, obtain genes for increased offspring attractiveness. Indeed, sons sired by extra-pair partners had larger ornaments, seemingly supporting the genetic benefit hypothesis. Yet, when comparing ornament size of the social and extra-pair partners, there was no difference. Hence, the observed differences most likely had an environmental basis, mediated, for example, via differential maternal investment of resources into the eggs fertilized by extra-pair and social partners. Such maternal effects may (at least partly) be mediated by egg size, which we found to be associated with mean ornament expression in sons. Our results are consistent with the idea that maternal effects can shape sexual selection by altering the genotype-phenotype relationship for ornamentation. They also caution against automatically attributing greater offspring attractiveness or viability to an extra-pair mate's superior genetic quality, as without controlling for differential maternal investment we may significantly overestimate the role of genetic benefits in the evolution of extra-pair mating behaviour.     

The functions of societies and the evolution of group living: spider societies as a test case

Many models have been advanced to suggest how different expressions of sociality have evolved and are maintained. However these models ignore the function of groups for the particular species in question. Here we present a new perspective on sociality where the function of the group takes a central role. We argue that sociality may have primarily a reproductive, protective, or foraging function, depending on whether it enhances the reproductive, protective or foraging aspect of the animal's life (sociality may serve a mixture of these functions). Different functions can potentially cause the development of the same social behaviour. By identifying which function influences a particular social behaviour we can determine how that social behaviour will change with changing conditions, and which models are most pertinent. To test our approach we examined spider sociality, which has often been seen as the poor cousin to insect sociality. By using our approach we found that the group characteristics of eusocial insects is largely governed by the reproductive function of their groups, while the group characteristics of social spiders is largely governed by the foraging function of the group. This means that models relevant to insects may not be relevant to spiders. It also explains why eusocial insects have developed a strict caste system while spider societies are more egalitarian. We also used our approach to explain the differences between different types of spider groups. For example, differences in the characteristics of colonial and kleptoparasitic groups can be explained by differences in foraging methods, while differences between colonial and cooperative spiders can be explained by the role of the reproductive function in the formation of cooperative spider groups. Although the interactions within cooperative spider colonies are largely those of a foraging society, demographic traits and colony dynamics are strongly influenced by the reproductive function. We argue that functional explanations help to understand the social structure of spider groups and therefore the evolutionary potential for speciation in social spiders.     

Pollen use by Megalopta sweat bees in relation to resource availability in a tropical forest

1. Spatial and temporal availability of pollen helps shape bee foraging behaviour and productivity, which has been studied in great detail at the landscape level, but never in a diverse tropical forest. 2. To study the effect of spatio‐temporal variation in resource distribution on pollen use and productivity, we identified pollen from spatially explicit nest collections of two generalist sweat bees, Megalopta genalis Meade‐Waldo and M. centralis Friese, from Barro Colorado Island, Panama, a 50‐ha forest dynamics plot during the 2007 dry and early wet seasons. Pollen from nests collected in 1998–1999 without spatial information was also identified. 3. Bees used pollen of at least 64 species; many of these occurred in only one collection. The 2007 collections contained pollen of 35 different species, but were dominated by five species, especially Hura crepitans L. and Pseudobombax septenatum (Jacq.) Dugand. 4. Temporal availability, but not distance from nest, influenced flower use at a 50‐ha scale. 5. Body size was not associated with minimum flight distance as inferred from pollen collections. 6. Nest productivity and pollen diversity decreased from the dry to wet seasons, mirroring community‐level availability of floral resources. 7. Results suggest that on a scale of 50 ha, bees are choosing certain host plant species regardless of distance from the nest, but adjusting foraging behaviour opportunistically based on the temporal availability of host flowers.     

Selective Foraging Behavior in Nest-Provisioning Females of Parastrachia japonensis (Hemiptera: Cydnidae): Cues for Preferred Food

Females of Parastrachia japonensis (Hemiptera: Cydnidae) provision nymph-containing nests with drupes of the single host tree, Schoepfia jasminodora (Rosidae: Santales). P. japonensis feeds on the endosperm of these drupes. Foraging females approached and accepted only a few selected drupes for transport to their nests from among the hundreds of drupes scattered on the ground. The characteristics of the drupes that elicited an acceptance response under field conditions were examined. Females estimated the degree of endosperm development using volatile and nonvolatile chemicals in the outer skin as cues and selected only those drupes which had a well-developed endosperm. Although the cues that prompted approach and inspection of a drupe are in the fleshy outer skin, females presented with various substitute drupes coated with outer skin juices of acceptable drupes selected only those they could recognize as a solid mass, suggesting that they used volatile chemicals in the outer skin as cues for approaching and inspecting a drupe and then taste and tactile stimuli as cues for acceptance. Thus, this bug possesses a complex, ecologically sensitive cognitive system that enables it to recognize valuable food items by using reliable cues. The importance of selective foraging by P. japonensis females and the evolutionary significance of this behavior are discussed.     

Transgenerational effects of parent and grandparent gender on offspring development in a biparental beetle species

Parental effects on offspring life-history traits are common and increasingly well-studied. However, the extent to which these effects persist into offspring in subsequent generations has received less attention. In this experiment, maternal and paternal effects on offspring and grand-offspring were investigated in the biparental burying beetle Nicrophorus vespilloides, using a split-family design. This allowed the separation of prenatal and postnatal transgenerational effects. Grandparent and parent gender were found to have a cumulative effect on offspring development and may provide a selection pressure on the division of parental investment in biparental species.     

Flexible responses to stage‐specific offspring threats

When caring for their young, parents must compensate for threats to offspring survival in a manner that maximizes their lifetime reproductive success. In birds, parents respond to offspring threats by altering reproductive strategies throughout the breeding attempt. Because altered reproductive strategies are costly, when threats to offspring are limited, parents should exhibit a limited response. However, it is unclear if response to offspring threat is the result of an integrated set of correlated changes throughout the breeding attempt or if responses are a flexible set of dissociable changes that are stage‐specific. We test these hypotheses in a system where house wrens (Troglodytes aedon) compete for nesting cavities with Carolina chickadees (Poecile carolinensis) by usurping and destroying their nests during the early stage of the breeding attempt (the egg stage). Due to the specificity of the house wren threat, we can test whether parental responses to an offspring threat show flexibility and stage specificity or if parental strategies are an integrated and persistent response. We monitored nests in a natural population to compare life history traits of chickadees nesting in boxes that were in the presence of house wrens to chickadees nesting in boxes that did not overlap with house wrens. Carolina chickadees that nested near house wrens laid significantly smaller clutch sizes (early change in reproductive strategy) but did not alter nestling provisioning or nestling stage length (late change in reproductive strategy), suggesting that chickadees respond in a flexible and stage‐specific manner to the threat of house wrens. By responding only when a threat is highest, parents minimize the cost of antithreat responses. Our study suggests that parents can respond in subtle and nuanced ways to offspring threats in the environment and specifically alter reproductive behaviors at the appropriate stage.     

Maternal behavior regulates long-term hippocampal expression of BAX and apoptosis in the offspring

Naturally occurring variations in maternal care influence hippocampal development in the rat. In the present study we found that variations in maternal licking/grooming (LG) during the first week of life are associated with altered hippocampal expression of BAX (group-1 tumor necrosis factor family mediated cell death effector) in 90-day-old male offspring. BAX-like immunoreactivity on western blots is significantly increased in the adult offspring of low-level LG mothers. There is no effect of maternal care on levels of either B-cell lymphoma-2 (BCL-2) (group-II mitochondria mediated cell death suppressor) or BAD (group-III endoplasmic reticulum mediated cell death effector). The most striking biochemical event in apoptosis is DNA fragmentation. Terminal deoxynucleotidyl transerferase (Tdt)-mediated dUTP-biotin nick-end labeling (TUNEL) and 4',6'-diamidino-2-phenylindole hydrochloride (DAPI) staining showed that the number of TUNEL-positive cells in both the dentate gyrus and CA1 region of the hippocampus is significantly increased in the adult offspring of low-level LG mothers. In conclusion, we propose that hippocampal neurons in the offspring of low-level LG mothers may be more vulnerable to loss through apoptosis.     

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.     

Selfish mothers: reproductive expenditure and resource availability in bighorn ewes

We present a marginal value model explaining intraspecific andinterspecific variation of mating systems in nonterritorialungulates. The model takes into account the simultaneous effectsof spatial and temporal distribution of females, female groupsize, male-male competition, female choice, and the operationalsex ratio (i.e., the proportion of estrous females). The modelpredicts that higher numbers of females per group increasesthe average exploitation time of such groups by males. An increasein female group density, operational sex ratio, and age-specificfighting success of males are predicted to reduce the averageexploitation time of female groups, leading to roving of males(i.e., moving between female groups). In contrast, an increasein die female rejection rate of males and in the time spentby males on nonmating activities (i. e., foraging, lying down,ruminating, migrating) are predicted to increase the averageexploitation time of female groups and to favor staying behaviorof males (i.e., defending a female group over a longer periodof time). Consequently, die model predicts that young maleswill tend to be "stayers," whereas middle-aged and old malesare expected to be "rovers." Model predictions were tested widifield data collected on muskoxen Ovibos moschatus in a naturalpopulation in west Greenland. Observed correlations betweenbull exploitation times of cow groups and the six above-mentionedsocial and environmental parameters were all in die predicteddirection and statistically significant in five of die six cases.Overall, 69% of die observed variation in exploitation timeof cow groups by males was explained by die model predictions.Stepwise regression suggested that, of die six parameters, variationin sex ratio (R² = .56) and time spent on nonmating activities(R² = .35) had the largest effects on male exploitation time.Also, die observed age-specific variation in bull exploitationtime of cow groups was as predicted.     

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.     

Big mothers invest more in daughters – reversed sex allocation in a weakly polygynous mammal

How mothers allocate resources to offspring is central to understanding life history strategies. High quality mothers are predicted to favour investment in sons over daughters when to do so increases inclusive fitness. This is the case in ungulates with polygynous mating systems, where reproductive success is more variable among males than females, but information is scarce on sex allocation in less polygynous species. Here, for the weakly dimorphic roe deer, we show that as maternal capacity to invest increases, mothers increase allocation to daughters more than to sons, so that relative allocation to daughters increases markedly with increasing maternal quality. This cannot be explained by a between sex difference in growth priority, hence we conclude that this is evidence for active maternal discrimination. Further, we demonstrate that condition differences between offspring persist to adulthood. For high quality mothers of weakly polygynous species, daughters may be more valuable than sons.     

Regulation of nectar collection in relation to honey storage levels by honey bees, Apis mellifera

Honey bees collect distinct nutrient sources in the form ofnectar (energy) and pollen (nitrogen). We investigated the effectof varying energy stores on nectar and pollen foraging. We foundno significant changes in nectar foraging in response to changesin honey storage levels within colonies. Individual foragersdid not vary activity rates or nectar load sizes in responseto changes in honey stores, and colonies did not increase nectarintake rates when honey stores within the hive were decreased.This result contrasts with pollen foraging behavior, which isextremely sensitive to colony state. Our data show that individualforaging decisions during nectar collection and colony regulationof nectar intake are distincdy different from pollen foraging.The behavior of honey bees illustrates that foraging strategy(and therefore foraging models) can incorporate multiple currencies,including both energy and protein intake.[Behav Ecol 7: 286–291(1996)]     

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.     

Maternal and paternal effects on offspring phenotype in the dung beetle Onthophagus taurus

Abstract.— Parents often have important influences on the development of traits in their offspring. One mechanism by which parents are able to influence offspring phenotype is through the level of care they provide. In onthophagine dung beetles, parents typically provision their offspring by packing dung fragments into a brood mass. Onthophagus taurus males can be separated into two discrete morphs: Large, "major" males have head horns, whereas "minor" males are hornless. Here we show that a switch in parental provisioning strategies adopted by males coincides with the switch in male morphology. Male provisioning results in the production of heavier brood masses than females will produce alone. However, unlike females in which the level of provisioning increases with body size in a continuous manner, the level of provisioning provided by males represents an "all-or-none" tactic with all major males providing a fixed level of provisioning irrespective of their body size. Offspring size is determined largely by the quantity of dung provided to the developing larvae so that paternal and maternal provisioning affects the body size and horn size of offspring produced. The levels of provisioning by individual parents are significantly repeatable, suggesting paternal and maternal effects as candidate indirect genetic effects in the evolution of horn size in the genus Onthophagus .     

Maternal effects in Daphnia: what mothers are telling their offspring and do they listen?

Maternal effects can significantly impact offspring performance. Provisioning of offspring with energy stores can quantitatively alter their growth rates, survivorship, and future fecundity, and influence population regulatory mechanisms. In this paper, we show that maternal effects can also qualitatively affect offspring reproduction (i.e. their mode of reproduction). The freshwater herbivore Daphnia pulex can change the amount of energy allocated between asexual and ephippial egg production. Our experiments on individuals, experiencing “step‐up” or “step‐down” food manipulations, reveal that offspring qualitatively shift their energy allocation away from asexual reproduction to ephippial egg production when there is a simple mismatch between maternal and offspring food environments. We show that the response is asymmetric with respect to changes in food level, ephippial egg production is higher with a greater mismatch between environments, and that the effect can be observed in dynamic experimental populations. These results point to a “generational memory” that could challenge our interpretation of field patterns and mechanisms influencing population dynamics in Daphnia–algal systems.