Brood ball size but not egg size correlates with maternal size in a dung beetle,Onthophagus atripennis

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A cost of maternal care in the dung beetle Onthophagus taurus?

Parental care theory assumes that investment in current offspring will trade against future investment. A number of field studies on birds have used clutch size manipulations to demonstrate a survival cost to chick rearing. However, such studies do not account for costs accrued during earlier stages of reproduction because not all aspects of reproductive effort are manipulated by varying the number of nestlings. In this study, we investigate the effect of reproductive effort on female survival in the dung beetle, Onthophagus taurus. By experimentally manipulating mating status and dung availability, we demonstrate that virgin females survive longer than mated females and that the survival of mated females was negatively associated with the number of brood masses produced. Using a novel manipulation of the mating system, we separated the effects of egg production and maternal care on female survival. Previously, we have shown that females provisioning with the assistance of a major male provide relatively less care than unassisted females. However, paternal assistance did not alter the number of brood masses produced and hence the amount of reproductive effort that was allocated to egg production. Therefore, our finding that female survival was increased when receiving paternal assistance provides, to our knowledge, the first definitive evidence that maternal care reduces female lifespan. These results are of major importance to theoretical models on the evolution of parental care.     

Behavioural dynamics of biparental care in the dung beetle Onthophagus taurus

In the dimorphic dung beetle Onthophagus taurus major males provide assistance during offspring provisioning. We examined the behavioural dynamics of biparental care to quantify directly how males and females allocate time to parental and nonparental behaviours and to determine whether parents adjust their level of investment relative to their partner's contribution. Females allocated more of their time budget to parental behaviours than males. The proportion of time females allocated to parental behaviours increased after oviposition while that of a male decreased. Male paternity assurance behaviours were negatively associated with male and female parental behaviours. Theoretical models predict that the investment provided by the members of a cooperative pair should be negatively correlated and that any shortfall of one parent should be partially compensated for by the other. In the absence of a male, unassisted females allocated more time to parental care, and performed more parental behaviours. However, compensation was incomplete as unassisted females performed fewer parental behaviours than pairs, resulting in significantly lighter brood masses (the egg and its associated dung supply). Males performed more parental behaviours when paired with small females, and small females more than large females. Contrary to prediction, the investments provided by males and females in a cooperative pair were positively correlated. Males coordinated their parental behaviours with the females rather than acting independently. Since parental behaviours were directly related to the weight of brood masses, the observed parental interactions will have important fitness consequences in this species. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Maternal effects on male weaponry: female dung beetles produce major sons with longer horns when they perceive higher population density

ABSTRACT: BACKGROUND: Maternal effects are environmental influences on the phenotype of one individual that are due to the expression of genes in its mother, and are expected to evolve whenever females are better capable of assessing the environmental conditions that their offspring will experience than the offspring themselves. In the dung beetle Onthophagus taurus, conditional male dimorphism is associated with alternative reproductive tactics: majors fight and guard females whereas minors sneak copulations. Furthermore, variation in dung beetle population density has different fitness consequences for each male morph, and theory predicts that higher population density might select for a higher frequency of minors and/or greater expenditure on weaponry in majors. Because adult dung beetles provide offspring with all the nutritional resources for their development, maternal effects strongly influence male phenotype. RESULTS: Here we tested whether female O. taurus are capable of perceiving population density, and responding by changing the phenotype of their offspring. We found that mothers who were reared with other conspecifics in their pre-mating period produced major offspring that had longer horns across a wider range of body sizes than the major offspring of females that were reared in isolation in their pre-mating period. Moreover, our results indicate that this maternal effect on male weaponry does not operate through the amount of dung provided by females to their offspring, but is rather transmitted through egg or brood mass composition. Finally, although theory predicts that females experiencing higher density might produce more minor males, we found no support for this, rather the best fitting models were equivocal as to whether fewer or the same proportions of minors were produced. CONCLUSIONS: Our study describes a new type of maternal effect in dung beetles, which probably allows females to respond to population density adaptively, preparing at least their major offspring for the sexual competition they will face in the future. This new type of maternal effect in dung beetles represents a novel transgenerational response of alternative reproductive tactics to population density.     

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).     

The mother-in-law effect

Individuals often derive considerable evolutionary benefit from manipulating others. In the majority of cases, manipulation involves direct interactions between individuals. In the dung beetle, Onthophagus taurus, females mated with large males provide more resources to their offspring. Here, we demonstrate, however, that this may result in manipulation that extends across generations: the care that a mother provides to a developing son influences the parental effort of his mate (the mother's daughter-in-law (DIL)). Maternal care associated with constructing heavier brood masses has previously been shown substantially to influence offspring size, male mating success and female survival and fecundity in this species. The mother-in-law effect that we document here is, however, the ability to produce large sons from relatively lighter brood masses. Our results demonstrate not only that females are able to manipulate the parental effort of DILs that they do not directly encounter, but that provisioning relatively lighter brood masses may have evolutionary benefits that trade off against the considerable benefits of producing heavy brood masses.     

No fecundity cost of female secondary sexual trait expression in the horned beetle Onthophagus sagittarius

Typically males bear the products of sexual selection in the form of ornaments and/or weapons used to compete for and attract females. Secondary sexual traits in females have been thought of as the product of correlated responses to sexual selection on males. However, there is increasing phylogenetic evidence that female secondary sexual traits can arise independently of selection on males, and may be subject to sexual selection. Theoretical models of the evolution of female ornamentation via male mate choice have assumed that females suffer a cost of ornament expression via reduced fecundity, and hence female ornaments are less likely to evolve than male ornaments. In the dung beetle Onthophagus sagittarius, there has been an independent evolutionary origin of horns in females that are qualitatively different from the horns produced by males. We use this system as a model to examine the costs of horn expression for females within a life-history context. We identified a longevity cost of reproduction for females that was independent of horn expression. Large females lived longer, and after controlling for lifespan, had a higher lifetime fecundity, and invested more heavily in maternal provisioning than did small females. We found no evidence of a cost to females of investment in horns. Rather, the rate of increase in fecundity and horn expression with body size were equal, so that absolute horn size provides an accurate indicator of body size and maternal quality. The effects we observe were independent of female contest competition and/or male mate choice, which were excluded in our experimental protocol. However, we speculate on the potential functional contributions female horns might make to female fitness.     

Adjustment of Parental Investment in the Dung Beetle Onthophagus atripennis (Col., Scarabaeidae)

If parents can invest resources optimally per offspring, they should adjust the amount of investment in an offspring according to environmental heterogeneity. Many studies have demonstrated changes in egg size or the amount of resource supplied in response to environmental heterogeneity. However, it remains unclear whether parents simply know the resource type a priori or can assess resource quality and adjust the quantity of investment accordingly. We examined the parental capability to adjust the amount of investment per offspring by providing Onthophagus atripennis dung beetle parents with one of three dung types of different quality: monkey dung (high quality), cow dung (low quality), or a mixture of monkey and cow dung (medium quality). The beetle parents cooperatively produce dung brood masses each with one egg under the ground. The size of a brood mass, on which a larva can only feed until adult, represents a large part of the amount of investment. Parents produced a greater number of smaller brood masses given high‐quality resource, while they compensated for low quality of the resource by providing a larger amount of the resource, at the cost of offspring number. However, despite this compensation in the amount of food, offspring raised on low‐quality food was still smaller than offspring raised on high‐quality food. Thus, O. atripennis parents assessed resource quality partly and adjusted the amount of resource provided for their offspring.     

Maternal investment tactics in superb fairy-wrens

In cooperatively breeding species, parents often use helper contributions to offspring care to cut their own costs of investment (i.e. load-lightening). Understanding the process of load-lightening is essential to understanding both the rules governing parental investment and the adaptive value of helping behaviour, but little experimental work has been conducted. Here we report the results of field experiments to determine maternal provisioning rules in cooperatively breeding superb fairy-wrens (Malurus cyaneus). By manipulating carer: offspring ratios, we demonstrate that helpers allow females to reduce the rate at which they provision their brood. Female reductions, however, were less than that provided by helpers, so that chicks still received food at a faster rate in the presence of helpers. Despite this, chicks fed by parents and helpers were not heavier than those provisioned by parents alone. This is because maternal load-lightening not only occurs during the chick provisioning stage, but also at the egg investment stage. Theoretically, complete load-lightening is predicted when parents value themselves more highly than their offspring. We tested this idea by 'presenting' mothers with a 'choice' between reducing their own levels of care and increasing investment in their offspring. We found that mothers preferred to cut their contributions to brood care, just as predicted. Our experiments help to explain why helper effects on offspring success have been difficult to detect in superb fairy-wrens, and suggest that the accuracy with which theoretical predictions of parental provisioning rules are matched in cooperative birds depends on measuring maternal responses to helper presence at both the egg and chick stages.     

Why make daughters larger? Maternal sex-allocation and sex-dependent selection for body size in a mass-provisioning wasp, Trypoxylon politum

Mass-provisioning wasps package maternal investment into broodcells, sealed structures that contain all the provisions necessaryfor an offspring's growth and development. Optimal sex-allocationtheory predicts that if maternal provisions determine the sizeof each offspring, and the amount of provisions available toeach offspring varies, females should allocate well-stockedbrood cells to the sex that benefits most from being large.I tested this hypothesis using observations of organ-pipe wasps,Trypoxylon politum, and dissections of their nests. A Mississippipopulation of T. politum was intensively studied from 1993 to1995. This population fit the assumptions of optimal sex-allocationmodels by Green and Brockmann and Grafen. Female weight at emergencewas 1.29 times that of males, and wing length was 1.15 timesthat of males. This discrepancy in size occurred because thevolume of parental provisions strongly influenced adult bodysize, and better-stocked brood cells were preferentially allocatedto daughters. Brood-cell volume correlated with both wing lengthand weight at emergence in both sexes, and the chance that agiven brood cell contained a female offspring increased withincreasing brood-cell volume. Fitness was positively relatedto body size for females, but I found no evidence of an advantageto large males. Although there was evidence of stabilizing selectionfor male wing length in one year, there was no evidence of anincreasing relationship between body size and fitness (directionalselection) for males in either 1993 or 1994. Female fecunditywas positively related to body size in both years, indicatingthat larger females have increased reproductive success. Therate at which females provisioned brood cells was also correlatedwith body size. Observed patterns of investment in brood cellsare quantitatively consistent with the predictions of optimalsex-allocation theory, but certain aspects of female provisioningbehavior suggest females are not following a single "optimal"strategy. Patterns of provisioning were variable among differentfemales at the study site during the same year. Large femalestended to produce larger offspring. Although Brockmann and Grafen'smodel predicts a single, population wide "switchpoint" fromthe production of male to female offspring, there was no evidencefor such a switchpoint     

Male and female secondary sexual traits show different patterns of quantitative genetic and environmental variation in the horned beetle Onthophagus sagittarius

The expression of secondary sexual traits in females has often been attributed to a correlated response to selection on male traits. In rare cases, females have secondary sexual traits that are not homologous structures to secondary sexual traits in males and are thus less likely to have evolved in females because of correlated selection. In this study, we used the dung beetle Onthophagus sagittarius, a species with sex‐specific horns, to examine the environmental and quantitative genetic control of horn expression in males and females. Offspring subjected to different brood mass manipulations (dung addition/removal) were found to differ significantly in body size. Brood mass manipulation also had a significant effect on the length of male horns; however, female horn length was found to be relatively impervious to the treatment, showing stronger patterns of additive genetic variance than males. We found no correlations between horn expression in males and females. We therefore conclude that the horns of O. sagittarius females are unlikely to result from genetic correlations between males and females. Rather, our data suggest that they may be under independent genetic control.     

Parental differences in brood provisioning by Hen Harriers Circus cyaneus

Capsule Females varied their provisioning patterns according to brood age and brood size, whereas males did not.

Aims To quantify how parents balance the needs of their offspring for food and protection.

Methods We studied 13 nests from hides and spent on average 101 hours per nest monitoring prey types, provisioning rate and the time spent at the nest by both sexes in relation to brood size and brood age.

Results Males always provided more food than females. Males brought similar amounts of prey items irrespective of brood size and nestling age, whereas females brought more prey and bigger items to larger and older broods. Females spent less time brooding larger broods, particularly early on.

Conclusions Hen Harrier parents share the provisioning burden, with each parent delivering prey as a function of brood care requirements, hunting capability and the behaviour of the other parent.     

Males influence maternal effects that promote sexual selection: a quantitative genetic experiment with dung beetles Onthophagus taurus

Recently, doubt has been cast on studies supporting good genes sexual selection by the suggestion that observed genetic benefits for offspring may be confounded by differential maternal allocation. In traditional analyses, observed genetic sire effects on offspring phenotype may result from females allocating more resources to the offspring of attractive males. However, maternal effects such as differential allocation may represent a mechanism promoting genetic sire effects, rather than an alternative to them. Here we report results from an experiment on the horned dung beetle Onthophagus taurus, in which we directly compare genetic sire effects with maternal effects that are dependent on sire phenotype. We found strong evidence that mothers provide more resources to offspring when mated with large-horned males. There were significant heritabilities for both horn length and body size, but when differential maternal effects were controlled, the observed estimates of genetic variance were greatly reduced. Our experiment provides evidence that differential maternal effects may amplify genetic effects on offspring traits that are closely related to fitness. Thus, our results may partly explain the relatively high coefficients of additive genetic variation observed in fitness-related traits and provide empirical support for the theoretical argument that maternal effects can play an important role in evolution.     

The Nesting Behavior of Dawson's Burrowing Bee, Amegilla dawsoni (Hymenoptera: Anthophorini), and the Production of Offspring of Different Sizes

Females of Dawson's burrowing bees have a well-defined brood cell cycle involving cell construction, waxing, provisioning, egg laying, and cell capping. In one study population, nesting bees built smaller brood cells for offspring of lower weight and larger ones for heavier offspring, demonstrating their ability to anticipate the desired size of an offspring at the outset of a brood cell cycle. Furthermore, individual females varied the number of provisioning trips made per brood cell cycle by a factor of two or more, apparently exercising control over the amount of brood provisions supplied to an offspring. The size distribution of emerging males at two widely separated locations in 1997 was nearly identical to that recorded in 1995. These findings suggest that the production of small males (minors) is the result of active female control rather than the product of food shortages that force females to undersupply some brood cells. Female foraging decisions resulted in a bimodal distribution of weights of mature dormant larvae at one site in 1997. However, the times required to complete brood cell cycles at this site were not distributed bimodally. This result stemmed in part from daily variation among females in the duration of their provisioning trips as well as from seasonal variation in provisioning trip times. When provisioning trips lasted longer, females tended to make fewer trips per brood cell cycle, and so were presumably more likely to produce minor sons. As a result, the weight of an offspring was not tightly linked to the time investment required to produce it, making it difficult to compare the relative costs of minors and majors in terms of maternal time investments.     

Providing chicks with extra food lowers male but not female provisioning in the House Sparrow Passer domesticus

We assessed whether adult House Sparrows Passer domesticus adjusted their provisioning in response to an experimental increase in the nutritional condition of their nestlings. When we supplemented chicks directly with additional food, male parents, but not female parents, reduced their provisioning. The results for males, but not females, run contrary to a previous experiment in this species. In addition, female provisioning was positively associated with both brood size and the age of the brood. In contrast, whereas male provisioning was positively associated with brood size, males did not increase provisioning as their chicks grew older. Males, but not females, exhibited repeatability in their provisioning. Food supplementation had a larger positive effect upon nestling survival in smaller broods than in larger broods. Overall, there appear to be fundamental differences between males and females in how decisions regarding the level of parental investment in the current brood are made.     

Intraspecific female brood parasitism in the dung beetle Onthophagus taurus

Abstract.  1. Brood parasitism occurs when individuals parasitise each others' investment into parental care, and has been documented primarily as an interspecific interaction. Intraspecific brood parasitism, in contrast, is often difficult to detect and quantify, and evidence for it is comparatively scarce. The present study documents the occurrence of intraspecific brood parasitism by females of the tunnelling dung beetle Onthophagus taurus , and investigates the contributions of two variables to the propensity of female brood parasitism: female body size and dung desiccation rate.
2. Female O. taurus were found to routinely utilise brood balls made by conspecific females as food provisions for their own offspring.
3. Contrary to expectations, large and small females did not differ in the likelihood of engaging in brood-parasitic behaviour.
4. Dung desiccation rate appeared to influence likelihood of brood parasitism. Females that were given access to rapidly drying dung were significantly more likely to detect and utilise brood balls produced by conspecific females.
5. While interspecific brood parasitism has been documented in dung beetles before, the present study is among the first to present evidence for intraspecific brood parasitism as an alternative reproductive tactic of female dung beetles. Results are discussed in the context of the evolutionary ecology of onthophagine beetles.     

Unravelling the effects of differential maternal allocation and male genetic quality on offspring viability in the dung beetle, Onthophagus sagittarius

Good genes models of mate choice assume heritability of fitness-related traits. However, maternal effects can inflate estimates of trait heritability, and genotype-environment interactions can have significant effects on good genes processes of evolution. Thus, partitioning genetic and maternal/environmental sources of variation in studies of good genes mate choice represents an empirical challenge. In this study, we used the dung beetle Onthophagus sagittarius to examine additive genetic and maternal effects on egg-to-adult offspring viability. We used a half-sib full-sib breeding design and manipulated the maternally provided environment by reducing or increasing the mass of the brood ball within which each offspring developed. We found evidence of differential allocation of investment by females in the brood balls they produced. However, experimental manipulations of maternal allocation to brood balls had only a weak and non-significant influence on the sire effects on offspring viability. Significant additive genetic effects on offspring viability were pervasive across our manipulations of the maternally provided larval environment. This finding indicates that although females do show differential allocation to offspring based on sire phenotype, ‘good genes’ benefits of mate choice are not dependent upon differential maternal allocation.     

Maternal and paternal condition effects on offspring phenotype in Telostylinus angusticollis (Diptera: Neriidae)

It is widely recognized that maternal phenotype can have important effects on offspring, but paternal phenotype is generally assumed to have no influence in animals lacking paternal care. Nonetheless, selection may favour the transfer of environmentally acquired condition to offspring from both parents. Using a split-brood, cross-generational laboratory design, we manipulated a key environmental determinant of condition - larval diet quality - of parents and their offspring in the fly Telostylinus angusticollis, in which there is no evidence of paternal provisioning. Parental diet did not affect offspring survival, but high-condition mothers produced larger eggs, and their offspring developed more rapidly when on a poor larval diet. Maternal condition had no effect on adult body size of offspring. By contrast, large, high-condition fathers produced larger offspring, and follow-up assays showed that this paternal effect can be sufficient to increase mating success of male offspring and fecundity of female offspring. Our findings suggest that both mothers and fathers transfer their condition to offspring, but with effects on different offspring traits. Moreover, our results suggest that paternal effects can be important even in species lacking conventional forms of paternal care. In such species, the transfer of paternal condition to offspring could contribute to indirect selection on female mate preferences.     

Sperm environment affects offspring quality in broadcast spawning marine invertebrates

The provisioning of offspring can have far-reaching consequences for later life in a wide range of organisms and generally this provisioning is thought to be under maternal influence or control. In experiments with a broadcast-spawning ascidian, we found that the size of offspring was determined by egg size and the abundance of sperm present during fertilization. Larger eggs were fertilized at low sperm concentrations, whilst smaller eggs were successfully fertilized at high sperm concentrations. These differences in fertilized egg size resulted in differences in the development rate, hatching success and mean size of the subsequent larvae. Our results suggest that, in contrast to females that reproduce by other mating systems, free-spawning mothers lack some control over the provisioning of offspring. Furthermore, because males can alter the sperm environment, they can exert paternal (non-genetic) control over key offspring characteristics.     

Duration and benefits of biparental brood care in the dung beetle Onthophagus vacca (Coleoptera: Scarabaeidae)

Abstract.

• 1 Single males, single females or pairs of dung beetles, Onthophagus vacca, were released on artificial small (100 g) or large (1000 g) dung pats in the laboratory. Emigrating beetles were trapped at 12 h intervals, and the number and size of the brood chambers were recorded after each replicate.
• 2 Emigration of males was delayed if females were present in the same dung pats, whereas emigration times of females were independent of the presence or absence of males.
• 3 A residency of 60 h proved to be a threshold value. Females emigrating before this time did not breed, whereas those emigrating later had built at least two brood chambers.
• 4 Females paired with males built more brood chambers than single females.
• 5 The reproductive success of pairs was not influenced by the size of the dung pats.