Interspecific Interactions and the Scope for Parent-Offspring Conflict: High Mite Density Temporarily Changes the Trade-Off between Offspring Size and Number in the Burying Beetle,Nicrophorus vespilloides

Parents have a limited amount of resources to invest in reproduction and commonly trade-off how much they invest in offspring size (or quality) versus brood size. A negative relationship between offspring size and number has been shown in numerous taxa and it underpins evolutionary conflicts of interest between parents and their young. For example, previous work on vertebrates shows that selection favours mothers that produce more offspring, at the expense of individual offspring size, yet favours offspring that have relatively few siblings and therefore attain a greater size at independence. Here we analyse how this trade-off is temporarily affected by stochastic variation in the intensity of interspecific interactions. We examined the effect of the mite Poecilochirus carabi on the relationship between offspring size and number in the burying beetle, Nicrophorus vespilloides. We manipulated the initial number of mites in the reproductive event (by introducing either no mites, 4 mites, 10 mites, or 16 mites), and assessed the effect on the brood. We found a similar trade-off between offspring size and number in all treatments, except in the ''16 mite'' treatment where the correlation between offspring number and size flattened considerably. This effect arose because larvae in small broods failed to attain a high mass by dispersal. Our results show that variation in the intensity of interspecific interactions can temporarily change the strength of the trade-off between offspring size and number. In this study, high densities of mites prevented individual offspring from attaining their optimal weight, thus potentially temporarily biasing the outcome of parent-offspring conflict in favour of parents.     

Differences in Patterns of Reproductive Allocation between the Sexes in Nicrophorus orbicollis

Organisms are selected to maximize lifetime reproductive success by balancing the costs of current reproduction with costs to future survival and fecundity. Males and females typically face different reproductive costs, which makes comparisons of their reproductive strategies difficult. Burying beetles provide a unique system that allows us to compare the costs of reproduction between the sexes because males and females are capable of raising offspring together or alone and carcass preparation and offspring care represent the majority of reproductive costs for both sexes. Because both sexes perform the same functions of carcass preparation and offspring care, we predict that they would experience similar costs and have similar life history patterns. In this study we assess the cost of reproduction in male Nicrophorus orbicollis and compare to patterns observed in females. We compare the reproductive strategies of single males and females that provided pre- and post-hatching parental care. There is a cost to reproduction for both males and females, but the sexes respond to these costs differently. Females match brood size with carcass size, and thus maximize the lifetime number of offspring on a given size carcass. Males cull proportionately more offspring on all carcass sizes, and thus have a lower lifetime number of offspring compared to females. Females exhibit an adaptive reproductive strategy based on resource availability, but male reproductive strategies are not adaptive in relation to resource availability.     

Environmental cues influence parental brood structure decisions in the burying beetle <Emphasis Type="Italic">Nicrophorus marginatus</Emphasis>

Parents evaluate multiple extrinsic and intrinsic cues when making decisions associated with reproduction. These decisions often reflect classic trade-offs between the cost of a strategy and its perceived fitness payoff. Life history theory predicts that when parents experience austere conditions, reproductive success is increased by producing fewer but larger offspring with a competitive advantage in this environment. Conversely, parents experiencing favorable conditions are expected to increase current reproductive success by favoring quantity over quality of offspring. We tested the predictions of life history theory using Nicrophorus marginatus (Coleoptera: Silphidae), a burying beetle species that exhibits infanticide during biparental care and hypervariable adult size across populations, by employing a factorial design that manipulated density and nutritional quality of food. We measured (1) the average number of offspring produced, (2) the average individual size of offspring, and (3) the sex ratio of the offspring. We found no effect of density or food quality on offspring sex ratio, but mean offspring size and number differed between low and high-density treatments. Nutritional environment interacted with density effects such that parents with access to high quality diets were able to modulate offspring size and number to match the perceived competitive environment, whereas those in poor nutritional condition appeared to exhibit physiological constraints to producing optimal brood structures.     

Effects of parental survival on clutch size decisions in fluctuating environments

Whereas in constant environments parental survival has no effect on optimal clutch size in the absence of trade-offs between juvenile and parental survival, the situation is drastically different in fluctuating environments. We consider a model in which, with respect to reproduction, parents and offspring are equivalent at the start of the next breeding season. When generations are non-overlapping, the clutch size maximizing geometric mean surviving number of offspring is optimal among all pure clutch size strategies. We prove that, as parental survival increases relative to that of the offspring, the optimal clutch size converges to the arithmetic mean maximizing clutch size (the so-called ‘Lack clutch size’). We also give a numerical procedure for calculating optimal mixed strategies and we show that, as environmental variance increases and/or parental survival decreases, mixed rather than pure strategies become optimal. Furthermore, we explain how to estimate fitness from empirical data under the assumptions of our model. This revised version was published online in July 2006 with corrections to the Cover Date.     

How optimal life history changes with the community size-spectrum

This paper derives optimal life histories for fishes or other animals in relation to the size spectrum of the ecological community in which they are both predators and prey. Assuming log-linear size-spectra and well known scaling laws for feeding and mortality, we first construct the energetics of the individual. From these we find, using dynamic programming, the optimal allocation of energy between growth and reproduction as well as the trade-off between offspring size and numbers. Optimal strategies were found to be strongly dependent on size spectrum slope. For steep size spectra (numbers declining rapidly with size), determinate growth was optimal and allocation to somatic growth increased rapidly with increasing slope. However, restricting reproduction to a fixed mating season changed optimal allocations to give indeterminate growth approximating a von Bertalanffy trajectory. The optimal offspring size was as small as possible given other restrictions such as newborn starvation mortality. For shallow size spectra, finite optimal maturity size required a decline in fitness for large size or age. All the results are compared with observed size spectra of fish communities to show their consistency and relevance.     

Gender Separation Increases Somatic Growth in Females but Does Not Affect Lifespan in Nothobranchius furzeri

According to life history theory, physiological and ecological traits and parameters influence an individual''s life history and thus, ultimately, its lifespan. Mating and reproduction are costly activities, and in a variety of model organisms, a negative correlation of longevity and reproductive effort has been demonstrated. We are employing the annual killifish Nothobranchius furzeri as a vertebrate model for ageing. N. furzeri is the vertebrate displaying the shortest known lifespan in captivity with particular strains living only three to four months under optimal laboratory conditions. The animals show explosive growth, early sexual maturation and age-dependent physiological and behavioural decline. Here, we have used N. furzeri to investigate a potential reproduction-longevity trade-off in both sexes by means of gender separation. Though female reproductive effort and offspring investment were significantly reduced after separation, as investigated by analysis of clutch size, eggs in the ovaries and ovary mass, the energetic surplus was not reallocated towards somatic maintenance. In fact, a significant extension of lifespan could not be observed in either sex. This is despite the fact that separated females, but not males, grew significantly larger and heavier than the respective controls. Therefore, it remains elusive whether lifespan of an annual species evolved in periodically vanishing habitats can be prolonged on the cost of reproduction at all.     

Coadaptation of prenatal and postnatal maternal effects

In a wide variety of species, a female's age of first reproduction influences offspring size and survival, suggesting that there exists an optimal timing of reproduction. Mothers in many species also influence offspring size and survival after birth through variation in parental care. We experimentally separated these effects in the burying beetle Nicrophorus vespilloides to test for coadaptation between prenatal and postnatal maternal effects associated with age at first reproduction. Females that reproduced early produced offspring with lower birth weight. The amount of parental care depended on the age of first reproduction of the caretaker, as did the extent of offspring begging. As predicted for a coadaptation of maternal effects, prenatal and postnatal effects were opposite for different-aged mothers, and larval weight gain and survival was greatest when the age of the caretaker and birth mother matched. Thus, prenatal effects intrinsically associated with age of first reproduction can be ameliorated by innate plasticity in postnatal care. A coadaptation of prenatal and postnatal maternal effects may evolve to allow variable timing of the first reproductive attempt. Such a coadaptation might be particularly valuable when females are constrained from reproducing at an optimal age, as, for example, in species that breed on scarce and unpredictable resources.     

Helpers at the nest improve late-life offspring performance: evidence from a long-term study and a cross-foster experiment

Background

Conditions during an individual''s rearing period can have far reaching consequences for its survival and reproduction later in life. Conditions typically vary due to variation in parental quality and/or the environment, but in cooperative breeders the presence of helpers adds an important component to this. Determining the causal effect of helpers on offspring fitness is difficult, since high-quality breeders or territories are likely to produce high-quality offspring, but are also more likely to have helpers because of past reproductive success. This problem is best resolved by comparing the effect of both helping and non-helping subordinates on offspring fitness, however species in which both type of subordinates commonly occur are rare.

Methodology/Principal Findings

We used multi-state capture-recapture models on 20 years of data to investigate the effect of rearing conditions on survival and recruitment in the cooperatively breeding Seychelles warbler (Acrocephalus sechellensis), with both helping and non-helping subordinates. The number of helpers in the rearing territory, but not territory quality, group- or brood size, was positively associated with survival of offspring in their first year, and later in life. This was not a result of group size itself since the number of non-helpers was not associated with offspring survival. Furthermore, a nestling cross-foster experiment showed that the number of helpers on the pre-foster territory was not associated with offspring survival, indicating that offspring from territories with helpers do not differ in (genetic) quality.

Conclusions/Significance

Our results suggest that the presence of helpers not only increase survival of offspring in their first year of life, but also subsequent adult survival, and therefore have important fitness consequences later in life. This means that when calculating the fitness benefits of helping not only short-term but also the late-life benefits have to be taken into account to fully understand the evolution of cooperative breeding.     

Effects of variation in resource acquisition during different stages of the life cycle on life‐history traits and trade‐offs in a burying beetle

Individual variation in resource acquisition should have consequences for life‐history traits and trade‐offs between them because such variation determines how many resources can be allocated to different life‐history functions, such as growth, survival and reproduction. Since resource acquisition can vary across an individual's life cycle, the consequences for life‐history traits and trade‐offs may depend on when during the life cycle resources are limited. We tested for differential and/or interactive effects of variation in resource acquisition in the burying beetle Nicrophorus vespilloides. We designed an experiment in which individuals acquired high or low amounts of resources across three stages of the life cycle: larval development, prior to breeding and the onset of breeding in a fully crossed design. Resource acquisition during larval development and prior to breeding affected egg size and offspring survival, respectively. Meanwhile, resource acquisition at the onset of breeding affected size and number of both eggs and offspring. In addition, there were interactive effects between resource acquisition at different stages on egg size and offspring survival. However, only when females acquired few resources at the onset of breeding was there evidence for a trade‐off between offspring size and number. Our results demonstrate that individual variation in resource acquisition during different stages of the life cycle has important consequences for life‐history traits but limited effects on trade‐offs. This suggests that in species that acquire a fixed‐sized resource at the onset of breeding, the size of this resource has larger effects on life‐history trade‐offs than resources acquired at earlier stages.     

Fitness of alternative modes of reproduction: developmental constraints and the evolutionary maintenance of sex

Parthenogenesis, including facultative parthenogenesis, is common among orthopteroid insects. We investigated the fitness associated with sexual and asexual reproduction within a population of the facultatively parthenogenetic cockroach Nauphoeta cinerea. There is significantly reduced fitness for females reproducing parthenogenetically compared to sexually. Fewer than half of all females can reproduce parthenogenetically. In addition, tenfold fewer offspring are produced by parthenogenesis due to reductions in both the number of offspring produced per clutch and the number of clutches produced. Development and brooding of sexually or parthenogenetically produced first instar nymphs does not differ, although the production of the first parthenogenetic clutch is delayed relative to the first sexually produced clutch. The fitness of parthenogens is also lower than the fitness of sexually produced offspring. Parthenogens are less viable than sexually produced offspring even in the benign conditions of the laboratory. Development to adulthood of parthenogens is slower. Fewer parthenogens survive to adulthood and the adult life span of parthenogens is reduced. Individuals produced by parthenogenetic reproduction are unlikely to reproduce parthenogenetically themselves. Finally, parthenogenetically produced females produce fewer offspring by sexual reproduction than do sexually produced females. Since parthenogenetic reproduction is apomictic in N. cinerea and parthenogens are diploid, we suggest that asexual reproduction is developmentally constrained. Once meiosis has evolved, returning to a mitotic mode of reproduction may be difficult. Nauphoeta cinerea offers a system for testing how asexuality is constrained as modes of reproduction can be compared within a facultative parthenogen.     

Size-number trade-off and optimal offspring size for offspring produced sequentially using a fixed amount of reserves

We analysed the nature of size-number trade-off of offspring when multiple cohorts of such offspring are produced sequentially using a fixed amount of reserves. In the model, we incorporated sink-limitation in the resource absorption rate of offspring from the mother tissue and the loss of resources by maintenance respiration. We found that the later the initiation of a cohort, the greater the cost of producing a cohort with the same size and number of offspring. This is due to the loss of resources by maintenance respiration during the period from the beginning of reproduction to the initiation of the cohort. Also, the extra cost increases with an increase in the specific maintenance respiration rate. Thus, resources lost to respiration over time reduces the fitness value of producing late cohorts. Hence, it is advantageous to produce all offspring simultaneously unless there are fitness advantages of producing offspring sequential which overcome this cost or constraints preventing simultaneous production. Sequentially offspring production evolves if there is a constraint on the number of offspring of each cohort. With this constraint, the optimal offspring size decreases with the production sequence of cohorts.     

Parasite resistance and parasite tolerance: insights into transgenerational immune priming in an invertebrate host

Parasites impose different selection regimes on their hosts, which respond by increasing their resistance and/or tolerance. Parental challenge with parasites can enhance the immune response of their offspring, a phenomenon documented in invertebrates and termed transgenerational immune priming. We exposed two parental generations of the model organism Daphnia magna to the horizontally transmitted parasitic yeast Metschnikowia bicuspidata and recorded resistance- and tolerance-related traits in the offspring generation. We hypothesized that parentally primed offspring will increase either their resistance or their tolerance to the parasite. Our susceptibility assays revealed no impact of parental exposure on offspring resistance. Nonetheless, different fitness-related traits, which are indicative of tolerance, were altered. Specifically, maternal priming increased offspring production and decreased survival. Grandmaternal priming positively affected age at first reproduction and negatively affected brood size at first reproduction. Interestingly, both maternal and grandmaternal priming significantly reduced within-host–parasite proliferation. Nevertheless, Daphnia primed for two consecutive generations had no competitive advantage in comparison to unprimed ones, implying additive maternal and grandmaternal effects. Our findings do not support evidence of transgenerational immune priming from bacterial infections in the same host species, thus, emphasizing that transgenerational immune responses may not be consistent even within the same host species.     

Warmer springs lead to mistimed reproduction in great tits (Parus major)

In seasonal environments, the main selection pressure on the timing of reproduction (the ultimate factor) is synchrony between offspring requirements and food availability. However, reproduction is initiated much earlier than the time of maximum food requirement of the offspring. Individuals should therefore start reproduction in response to cues (the proximate factors), available in the environment of reproductive decision making, which predict the later environment of selection. With increasing spring temperatures over the past decades, vegetation phenology has advanced, with a concomitant advancement in the reproduction of some species at higher trophic levels. However, a mismatch between food abundance and offspring needs may occur if changes in the environment of decision making do not match those in the environment of selection. Date of egg laying in a great tit (Parus major) population has not advanced over a 23-year period, but selection for early laying has intensified. We believe that this is the first documented case of an adaptive response being hampered because a changing abiotic factor affects the environment in which a reproductive decision is made differently from the environment in which selection occurs.     

Negative effects of habitat degradation and fragmentation on the declining grassland plant Trifolium montanum

Changes in land use have resulted in a strong decline in the plant diversity of nutrient-poor grasslands, but little is known about the combined effects of habitat degradation and fragmentation on populations of individual species. We studied these effects on stage structure, recruitment, reproduction and offspring fitness in populations of the declining perennial grassland plant Trifolium montanum in central Germany. Density and survival probability of juvenile plants decreased with light competition, measured as leaf area index (LAI) above T. montanum plants, resulting in aged populations with few juvenile plants at unmanaged sites with higher LAI. Reproduction of T. montanum was not related to LAI, but increased strongly with local density, suggesting pollinator limitation in fragmented populations with a low density of flowering plants. In the common garden, the survival of sown offspring increased with mean seed size, whereas seed production of offspring decreased with isolation, and in strong contrast to previous studies, also decreased with size and density of the population of origin. This could be due to increased inbreeding because of pollination between closely related neighbouring plants in dense and large populations. Our results indicate that both habitat degradation and fragmentation have negative effects on populations of T. montanum, but affect different phases of the life cycle. In the short term, the effects of habitat degradation are more important than those of fragmentation, and populations of T. montanum are primarily threatened by an increase in light competition in unmanaged sites, which rapidly affects the dynamics of the populations. The observed opposite effects of habitat fragmentation on reproduction and offspring fitness indicate that the effects of population size, density and isolation on plant fitness and population viability may be complex.     

Follow up estimation of Aedes aegypti entomological parameters and mathematical modellings

The dengue virus is a vector-borne disease transmitted by mosquito Aedes aegypti and the incidence is strongly influenced by temperature and humidity which vary seasonally. To assess the effects of temperature on dengue transmission, mathematical models are developed based on the population dynamics theory. However, depending on the hypotheses of the modelling, different outcomes regarding to the risk of epidemics are obtained. We address this question comparing two simple models supplied with model's parameters estimated from temperature-controlled experiments, especially the entomological parameters regarded to the mosquito's life cycle in different temperatures. Once obtained the mortality and transition rates of different stages comprising the life cycle of mosquito and the oviposition rate, we compare the capacity of vector reproduction (the basic offspring number) and the risk of infection (basic reproduction number) provided by two models. The extended model, which is more realistic, showed that both mosquito population and dengue risk are situated at higher values than the simplified model, even that the basic offspring number is lower.     

Temporal variation in reproductive allocation in a shield bug Elasmostethus interstinctus

We investigated changes in the reproductive output and the effect of female phenotype on reproductive parameters in a shield bug Elasmostethus interstinctus (L.) (Heteroptera: Acanthosomatidae) over the whole reproductive period. At the beginning and the middle of the reproductive period eggs were smaller than at the end of the period. Clutch mass and number of eggs per clutch decreased in laying sequence, first clutches being much larger than any of the later ones. Lifetime fecundity correlated positively with female size: large females produced more eggs and lived longer than small ones. Egg size did not vary with female size. Offspring survival until adulthood increased with egg weight. Individuals overwinter before reproduction, and because the nymphs from later-laid eggs have the least time to gather resources before overwintering, it may be important for later-laid eggs to be of high quality. Reproductive allocation varies during the reproductive period; females allocate resources relatively more to offspring number at the beginning of the reproductive period and more to offspring quality at the end of their life.     

Not All Offspring Are Created Equal: Variation in Larval Characteristics in a Serially Spawning Damselfish

The way organisms allocate their resources to growth and reproduction are key attributes differentiating life histories. Many organisms spawn multiple times in a breeding season, but few studies have investigated the impact of serial spawning on reproductive allocation. This study investigated whether resource allocation was influenced by parental characteristics and prior spawning history in a serial spawning tropical damselfish (Pomacentrus amboinensis). The offspring attributes of isolated parents of known characteristics were monitored over a 6-week breeding period in the field. Smaller females produced larvae of longer length and larger energy reserves at hatching. This finding is contrary to several other studies that found larger females produce offspring of greater quality. We found that resource allocation in the form of reproductive output was not influenced by the number of spawning events within the breeding season, with larger females producing the greatest number of offspring. Larval characteristics changed as spawning progressed. There was a general decline in length of larvae produced, with an increase in the size of the larval yolk-sac, for all females regardless of size as spawning progressed. This trend was accentuated by the smallest females. This change in larval characteristics may reflect a parental ability to forecast unfavourable conditions as the season progresses or a mechanism to ensure that some will survive no matter what conditions they encounter. This study highlights the importance of accounting for temporal changes in reproductive allocation in studies of reproductive trade-offs and investigations into the importance of parental effects.     

Direct and indirect effects of environmental temperature on the evolution of reproductive strategies: an information-theoretic approach

For ectotherms, environmental temperature affects the optimal size and number of offspring via multiple mechanisms. First, temperature influences the performance of offspring, which directly affects the optimal size of offspring. Second, temperature influences maternal body size, which indirectly affects the optimal size and/or number of offspring when larger females acquire more energetic resources or provide better parental care. Although traditional statistical approaches might distinguish the relative importance of these effects, an information-theoretic approach enables one to estimate effects more accurately by identifying the best evolutionary model in a set of candidate models. Here, we use the Akaike Information Criterion to calculate the likelihoods of seven path models, each derived from one or more optimality models of reproduction. Variation in reproductive traits among populations of lizards (Sceloporus undulatus) was used to quantify support for the models. Our results overwhelmingly supported a model based on an indirect effect of temperature that is mediated by maternal size. Path coefficients of this model were consistent with the hypotheses that, first, larger females can acquire more energy for reproduction and, second, the survival of offspring depends on both their size and their density. Our analyses exemplify how information theory can identify evolutionary hypotheses that merit experimental testing.     

The effects of density-dependent offspring mortality on the synchrony of reproduction

Mortality rates often depend on the size of a population. Using ideal free theory to model the optimal timing of reproduction in model populations, I considered how the specific relationship between density-dependent offspring mortality and population size affects the optimal temporal distribution of reproduction. The results suggest that the specific form of the relationship between density-dependent mortality and the number of offspring produced determines the degree to which reproduction within a population is synchronous. Specifically, reproductive synchrony decreases as density-dependent mortality becomes increasingly inversely related to the number of offspring produced and is highest when density-dependent mortality is directly density-dependent. These findings support the suggestion that predation pressure selects for greater reproductive synchrony in species where mortality is directly density-dependent, but does not affect the timing of reproduction in species with density-independent rates of mortality. This revised version was published online in July 2006 with corrections to the Cover Date.     

The fitness effects of delayed switching to sex in a facultatively asexual insect

Facultative reproductive strategies that incorporate both sexual and parthenogenetic reproduction should be optimal, yet are rarely observed in animals. Resolving this paradox requires an understanding of the economics of facultative asexuality. Recent work suggests that switching from parthenogenesis to sex can be costly and that females can resist mating to avoid switching. However, it remains unclear whether these costs and resistance behaviors are dependent on female age. We addressed these questions in the Cyclone Larry stick insect, Sipyloidea larryi, by pairing females with males (or with females as a control) in early life prior to the start of parthenogenetic reproduction, or in mid‐ or late life after a period of parthenogenetic oviposition. Young females were receptive to mating even though mating in early life caused reduced fecundity. Female resistance to mating increased with age, but reproductive switching in mid‐ or late life did not negatively affect female survival or offspring performance. Overall, mating enhanced female fitness because fertilized eggs had higher hatching success and resulted in more adult offspring than parthenogenetic eggs. However, female fecundity and offspring viability were also enhanced in females paired with other females, suggesting a socially mediated maternal effect. Our results provide little evidence that switching from parthenogenesis to sex at any age is costly for S. larryi females. However, age‐dependent effects of switching on some fitness components and female resistance behaviors suggest the possibility of context‐dependent effects that may only be apparent in natural populations.