How should parents adjust the size of their young in response to local environmental cues?

Models of parental investment typically assume that populations are well mixed and homogeneous and have devoted little attention to the impact of spatial variation in the local environment. Here, in a patch‐structured model with limited dispersal, we assess to what extent resource‐rich and resource‐poor mothers should alter the size of their young in response to the local environment in their patch. We show that limited dispersal leads to a correlation between maternal and offspring environments, which favours plastic adjustment of offspring size in response to local survival risk. Strikingly, however, resource‐poor mothers are predicted to respond more strongly to local survival risk, whereas resource‐rich mothers are predicted to respond less strongly. This lack of sensitivity on the part of resource‐rich mothers is favoured because they accrue much of their fitness through dispersing young. By contrast, resource‐poor mothers accrue a larger fraction of their fitness through philopatric young and should therefore respond more strongly to local risk. Mothers with more resources gain a larger share of their fitness through dispersing young partly because their fitness in the local patch is constrained by the limited number of local breeding spots. In addition, when resource variation occurs at the patch level, the philopatric offspring of resource‐rich mothers face stronger competition from the offspring of other local mothers, who also enjoy abundant resources. The effect of limited local breeding opportunities becomes less pronounced as patch size increases, but the impact of patch‐level variation in resources holds up even with many breeders per patch.     

The causes and consequences of variation in offspring size: a case study using Daphnia

Offspring size can have large and direct fitness implications, but we still do not have a complete understanding of what causes offspring size to vary. Daphnia (water fleas) generally produce fewer and larger offspring when food is limited. Here, we use a mathematical model to show that this could be explained by either: (1) an advantage of producing larger eggs when food is limited; or (2) a lower boundary on egg volume (below which eggs do not have sufficient resources to be viable), that is similar in volume to the evolutionarily stable egg volume predicted by standard clutch size models. We tested the first possibilities experimentally by placing offspring from mothers kept at two food treatments (high and low - leading to relatively small and large eggs respectively) into two food treatments (same as maternal treatments, in a fully factorial design) and measuring their fitness (reproduction, age at maturity, and size at maturity). We also tested survival under starvation conditions of offspring produced from mothers at low and high food treatments. We found that (larger) offspring produced by low-food mothers actually had lower fitness as they took longer to reproduce, regardless of their current food treatment. Additionally, we found no survival advantage to being born of a food-stressed mother. Consequently, our results do not support the hypothesis that there is an advantage to producing larger eggs when food is limited. In contrast, data from the literature support the importance of a lower boundary on egg size.     

Adaptive decision making or differential mortality: what causes offspring emergence in a gregarious parasitoid?

Hosts represent a limited resource for the developing offspring of parasitic insects laying eggs in or on spatially discrete resources like fruits, seeds, or other insects. The quality of hosts differs with respect to the value and amount of resources they provide for the feeding larvae. Accordingly, the size of a clutch of eggs laid on a given host should be a function of host quality, because severe competition between developing larvae can lead to increased mortality and/or decreased size of the offspring, both causing a fitness loss for the offspring and the mother. Therefore, females should be selected for the ability to estimate host quality and to adjust their clutch size accordingly. Using the parasitic wasp Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) this study investigated the respective contribution of developmental mortality of offspring vs. the clutch size decision of the mother as a determinant of final offspring emergence per host. In addition, taking offspring size into account, the study examined the fitness consequences of female oviposition decisions. Developmental mortality was very low in all quality classes of hosts except previously frozen and thus dead host pupae. Females laid reduced clutch sizes on dead, previously parasitized, and smaller hosts. In contrast to offspring number, offspring size did not differ between host qualities. We conclude that females are able to sense the quality of a host and adjust the number of eggs they lay to mitigate larval competition.     

The influence of a positive correlation between clutch size and offspring fitness on the optimal offspring size

Summary The effect is modeled of a positive relationship between clutch size and offspring fitness on the optimal investment in offspring. In species which meet the assumptions of the model, the model predicts a positive correlation between maternal resource level and offspring size. If larger mothers are able to allocate more resources to offspring, then the model would also predict a positive correlation between maternal size and offspring size when the assumptions of the model are met. Thus, this model may help explain both among and within individual variation in offspring size. When offspring are produced in groups and the number of offspring killed per clutch is limited by predator satiation, offspring in larger clutches may experience a higher probability of survival. Such a life style may be found in animals such as sea turtles. Offspring size is positively correlated with maternal size in some members of this group.     

The pay‐offs of maternal care increase as offspring develop,favouring extended provisioning in an egg‐feeding frog

Offspring quantity and quality are components of parental fitness that cannot be maximized simultaneously. When the benefits of investing in offspring quality decline, parents are expected to shift investment towards offspring quantity (other reproductive opportunities). Even when mothers retain complete control of resource allocation, offspring control whether to allocate investment to growth or development towards independence, and this shared control may generate parent–offspring conflict over the duration of care. We examined these predictions by, in a captive colony, experimentally removing tadpoles of the strawberry poison frog (Oophaga pumilio) from the mothers that provision them with trophic eggs throughout development. Tadpoles removed from their mothers were no less likely to survive to nutritional independence (i.e. through metamorphosis) than were those that remained with their mothers, but these offspring were smaller at metamorphosis and were less likely to survive to reach adult size, even though they were fed ad libitum. Tadpoles that remained with their mothers developed more slowly than those not receiving care, a pattern that might suggest that offspring extracted more care than was in mothers’ best interests. However, the fitness returns of providing care increased with offspring development, suggesting that mothers would be best off continuing care until tadpoles initiated metamorphosis. Although the benefits of parental investment in offspring quality are often thought to asymptote at high levels, driving parent–offspring conflict over weaning, this assumption may not hold over natural ranges of investment, with selection on both parents and offspring favouring extended durations of parental care.     

Parent–offspring conflict and selection on egg size in turtles

The trade‐off between offspring size and number can present a conflict between parents and their offspring. Because egg size is constrained by clutch size, the optimal egg size for offspring fitness may not always be equivalent to that which maximizes parental fitness. We evaluated selection on egg size in three turtle species (Apalone mutica, Chelydra serpentina and Chrysemys picta) to determine if optimal egg sizes differ between offspring and their mothers. Although hatching success was generally greater for larger eggs, the strength and form of selection varied. In most cases, the egg size that maximized offspring fitness was greater than that which maximized maternal fitness. Consistent with optimality theory, mean egg sizes in the populations were more similar to the egg sizes that maximized maternal fitness, rather than offspring fitness. These results provide evidence that selection has maximized maternal fitness to achieve an optimal balance between egg size and number.     

Mothers modify eggs into shields to protect offspring from parasitism

Eggs are an immobile, vulnerable stage of development and their success often depends on the oviposition decisions of the mother. Studies show that female animals, and sometimes males, may invest parental resources in order to increase the survival of their offspring. Here, we describe a unique form of parental investment in offspring survival. The seed beetle Mimosestes amicus may lay eggs singly, or may cover eggs with additional egg(s). This egg stacking serves to significantly reduce the mortality of the protected egg from parasitism by the parasitic wasp, Uscana semifumipennis. The smaller top eggs serve only as protective shields; they are inviable, and wasps that develop in them suffer negative fitness consequences. Further, we found egg stacking to be inducible; M. amicus increase the number of stacks they lay when parasitoids are present. However, stacking invokes a cost. When wasps are absent, beetles lay more single eggs, and produce more offspring, highlighting the adaptive value of this extraordinary example of behavioural plasticity in parental investment.     

Why do large mothers produce large offspring? Theory and a test

To explain the general tendency of large mothers to produce large offspring, we developed two models in which either the rate at which each single offspring extracts resources from the mother or the rate at which the mother supplies resources to all the offspring is limited (terminal- or upper-stream-limitation on resource transport, respectively). We also reanalyzed the data of Erythronium japonicum to test the models. The terminal-stream-limitation model predicted that the optimal offspring size that maximizes the fitness of the mother increases with an increase in the maximum rate of resource extraction by each single offspring. Thus, large mothers produce large offspring if the maximum resource extraction rate is high in those mothers. The upper-stream-limitation model predicted that the optimal offspring size decreases with an increase in the maximum rate of resource supply by the mother to all the offspring. In E. japonicum, the maximum growth rate of a seed was independent of the number of seeds of a plant, suggesting that the resource extraction rate is limited at the individual seed level. The maximum growth rate was high in large plants and had a strong positive effect on final seed mass. Thus, the results were consistent with the terminal-stream-limitation model.     

Phenotypic variability in nesting success among Osmia lignaria propinqua females in a glasshouse environment: (Hymenoptera: Megachilidae)

Abstract. 1. The phenotypic variability of several estimates of fitness among seventeen nesting female O.lignaria Cresson was examined in a glasshouse provided with abundant resources.
2. Females exhibited wide variation in: (a) number of nests and cells made and in their rate of construction, (b) the incidence of mortality of offspring, and (c) the percentage of male offspring produced (52–100%).
3. In confirmation of earlier field studies: (a) more offspring of both sexes were produced during the first half of the nesting season, (b) most female offspring were produced early in the nesting season, (c) most parental investment during the last half of the flight season was made in male offspring, (d) there was a decrease in offspring size with season, with females decreasing more than males, and (e) the ratio of female/male body weight was = 1.8. These results appear to be due to ageing rather than to a reduction in resource availability.
4. No relation between female size and fecundity was evident.
5. There was no evidence that small females tended to produce a greater proportion of the smaller sex (males) than did large females.
6. Smaller offspring of both sexes had a much greater probability of dying overwinter than did large offspring. However, where the sexes overlapped in size (large males, small females), almost all females died and almost all males survived. We hypothesize that as size of offspring produced declines with season, a greater proportion of males are produced because they have a much greater probability of surviving at small body sizes.     

Sex allocation in yellow-legged gulls (Larus michahellis) depends on nutritional constraints on production of large last eggs

Male and female offspring can differ in their susceptibility to pre-natal (e.g. egg quality) and post-natal (e.g. sib–sib competition) conditions, and parents can therefore increase their individual fitness by adjusting these maternal effects according to offspring sex. In birds, egg mass and laying/hatching order are the main determinants of offspring viability, but these effects can act differently on each sex. In a previous study, relatively large last-laid (c-)eggs of yellow-legged gulls (Larus michahellis) were more likely to carry a female embryo. This suggests compensatory allocation of maternal resources to daughters from c-eggs, which suffer reduced viability. In the present study, we supplemented yellow-legged gulls with food during the laying period to experimentally test whether their nutritional conditions were responsible for the observed covariation between c-egg sex and mass. As predicted, food supplementation enhanced female c-eggs'' mass more than that of male c-eggs. Thus, this experiment indicates that mothers strategically allocated their resources to c-eggs, possibly in order to compensate for the larger susceptibility of daughters to hatching (and laying) order. The results also suggested that mothers decided on resource allocation depending on the sex of already ovulated c-eggs, rather than ovulating ova of either sex depending on food availability.     

How to balance the offspring quality–quantity tradeoff when environmental cues are unreliable

Maternal effects on offspring size can have a strong effect on fitness, as larger offspring often survive better under harsh environmental conditions. Selection should hence favour mothers that find an optimal solution to the offspring size versus number tradeoff. If environmental conditions are variable, there will not be a single optimal offspring size, as predicted in a constant environment, but plastic responses can be favoured. To be able to adjust offspring size in an adaptive manner, mothers have to use environmental cues to predict offspring environmental conditions. Cues can be unreliable, however, particularly in species where individuals occupy different niches at different life stages. Here we model the evolution of plasticity of offspring size when the environmental cues mothers use to predict the conditions experienced by their offspring are not perfectly reliable. Our results show that plastic strategies are likely to be superior to fixed strategies in a stochastically varying environment when the environmental cues are at least moderately reliable, with the threshold depending on plasticity costs and the difference of resources available to mothers. Plasticity is more likely to occur if resource availability is not too different between environments. For any given scenario, plasticity in offspring size is favoured if offspring survival varies greatly between environmental states. Whenever plastic strategies are optimal, the occurring switches performed by mothers between small and large offspring are predicted to be substantial, as small adjustments are unlikely to reap fitness benefits great enough to overcome the costs of plasticity.     

Body size-specific maternal effects on the offspring environment shape juvenile phenotypes in Atlantic salmon

Positive associations between maternal investment per offspring and maternal body size have been explained as adaptive responses by females to predictable, body size-specific maternal influences on the offspring’s environment. As a larger per-offspring investment increases maternal fitness when the quality of the offspring environment is low, optimal egg size may increase with maternal body size if larger mothers create relatively poor environments for their eggs or offspring. Here, we manipulate egg size and rearing environments (gravel size, nest depth) of Atlantic salmon (Salmo salar) in a 2 × 2 × 2 factorial experiment. We find that the incubation environment typical of large and small mothers can exert predictable effects on offspring phenotypes, but the nature of these effects provides little support to the prediction that smaller eggs are better suited to nest environments created by smaller females (and vice versa). Our data indicate that the magnitude and direction of phenotypic differences between small and large offspring vary among maternal nest environments, underscoring the point that removal of offspring from the environmental context in which they are provisioned in the wild can bias experimentally derived associations between offspring size and metrics of offspring fitness. The present study also contributes to a growing literature which suggests that the fitness consequences of egg size variation are often more pronounced during the early juvenile stage, as opposed to the egg or larval stage.     

Maternal effects and their consequences for offspring fitness in the Yellow Dung Fly

1. Maternal adult diet and body size influence the fecundity of a female and possibly the quality and the performance of her offspring via egg size or egg quality. In laboratory experiments, negative effects in the offspring generation have often been obscured by optimal rearing conditions.
2. To estimate these effects in the Yellow Dung Fly, Scathophaga stercoraria , how maternal body size and adult nutritional status affected her fecundity, longevity and egg size were first investigated.
3. Second, it was investigated how female age and adult nutritional experience, mediated through the effects of egg size or egg quality, influenced the performance of offspring at different larval densities.
4. Maternal size was less important than maternal adult feeding in increasing reproductive output. Without food restriction, large females had larger clutch sizes and higher oviposition rates, whereas under food restriction this advantage was reversed in favour of small females.
5. Offspring from mothers reared under nutritional stress experienced reduced fitness in terms of egg mortality and survival to adult emergence. If the offspring from low-quality eggs survived, the transmitted maternal food deficiency only affected adult male body size under stressful larval environments.
6. Smaller egg sizes due to maternal age only slightly affected the performance of the offspring under all larval conditions.     

Resource exploitation and relatedness: implications for offspring size variation within broods

Much of the theory on offspring size variation within a brood relies on unequal maternal allocation of resources to each embryo. However, maternal allocation strategies are subject to an inherent conflict between mothers and offspring: individual offspring, being more closely related to themselves than to their siblings, should always prefer a larger share of the available resources than that which is optimal from their mother's perspective. Thus, in species where mothers cannot unilaterally impose a resource allocation strategy, offspring can respond to this conflict by competing for more resources than is maternally optimal. Here we show that variation in offspring size within a brood can arise as a by‐product of competition between siblings over a common resource, even when 1) there are no competitive inequalities within families, and 2) maternal investment per brood is fixed. Moreover, we show that size variance among offspring increases with increasing levels of competition, brought about by decreasing relatedness among siblings. Conflict thus offers a simple, testable and, potentially general, explanation for the wide variability in offspring size seen in nature. This extends explanatory hypotheses for offspring size variation beyond those of maternal effects, under which most explanations have been subsumed to date.     

The maternal energetic environment affects both egg and offspring phenotypes in green anole lizards (Anolis carolinensis)

Animals exist in dynamic environments that may affect both their own fitness and that of their offspring. Maternal effects might allow mothers to prepare their offspring for the environment in which they will be born via several mechanisms, not all of which are well understood. Resource scarcity and forced resource allocation are two scenarios that could affect maternal investment by altering the amount and type of resources available for investment in offspring, albeit in potentially different ways. We tested the hypothesis that maternal dietary restriction and sprint training have different consequences for the offspring phenotype in an oviparous lizard (Anolis carolinensis). To do this, we collected and reared eggs from adult diet-manipulated females (low-diet [LD] or high-diet [HD]) and sprint-trained females (sprint trained [ST] or untrained [UT]) and measured both egg characteristics and hatchling morphology. ST and LD mothers laid both the fewest and heaviest eggs, and ST, UT, and LD eggs also had significantly longer incubation periods than the HD group. Hatchlings from the diet experiment (LD and HD offspring) were the heaviest overall. Furthermore, both body mass of the mother at oviposition and change in maternal body mass over the course of the experiment had significant and sometimes different effects on egg and offspring phenotypes, highlighting the importance of maternal energetic state to the allocation of maternal resources.     

Resource-Dependent Clutch Size Decisions and Size-Fitness Relationships in a Gregarious Ectoparasitoid Wasp, <Emphasis Type="Italic">Bracon brevicornis</Emphasis>

Gregarious parasitic wasps, which lay more than one egg into or onto a host arthropod’s body, are usually assumed to lay an optimal number of eggs per host. If females would lay too few eggs, some resources may be wasted, but if females lay too many eggs, offspring may develop into substantially smaller-sized adults or may not develop successfully and die. The availability of hosts can further influence a female’s clutch size decision, as more eggs should be laid when hosts are scarce. Here, we analyzed clutch size decisions and the fitness consequences thereof in the ectoparasitic wasp Bracon brevicornis (Hymenoptera: Braconidae), a potential biocontrol agent against pest moth species. For experiments, larvae of the Mediterranean flower moth, Ephestia kuehniella (Lepidoptera: Pyralidae) were used. Using artificially created as well as naturally laid clutches of eggs, the effects of clutch size on fitness of first (F1) and second (F2) generation offspring were investigated. Our results revealed that the fitness consequences of large clutches included both increased mortality and smaller adult sizes of the emerging offspring (F1). Smaller F1 females matured fewer eggs during their lifetime and their offspring (F2) had reduced egg-to-adult survival probability. Naturally laid clutches varied with host size up to a maximum, which probably reflects egg limitation. Clutches remained smaller than the calculated optimal (Lack) clutch size and females responded to high host availability with a decreased number of eggs laid. We thus conclude that large clutches may result in significantly smaller offspring with reduced fitness, and that host size as well as host availability influence the clutch size decision made by B. brevicornis females.     

Resource selection by female moths in a heterogeneous environment: what is a poor girl to do?

1. According to the preference-performance hypothesis, female insects select resources that maximize offspring performance. To achieve high fitness, leaf miner females should then adjust their oviposition behaviour in response to leaf attributes signalling high host quality. 2. Here we investigate resource selection in Tischeria ekebladella, a leaf-mining moth of the pedunculate oak (Quercus robur), in relation to two alternative hypotheses: (1) females select their resources with respect to their future quality for developing larvae; or (2) temporal changes in resource quality prevent females from selecting the best larval resources. 3. Specifically, we test whether females show the strongest selection at the levels at which quality varies the most (shoots and leaves); whether they respond to specific leaf attributes (leaf size, phenolic content and conspecific eggs); and whether female preference is reflected in offspring performance. 4. Female choice of leaves was found to be non-random. Within trees, the females preferred certain shoots, but when the shoots were on different trees the degree of discrimination was about four times larger than when they were on the same trees. 5. While females typically lay more eggs on large leaves, this is not a result of active selection of large leaves, but rather a result of females moving at random and ovipositing at regular intervals. 6. The females in our study did not adjust their oviposition behaviour in response to leaf phenolic contents (as measured by the time of larval feeding). Neither did they avoid leaves with conspecific eggs. 7. Female choice of oviposition sites did not match patterns of offspring performance: there was no positive association between offspring survival and counts of eggs. 8. We propose that temporal variation in resource quality may prevent female moths from evaluating resource quality reliably. To compensate for this, females may adopt a risk-spreading strategy when selecting their resources.     

Allocation of offspring size and sex by female black ratsnakes

How females allocate resources to each offspring and how they allocate the sex of their offspring are two powerful potential avenues by which mothers can affect offspring fitness. Previous research has focussed extensively on mean offspring size, with much less attention given to variance in offspring size. Here we focussed on variation in offspring size in black ratsnakes, Elaphe obsoleta . We collected and hatched 105 clutches (1283 eggs) over 9 years. We predicted that females should lay larger eggs, or more variable eggs, when the environment is less predictable. We also predicted that females laying early or laying larger eggs should produce mostly sons because adult males are larger than adult female ratsnakes. The largest hatchling was more than twice the length and almost four times the mass of the smallest hatchling. Variation in offspring size was itself highly variable, with CVs in offspring mass among clutches ranging from 1% to 25%. With one exception, the variables we expected should influence variation in offspring size had little effect. We found that clutch size increased with maternal size and that egg size decreased with clutch size, but we found no evidence that variance in egg size among clutches increased as the season progressed or that females increased the mean size of their offspring the later in the season they laid their eggs. Females in better condition after they finish laying their eggs did produce larger eggs. There was no relationship between within-clutch variation in egg size and laying date or mean egg size. Finally, sex ratio did not vary with mean egg size or hatching date. Given evidence that offspring size in snakes affects survival, selection should reduce variation in offspring size unless that variance enhances maternal fitness and yet we found little support for hypothesized advantages of varying offspring size.     

Mothers reduce egg provisioning with age

Precise and comprehensive data on resource allocation into individual eggs are rare and this empirical void in the literature of life history strategies contrasts with the large number of theoretical studies. We show a marked decrease in reproductive investment in eggs with mother's age for egg size, sugar, protein, lipid and energy contents of eggs for a parasitic wasp. Egg size is a good predictor of offspring fitness, measured as survival of starving neonate larvae, but does not reveal possible biochemical changes. Lipids stabilize quickly at a minimal threshold while proteins and sugars decrease smoothly down to about 30% of the amount invested in the first egg. Because proteins have the highest correlation with egg size, we predict that they should be better predictors of larval fitness than lipids and sugars. Assessing the adaptive value of the observed patterns will require a multidimensional approach to egg provisioning.     

Intergenerational effects of inbreeding in Nicrophorus vespilloides: offspring suffer fitness costs when either they or their parents are inbred

Inbreeding depression is the reduction in fitness caused by mating between related individuals. Inbreeding is expected to cause a reduction in offspring fitness when the offspring themselves are inbred, but outbred individuals may also suffer a reduction in fitness when they depend on care from inbred parents. At present, little is known about the significance of such intergenerational effects of inbreeding. Here, we report two experiments on the burying beetle Nicrophorus vespilloides, an insect with elaborate parental care, in which we investigated inbreeding depression in offspring when either the offspring themselves or their parents were inbred. We found substantial inbreeding depression when offspring were inbred, including reductions in hatching success of inbred eggs and survival of inbred offspring. We also found substantial inbreeding depression when parents were inbred, including reductions in hatching success of eggs produced by inbred parents and survival of outbred offspring that received care from inbred parents. Our results suggest that intergenerational effects of inbreeding can have substantial fitness costs to offspring, and that future studies need to incorporate such costs to obtain accurate estimates of inbreeding depression.