Spatial variation in egg size and egg number reflects trade-offs and bet-hedging in a freshwater fish

1.?Maternal reproductive investment is thought to reflect a trade-off between offspring size and fecundity, and models generally predict that mothers inhabiting adverse environments will produce fewer, larger offspring. More recently, the importance of environmental unpredictability in influencing maternal investment has been considered, with some models predicting that mothers should adopt a diversified bet-hedging strategy whilst others a conservative bet-hedging strategy. 2.?We explore spatial egg size and fecundity patterns in the freshwater fish southern pygmy perch (Nannoperca australis) that inhabits a diversity of streams along gradients of environmental quality, variability and predictability. 3.?Contrary to some predictions, N.?australis populations inhabiting increasingly harsh streams produced more numerous and smaller eggs. Furthermore, within-female egg size variability increased as environments became more unpredictable. 4.?We argue that in harsh environments or those prone to physical disturbance, sources of mortality are size independent with offspring size having only a minor influence on offspring fitness. Instead, maternal fitness is maximized by producing many small eggs, increasing the likelihood that some offspring will disperse to permanent water. We also provide empirical support for diversified bet-hedging as an adaptive strategy when future environmental quality is uncertain and suggest egg size may be a more appropriate fitness measure in stable environments characterized by size-dependent fitness. These results likely reflect spatial patterns of adaptive plasticity and bet-hedging in response to both predictable and unpredictable environmental variance and highlight the importance of considering both trait averages and variance. 5.?Reproductive life-history traits can vary predictably along environmental gradients. Human activity, such as the hydrological modification of natural flow regimes, alters the form and magnitude of these gradients, and this can have both ecological and evolutionary implications for biota adapted to now non-existent natural environmental heterogeneity.     

Bet-hedging as an evolutionary game: the trade-off between egg size and number

Bet-hedging theory addresses how individuals should optimize fitness in varying and unpredictable environments by sacrificing mean fitness to decrease variation in fitness. So far, three main bet-hedging strategies have been described: conservative bet-hedging (play it safe), diversified bet-hedging (don’t put all eggs in one basket) and adaptive coin flipping (choose a strategy at random from a fixed distribution). Within this context, we analyse the trade-off between many small eggs (or seeds) and few large, given an unpredictable environment. Our model is an extension of previous models and allows for any combination of the bet-hedging strategies mentioned above. In our individual-based model (accounting for both ecological and evolutionary forces), the optimal bet-hedging strategy is a combination of conservative and diversified bet-hedging and adaptive coin flipping, which means a variation in egg size both within clutches and between years. Hence, we show how phenotypic variation within a population, often assumed to be due to non-adaptive variation, instead can be the result of females having this mixed strategy. Our results provide a new perspective on bet-hedging and stress the importance of extreme events in life history evolution.     

Bet hedging in a warming ocean: predictability of maternal environment shapes offspring size variation in marine sticklebacks

Bet hedging at reproduction is expected to evolve when mothers are exposed to unpredictable cues for future environmental conditions, whereas transgenerational plasticity (TGP) should be favoured when cues reliably predict the environment offspring will experience. Since climate predictions forecast an increase in both temperature and climate variability, both TGP and bet hedging are likely to become important strategies to mediate climate change effects. Here, the potential to produce variably sized offspring in both warming and unpredictable environments was tested by investigating whether stickleback (Gasterosteus aculeatus) mothers adjusted mean offspring size and within‐clutch variation in offspring size in response to experimental manipulation of maternal thermal environment and predictability (alternating between ambient and elevated water temperatures). Reproductive output traits of F1 females were influenced by both temperature and environmental predictability. Mothers that developed at ambient temperature (17 °C) produced larger, but fewer eggs than mothers that developed at elevated temperature (21 °C), implying selection for different‐sized offspring in different environments. Mothers in unpredictable environments had smaller mean egg sizes and tended to have greater within‐female egg size variability, especially at 21 °C, suggesting that mothers may have dynamically modified the variance in offspring size to spread the risk of incorrectly predicting future environmental conditions. Both TGP and diversification influenced F2 offspring body size. F2 offspring reared at 21 °C had larger mean body sizes if their mother developed at 21 °C, but this TGP benefit was not present for offspring of 17 °C mothers reared at 17 °C, indicating that maternal TGP will be highly relevant for ocean warming scenarios in this system. Offspring of variable environment mothers were smaller but more variable in size than offspring from constant environment mothers, particularly at 21 °C. In summary, stickleback mothers may have used both TGP and diversified bet‐hedging strategies to cope with the dual stress of ocean warming and environmental uncertainty.     

Maternal source of variability in the embryo development of an annual killifish

Organisms inhabiting unpredictable environments often evolve diversified reproductive bet‐hedging strategies, expressed as production of multiple offspring phenotypes, thereby avoiding complete reproductive failure. To cope with unpredictable rainfall, African annual killifish from temporary savannah pools lay drought‐resistant eggs that vary widely in the duration of embryo development. We examined the sources of variability in the duration of individual embryo development, egg production and fertilization rate in Nothobranchius furzeri. Using a quantitative genetics approach (North Carolina type II design), we found support for maternal effects rather than polyandrous mating as the primary source of the variability in the duration of embryo development. The number of previously laid eggs appeared to serve as an internal physiological cue initiating a shift from rapid‐to‐slow embryo developmental mode. In annual killifish, extensive phenotypic variability in progeny traits is adaptive, as the conditions experienced by parents have limited relevance to the offspring generation. In contrast to genetic control, with high phenotypic expression and heritability, maternal control of traits under natural selection prevents standing genetic diversity from potentially detrimental effects of selection in fluctuating environments.     

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.     

Patterns and fitness consequences of intraclutch variation in egg provisioning in tropical Australian frogs

Intraclutch variation in offspring size should evolve when offspring encounter unpredictable environmental conditions. This form of bet-hedging should maximise the lifetime reproductive success of individuals that engage it. We documented the numbers of eggs and means and variances of yolk volume in 15 frog species that occur in tropical savanna woodland. We experimentally determined the effects of initial yolk volume on larval growth patterns in four species. Intraclutch variation in yolk volume occurred to some degree in all species surveyed. Some species had very low, others had very high, intraclutch variation in yolk volume, but all species in which some clutches were highly variable also produced clutches with low variability. Species that occur in areas where the offspring environment is likely to be unpredictable had elevated levels of intraclutch variation in egg provisioning. There was no trade-off between egg size and number in any species surveyed. Under benign laboratory conditions, tadpoles from eggs with larger yolk volumes hatched at larger sizes, and these size differences persisted through a substantial proportion of the larval stage. This indicates that intraclutch variation in egg size has major offspring and thus parental fitness consequences, and is therefore a functional selection variable. This study provides evidence in support of models which predict that intraclutch variation in offspring provisioning can evolve in organisms that reproduce in unpredictable habitats.     

Maternal effects of egg size in brown trout (Salmo trutta): norms of reaction to environmental quality

The magnitude of fitness variation caused by maternal effects and, thus, the adaptive significance of maternal traits may depend on environmental quality, generating crossing reaction norms among offspring phenotypes that shape life-history evolution. By manipulating intraclutch variation in egg size and comparing siblings we examined the maternal effects of egg size on offspring performance and tested for the existence of reaction norms to environmental quality using the brown trout Salmo trutta. When sibling groups of small and large eggs were reared separately in a hatchery environment initial size differences disappeared rapidly. However, in semi-natural environments and under direct competition, juveniles from large eggs experienced growth and survival advantages over siblings from small eggs. Moreover, distinct reaction norms existed, with the differences in performance of juveniles from small and large eggs being most pronounced in the poorer growth environments. Our results provide the first direct evidence, to our knowledge, for a causal relationship between egg size and fitness-related traits in fishes, independent of potentially confounding genetic effects. Moreover, they indicate that previous studies have been biased by experimental conditions that excluded competitive asymmetries and environmental variability. The existence of reaction norms indicates a shift in optimal egg size across gradients of environmental quality that probably shapes the evolution of this trait.     

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.     

Factors promoting maternal trophic egg provisioning in non-eusocial animals

The adaptive function of trophic egg-laying is generally regarded as extended parental investment to the offspring. However, the evolutionary factors promoting trophic egg-laying are still unclear, because the amount of maternal investment per offspring should be ideally equal between smaller offspring with trophic eggs and larger offspring without any additional investment. Several authors have suggested that trophic egg-laying should evolve only when egg size is constrained, but this hypothesis has not been evaluated. We investigated the evolutionary mechanisms of trophic egg-laying by two different approaches. First, we evaluated morphological constraints on egg size in two sibling ladybird species, Harmonia axyridis, which is known to produce trophic eggs, and H. yedoensis. Second, we theoretically predicted the optimal proportion of trophic eggs to total eggs and egg size in relation to environmental heterogeneity, predictability of environmental quality, and investment efficiency of trophic egg consumption. The intra- and interspecific morphological comparisons suggest that morphological constraints on the evolutionary determination of egg size are weak at best in the two ladybird species. Moreover, we theoretically showed that small egg size and trophic egg-laying are favoured in heterogeneous environments when mothers cannot adjust egg size plastically. We also showed that even a small reduction in investment efficiency makes a trophic egg strategy unlikely, despite relatively high environmental predictability. We conclude that trophic egg provisioning may be a flexible maternal adaptation to a highly heterogeneous environment rather than a response to a morphological constraint on egg size.     

Maternal investment increases with altitude in a frog on the Tibetan Plateau

Reproducing females can allocate energy between the production of eggs or offspring of different size or number, both of which can strongly influence fitness. The physical capacity to store developing offspring imposes constraints on maximum clutch volume, but individual females and populations can trade off whether more or fewer eggs or offspring are produced, and their relative sizes. Harsh environments are likely to select for larger egg or offspring size, and many vertebrate populations compensate for this reproductive investment through an increase in female body size. We report a different trade‐off in a frog endemic to the Tibetan Plateau, Rana kukunoris. Females living at higher altitudes (n = 11 populations, 2000–3500 m) produce larger eggs, but without a concomitant increase in female body size or clutch size. The reduced diel and seasonal activity at high altitudes may impose constraints on the maximum body size of adult frogs, by limiting the opportunity for energy accumulation. Simultaneously, producing larger eggs likely helps to increase the rate of embryonic development, causing tadpoles to hatch earlier. The gelatinous matrix surrounding eggs, more of which is produced by large females, may help buffer developing embryos from temperature fluctuations or offer protection from ultraviolet radiation. High‐altitude frogs on the Tibetan Plateau employ a reproductive strategy that favours large egg size independent of body size, which is unusual in amphibians. The harsh and unpredictable environmental conditions at high altitudes can thus impose strong and opposing selection pressures on adult and embryonic life stages, both of which can simultaneously influence fitness.     

A limit on the extent to which increased egg size can compensate for a poor postnatal environment revealed experimentally in the burying beetle,Nicrophorus vespilloides

It is often assumed that there is a positive relationship between egg size and offspring fitness. However, recent studies have suggested that egg size has a greater effect on offspring fitness in low‐quality environments than in high‐quality environments. Such observations suggest that mothers may compensate for poor posthatching environments by increasing egg size. In this paper we test whether there is a limit on the extent to which increased egg size can compensate for the removal of posthatching parental care in the burying beetle, Nicrophorus vespilloides. Previous experiments with N. vespilloides suggest that an increased egg size can compensate for a relatively poor environment after hatching. Here, we phenotypically engineered female N. vespilloides to produce large or small eggs by varying the amount of time they were allowed to feed on the carcass as larvae. We then tested whether differences between these groups in egg size translated into differences in larval performance in a harsh postnatal environment that excluded parental care. We found that females engineered to produce large eggs did not have higher breeding success, and nor did they produce larger larvae than females engineered to produce small eggs. These results suggest that there is a limit on the extent to which increased maternal investment in egg size can compensate for a poor posthatching environment. We discuss the implication of our results for a recent study showing that experimental N. vespilloides populations can adapt rapidly to the absence of posthatching parental care.     

Stress hormones: a link between maternal condition and sex-biased reproductive investment

In species where offspring fitness is sex-specifically influenced by maternal reproductive condition, sex allocation theory predicts that poor-quality mothers should invest in the evolutionarily less expensive sex. Despite an accumulation of evidence that mothers can sex-specifically modulate investment in offspring in relation to maternal quality, few mechanisms have been proposed as to how this is achieved. We explored a hormonal mechanism for sex-biased maternal investment by measuring and experimentally manipulating baseline levels of the stress hormone corticosterone in laying wild female European starlings (Sturnus vulgaris) and examining effects on sex ratio and sex-specific offspring phenotype adjustment. Here we show that baseline plasma corticosterone is negatively correlated with energetic body condition in laying starlings, and subsequent experimental elevation of maternal baseline plasma corticosterone increased yolk corticosterone without altering maternal condition or egg quality per se. Hormonal elevation resulted in the following: female-biased hatching sex ratios (caused by elevated male embryonic mortality), lighter male offspring at hatching (which subsequently grew more slowly during postnatal development), and lower cell-mediated immune (phytohemagglutinin) responses in males compared with control-born males; female offspring were unaffected by the manipulation in both years of the study. Elevated maternal corticosterone therefore resulted in a sex-biased adjustment of offspring quality favorable to female offspring via both a sex ratio bias and a modulation of male phenotype at hatching. In birds, deposition of yolk corticosterone may benefit mothers by acting as a bet-hedging strategy in stochastic environments where the correlation between environmental cues at laying (and therefore potentially maternal condition) and conditions during chick-rearing might be low and unpredictable. Together with recent studies in other vertebrate taxa, these results suggest that maternal stress hormones provide a mechanistic link between maternal quality and sex-biased maternal investment in offspring.     

Rearing conditions determine offspring survival independent of egg quality: a cross-foster experiment with Oystercatchers Haematopus ostralegus

Variation in rearing conditions, due either to parental or to environmental quality, can result in offspring of different quality (e.g. body condition, immune function). However, evidence is accumulating that egg size and composition can also affect offspring quality. In Oystercatchers Haematopus ostralegus , high-quality rearing conditions result in a higher quantity as well as quality of offspring. This is thought to be caused by increased parental food provisioning to the chicks in high-quality environments. However, variation in egg quality between rearing conditions could also affect the quantity and quality of offspring. Determining the mechanism and ontogeny of quality differences is important in unravelling the causes of variation in reproductive success. To disentangle the effects of egg quality, and quality of the rearing conditions, on the future survival of offspring, we cross-fostered complete clutches between nests. When reared under conditions of similar environmental quality, chicks originating from eggs laid in low-quality environments survived as well as chicks originating from eggs laid in a high-quality environment. However, chicks reared in high-quality environments survived twice as long as chicks reared in low-quality environments, independent of the environmental quality in which the eggs were laid. This suggests that variation in the future survival of offspring is primarily caused by differences in environmental and/or parental quality, with no clear effect of egg quality (size).     

Fitness consequences of variable maternal provisioning in quacking frogs (Crinia georgiana)

Variable maternal provisioning may evolve when there is variation in the quality of offspring environments. The frog Crinia georgiana has high variability in egg size both within and between clutches, independent of female phenotype. It breeds in ponds with high spatial and temporal variation in habitat quality. Egg size strongly affected offspring fitness in good and poor quality offspring environments, whether the egg size difference was from between or within clutches. Since there is a trade-off in egg size and number, these fitness consequences translate to strong effects on maternal fitness. In the variable and unpredictable offspring environment of C. georgiana, the maintenance of variable maternal provisioning both within and between clutches is likely to be an evolved response to the offspring environment.     

Egg size plasticity corresponding to maternal food conditions in an annual fish,Ayu <Emphasis Type="Italic">Plecoglossus altivelis</Emphasis>

The classic model of Smith and Fretwell predicts that the optimal egg size will vary according to the shape of the relationship between offspring size and offspring fitness, which may vary among environments. Adaptive significance of intrapopulation egg size variation was examined using Ayu (Plecoglossus altivelis). The species has an annual and migratory life history. Fish under controlled rearing conditions become sexually mature with a trend that smaller females produced larger eggs later in the season. Observed egg size variation was explained by the maternal specific growth rate, which was composed of maternal body size and growing period. Hatchlings from larger eggs had a larger notochord length, larger yolk-sac and grew faster. Such offspring traits provide general advantages of increased larval size, which confer competitive ability for assuring early survivorship. In conclusion, egg size plasticity in Ayu suggests higher offspring fitness through enhancement of their accessibility to food.     

Fatty acid content of eggs determines antipredator performance of fish larvae

Recent work has suggested that provisioning of eggs with certain critical nutrients could be a more meaningful measure of maternal investment and correlate of offspring fitness than traditional measures of egg size. The aim of our study was to assess variability in egg quality and larva quality and to identify connections between them and the implications for larval survival. Egg size, proximate composition, and fatty acid composition were measured for 40 batches of eggs from 8 captive pairs of red drum (Osteichthyes: Sciaenops ocellatus). We reared larvae from these batches of eggs to a common size (10 mm total length, 2-3 weeks posthatching) and assessed routine activity and escape response performance of 671 individuals. Egg fatty acid composition varied more than egg size or proximate composition. Concentrations of certain long chain, highly unsaturated essential fatty acids (e.g., arachidonic acid and docosahexaenoic acid) were the only egg traits that were significantly related to larva quality (measured as escape performance). Reduced escape performance of larvae from eggs with low fatty acid concentrations was not compensated by 3 weeks of feeding on a diet enriched with fatty acids, suggesting irreversible developmental effects. Since fatty acids in eggs originate from the maternal diet, offspring survival may be determined in part by availability of nutrient-rich prey to pre-spawning adults. Migrations, regime shifts, and exploitation of marine communities could operate through this mechanism to influence recruitment in fish populations. Our findings underscore the importance of non-genetic maternal contributions to egg quality and the linkage between environmental conditions experienced by adult females and offspring fitness.     

Elevated corticosterone during egg production elicits increased maternal investment and promotes nestling growth in a wild songbird

Glucocorticoids circulating in breeding birds during egg production accumulate within eggs, and may provide a potent form of maternal effect on offspring phenotype. However, whether these steroids affect offspring development remains unclear. Here, we employed a non-invasive technique that experimentally elevated the maternal transfer of corticosterone to eggs in a wild population of house wrens. Feeding corticosterone-injected mealworms to free-living females prior to and during egg production increased the number of eggs that females produced and increased corticosterone concentrations in egg yolks. This treatment also resulted in an increase in the amount of yolk allocated to eggs. Offspring hatching from these eggs begged for food at a higher rate than control offspring and eventually attained increased prefledging body condition, a trait predictive of their probability of recruitment as breeding adults in the study population. Our results indicate that an increase in maternal glucocorticoids within the physiological range can enhance maternal investment and offspring development.     

Adaptive egg size plasticity for larval competition and its limits in the seed beetle Callosobruchus chinensis

Life‐history theory predicts that females who experienced stressful conditions, such as larval competition or malnutrition, should increase their investment in individual offspring to increase offspring fitness (the adaptive parental hypothesis). In contrast, it has been shown that when females were reared under stressful conditions, they become smaller, which consequently decreases egg size (the parental stress hypothesis). To test whether females adjust their egg volume depending on larval competition, independent of maternal body mass constraint, we used a pest species of stored adzuki beans, Callosobruchus chinensis (L.) (Coleoptera: Chrysomelidae: Bruchinae). The eggs of females reared with competitors were smaller than those of females reared alone, supporting the parental stress hypothesis; however, correcting for female body size, females reared with competitors produced larger eggs than those reared in the absence of competition, supporting the adaptive parental hypothesis, as predicted. The phenotypic plasticity in females' investment in each offspring in stressful environments counteracts the constraint of body size on egg size.     

Predation risk affects the levels of maternal immune factors in avian eggs

Predation risk is an environmental stressor that can induce changes in prey behavior and physiology. Perception of predation risk may indirectly affect offspring traits and future fitness prospects via impacts on the condition of parents. Females may influence the survival of their offspring via maternal effects, especially when breeding in stressful conditions. We investigated the effects of continuous predation risk perceived by mothers on the maternal allocation of immune factors and carotenoids in eggs of the pied flycatcher Ficedula hypoleuca. We collected eggs from wild pied flycatchers that bred in the vicinity of a predator nest (pygmy owl Glaucidium passerinum), were exposed to cues of a mammalian nest predator (urine of least weasel Mustela nivalis), or received appropriate controls for these two groups. Pied flycatchers transferred more immunoglobulin in eggs under high predation risk in both owl and mammalian predator treatments. The presence of owl nests also lowered the level of lysozyme transferred in the eggs in one of the two study years. Predation risk did not modify egg size or overall carotenoid levels. Our results show that continuous predation risk perceived by females during egg‐laying affects egg composition. This different allocation of maternal immune factors may be an adaptive response evolved to increase the probability of offspring survival.     

Stressed mothers lay eggs with high corticosterone levels which produce low-quality offspring

Organisms frequently encounter stressful ecological conditions. In vertebrates, a major mechanism of physiological response to stress is mediated by the hypothalamic-pituitary-adrenal axis and results in increased secretion of glucocorticosteroids, which can have adverse consequences on diverse phenotypic traits affecting fitness. Maternal stress may thus have carry-over effects on progeny if it influences pre-natal offspring environment in terms of glucocorticosteroid concentration, although this hypothesis has never been tested in any species under field conditions. We manipulated stress experienced by female barn swallows Hirundo rustica, by exposing them to a predator during laying and measured egg corticosterone concentration. Stressed females laid eggs with greater corticosterone concentration than controls exposed to a herbivore. In another experiment, we injected physiological doses of corticosterone in the egg albumen and compared the phenotype of offspring originating from these eggs with their control siblings originating from either sham-inoculated or unmanipulated eggs and reared in the same nest. Eggs injected with corticosterone had lower hatchability and produced fledglings with smaller body size and slower plumage development than did control eggs. Nestling body size in our study population predicts long-term survival. Thus, maternal stress impaired offspring phenotype and viability by increasing transmission of glucocorticosteroids to the eggs. This study identifies a novel mechanism mediating early maternal effects whereby maternal stress affects offspring quality. These results are relevant to biological conservation because they disclose a mechanism that can link environmental conditions to population productivity and viability.