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.     

THE EVOLUTION OF MATERNAL INVESTMENT IN LIZARDS: AN EXPERIMENTAL AND COMPARATIVE ANALYSIS OF EGG SIZE AND ITS EFFECTS ON OFFSPRING PERFORMANCE

I used comparative and experimental analysis of egg size in a Sceloporus lizard to examine a fundamental tenet of life-history theory: the presumed trade-offs among offspring number, offspring size, and performance traits related to offspring size that are likely to influence fitness. I analyzed latitudinal and elevational patterns of egg life-history characteristics among populations and experimentally manipulated egg size and hatchling size by removing yolk from the eggs to examine the causal bases of population differences in offspring traits. Mean clutch size among populations increased to the north (seven vs. 12 eggs/clutch, California vs. Washington), whereas egg size decreased (0.65 g vs. 0.40 g). The elevational patterns in southern California paralleled the latitudinal trends. Several offspring life-history traits that are correlated with egg size also varied geographically; these traits included incubation time, hatchling size, growth rate, and hatchling sprint performance. Hatchling viability of experimentally reduced eggs was remarkably high (~70%), even when up to 50% of the yolk was removed. The experimentally reduced eggs and hatchlings demonstrated the degree to which size influences each of the offspring life-history traits considered. Northern eggs hatched sooner, in part because of their small size. Though growth rate is allometrically related to size within each population (i.e., smaller hatchlings grow faster on a mass-specific basis), population differences in growth rate, as measured in the laboratory, are likely to reflect genetic differentiation in the underlying physiology of growth. Moreover, smaller juveniles, because of experimental reduction, had slower sprint speeds than larger juveniles. The slower sprint speed of hatchlings from Washington compared to hatchlings from California is thus largely due to the fact that eggs are smaller in the Washington population. These results provide a basis for interpreting the evolutionary divergence of the suite of traits involved in the evolution of maternal investment per offspring in lizards. For example, evolutionary divergence in some offspring traits functionally related to size (e.g., sprint speed) may be constrained, relative to traits that are determined by other aspects of development or physiology (e.g., growth). I also discuss issues relating to the evolution of maternal investment that could be tested in laboratory and natural populations using experimentally reduced offspring.     

Differential effects of offspring and maternal inbreeding on egg laying and offspring performance in the burying beetle Nicrophorus vespilloides

We investigate the effect of offspring and maternal inbreeding on maternal and offspring traits associated with early offspring fitness in the burying beetle Nicrophorus vespilloides. We conducted two experiments. In the first experiment, we manipulated maternal inbreeding only (keeping offspring outbred) by generating mothers that were outbred, moderately inbred or highly inbred. Meanwhile, in the second experiment, we manipulated offspring inbreeding only (keeping females outbred) by generating offspring that were outbred, moderately inbred or highly inbred. In both experiments, we monitored subsequent effects on breeding success (number of larvae), maternal traits (clutch size, delay until laying, laying skew, laying spread and egg size) and offspring traits (hatching success, larval survival, duration of larval development and average larval mass). Maternal inbreeding reduced breeding success, and this effect was mediated through lower hatching success and greater larval mortality. Furthermore, inbred mothers produced clutches where egg laying was less skewed towards the early part of laying than outbred females. This reduction in the skew in egg laying is beneficial for larval survival, suggesting that inbred females adjusted their laying patterns facultatively, thereby partially compensating for the detrimental effects of maternal inbreeding on offspring. Finally, we found evidence of a nonlinear effect of offspring inbreeding coefficient on number of larvae dispersing. Offspring inbreeding affected larval survival and larval development time but also unexpectedly affected maternal traits (clutch size and delay until laying), suggesting that females adjust clutch size and the delay until laying in response to being related to their mate.     

Life-history consequences of egg size in Drosophila melanogaster

We used a novel approach to study the effects of egg size on offspring fitness components in Drosophila melanogaster. Populations that differed genetically in egg size were crossed, and the female offspring from these reciprocal crosses were examined for life-history traits. These flies expressed effects of egg size, because they developed from eggs of different sizes as a result of maternal genetic effects, but displayed an equivalent range of nuclear genetic variation. The crosses used four independent pairs of outbred populations that differed in the pattern of covariation between egg size and life-history traits, so that the maternal genetic effects of egg size on offspring characters could be contrasted to the associations present among the parental populations. Egg size showed positive maternal genetic effects on embryonic viability and development rate, hatchling weight and feeding rate, and egg-larva and egg-adult development rate but no consistent effects on larval competitive ability, adult weight, or egg size in the offspring. Our method revealed a pattern of causality that could not be deduced from interpopulation comparisons and therefore provides a good way of disentangling the causes and consequences of variation in egg size while controlling for zygotic genetic effects.     

Maternal investment in egg size: environment- and population-specific effects on offspring performance

Geographic variation in maternal investment in offspring size can be adaptive if differences in investment translate into improved offspring performance in the given environments. We compared two moor frog, Rana arvalis, populations in the laboratory to test the hypothesis that investment in large eggs in populations originating from stressful (acid) environments improves offspring performance when reared in stressful (acid) conditions. We found that large initial size (hatchling mass) had moderate to strong, environment-dependent positive effects on larval and metamorphic traits in the acidic origin population, but only weak effects in the neutral origin population. Our results suggest that interactions between environmental conditions and initial size can be important determinants of individual performance, and that investment in large eggs is adaptive in acid environments. These findings emphasize the role of maternal effects as adaptations to environmental stress.     

Geographic variation in hatchling size in an oviparous skink: effects of maternal investment and incubation thermal environment

Geographic variation in offspring size can be viewed as an adaptive response to local environmental conditions, but the causes of such variation remain unclear. Here, we compared the size and composition of eggs laid by female Chinese skinks (Plestiodon chinensis) from six geographically distinct populations in southeastern China to evaluate geographic variation in hatchling size. We also incubated eggs from these six populations at three constant temperatures (24, 28 and 32 °C) to evaluate the combined effects of incubation temperature and population source on hatchling size. Egg mass and composition varied among populations, and interpopulation differences in yolk dry mass and energy content were still evident after accounting for egg mass. Population mean egg mass and thus hatchling mass were greater in the colder localities. Females from three northern populations increased offspring size by laying larger eggs relative to their own size. Females from an inland population in Rongjiang could increase offspring size by investing relatively more dry materials and thus more energy into individual eggs without enlarging the size of their eggs. The degree of embryonic development at oviposition was almost the same across the six populations, so was the rate of embryonic development and thus incubation length at any given temperature. Both incubation temperature and population source affected hatchling traits examined, but the relative importance of these two factors varied between traits. Our data show that in P. chinensis hatchling traits reflecting overall body size (body mass, snout‐vent length and tail length) are more profoundly affected by population source. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 283–296.     

Access to multiple mates increases fecundity but does not affect per‐offspring maternal investment in a marine gastropod

Females of many organisms mate more than once and with more than one male, suggesting that polyandry confers some advantage to the female or her offspring. However, variation in maternal investment in response to mate choice and mate number can confound efforts to determine if there are benefits of polyandry. Access to multiple mates could increase maternal investment in offspring via a number of different mechanisms. Few studies have determined if investment is influenced by mate choice and number, and data are particularly lacking for marine invertebrates. This study was designed to determine if maternal investment and offspring size increase with access to increasing numbers of mates in the protandrous intertidal slipper snail Crepidula cf. marginalis. Virgin female slipper limpets were exposed to one, three, or five potential mates and their fecundity, egg size, and hatchling size were measured for multiple clutches. Treatment had a significant effect on fecundity, with fecundity increasing with the number of potential mates. Treatment did not have an effect on the size of eggs or hatchlings, on the variation in egg size or hatchling size within broods, or on the frequency of oviposition. Treatment did alter the variation in average offspring size among females, but not in the way predicted by theory. The main result, that access to multiple mates does not have an effect on per offspring maternal investment, makes C. cf. marginalis an ideal candidate to study the effects of polyandry on offspring fitness without having to take into account confounding effects of variation in maternal investment.     

The evolution of offspring size and number: a test of the Smith-Fretwell model in three species of crickets

Most models of parental investment in offspring assume a trade-off between propagule size and number, and an increasing concave down function relating offspring fitness to propagule size. In this study, we test these two fundamental assumptions, using three closely related species of crickets, Gryllus firmus, G. veletis, and G. pennsylvanicus. Egg weight, 35-day fecundity and 35-day egg biomass were estimated in a population of each species, and the relationships between these reproductive traits and date of egg laying and body size were estimated. The relationships between egg weight and offspring survival were also sought for eggs buried at different depths, soil moistures, and soil types (G. firmus and G. veletis), as well as in the field (G. pennsylvanicus). A trade-off between egg weight and 35-day fecundity was revealed in a multivariate analysis taking into account among-species variation in egg weight and body size. Independent of the environmental conditions affecting the eggs, a positive correlation existed between the number of larvae that emerged from the soil and propagule weight in each species. Therefore, these findings provide partial support for the assumptions considered in the models mentioned above. A single optimal egg size was favored in two out of the three sets of conditions in which the functions relating egg weight to larval survival could be derived. The conditions encountered by the eggs, however, influenced the average survival of the larvae, as well as the shape of the relationship between egg weight and offspring survival. This suggests that cricket eggs frequently face heterogeneous environments with respect to egg and hatchling survival; the implication of habitat heterogeneity on the evolution of an optimal egg size is considered. The relationships between the reproductive components and female age and size, as well as between egg size and variation in cricket life-history, are discussed in an ecological and evolutionary context.     

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.     

Nonlinear continuum of egg size-number trade-offs in a snake: is egg-size variation fitness related?

The relationship between offspring size and offspring number is crucial to life history evolution. To examine how these two life history variables are coupled and whether an altered balance between them will result in changes in maternal fitness, we manipulated clutch size of the Chinese cobra (Naja atra) by using the techniques of hormonal manipulation and follicle ablation. Females receiving exogenous follicle-stimulating hormone produced more but smaller eggs, and females undergoing follicle ablation produced fewer but larger eggs. Neither body size (body mass and snout-vent length) at hatching nor egg mass at oviposition had a role in determining hatchling survival and growth. Female hatchlings were more likely to die in early post-hatching days and grew more slowly than male hatchlings. Our data show that: (1) there is a nonlinear continuum of egg size-number trade-offs in N. atra within which there is a single inflexion where the rate at which egg size decreases with increasing clutch size, or clutch size increases with decreasing egg size, is maximized; (2) there is a fixed upper limit to egg size for a given-sized female, and the limit is not determined by her body volume; (3) egg size has no role in determining hatchling survival and growth; and (4) the extent to which females may enjoy reproductive benefits in a given reproductive episode depends on how well egg size and egg number are balanced.     

Differentiated egg size of the cannibalistic salamander <Emphasis Type="Italic">Hynobius retardatus</Emphasis>

Larvae of the salamander, Hynobius retardatus, are carnivorous, and even though there are two morphs, a typical morph and a broad-headed or “cannibal” morph, both are cannibalistic. They also sometimes eat other large prey, for example larvae of the frog, Rana pirica. In natural habitats, use of both conspecific and R. pirica larvae as food may contribute more strongly to high survival and substantially to fitness when larval densities are higher, because early-stage H. retardatus larvae sometimes experience scarcity of their typical prey. In cannibalistic oviparous amphibians, larger individuals that developed from larger eggs can more efficiently catch and consume larger prey and thus their survival may be better than that of smaller individuals developed from smaller eggs. Populations might therefore diverge in respect of egg size in response to variation in the density of conspecific and R. pirica larvae in natural ponds, with eggs being larger when larval density is higher. I examined how variance in hatchling size correlated with the incidence of cannibalism, and whether increasing larval density in natural ponds correlated with increasing egg size. Variance in initial larval body size facilitated cannibalism, and egg size increased as larval density in the ponds increased. In ponds with high larval density, where cannibalism and large prey consumption is a critical factor in offspring fitness, the production of fewer clutches with larger eggs, and thus of fewer and larger offspring, results in greater maternal fitness. Variation among the mean egg size in populations is likely to represent a shift in optimum egg size across larval density gradients.     

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.     

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.     

COOPERATIVE BREEDING FAVORS MATERNAL INVESTMENT IN SIZE OVER NUMBER OF EGGS IN SPIDERS

The transition to cooperative breeding may alter maternal investment strategies depending on density of breeders, extent of reproductive skew, and allo‐maternal care. Change in optimal investment from solitary to cooperative breeding can be investigated by comparing social species with nonsocial congeners. We tested two hypotheses in a mainly semelparous system: that social, cooperative breeders, compared to subsocial, solitarily breeding congeners, (1) lay fewer and larger eggs because larger offspring compete better for limited resources and become reproducers; (2) induce egg size variation within clutches as a bet‐hedging strategy to ensure that some offspring become reproducers. Within two spider genera, Anelosimus and Stegodyphus, we compared species from similar habitats and augmented the results with a mini‐meta‐analysis of egg numbers depicted in phylogenies. We found that social species indeed laid fewer, larger eggs than subsocials, while egg size variation was low overall, giving no support for bet‐hedging. We propose that the transition to cooperative breeding selects for producing few, large offspring because reproductive skew and high density of breeders and young create competition for resources and reproduction. Convergent evolution has shaped maternal strategies similarly in phylogenetically distant species and directed cooperatively breeding spiders to invest in quality rather than quantity of offspring.     

High variability in egg size and energetic content among intertidal mussels

Maternal investment is a fundamentally important parameter in life-history theory and models, yet the scales at which it varies (among individuals vs. among populations) is rarely reported. In this study, variability in attributes of eggs and early larvae of Mytilus californianus was examined from four sites spanning Point Conception, California, in June and September 2001. The effects of female, site, and month were examined for the following variables: egg volume (microl), egg energy content (microg carbon per egg), and initial larval size (microm). The only significant effect on both egg traits was that of female. Females differed by up to 57% in mean egg volume and 116% in mean egg energetic content. Although there were significant effects of rearing environment, female, site, and month on initial larval size, variability in larval length was small compared to the egg traits. Mean larval length was maximally 11% different among females. Neither female body weight nor length was correlated to mean offspring traits, and there were also no significant relationships between egg traits and initial larval size. The primary source of variation in maternal investment in this system appears to be among individual females rather than over space or time.     

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.     

MATERNAL EFFECTS AND THE PERVASIVE IMPACT OF NESTLING HISTORY ON EGG SIZE IN A PASSERINE BIRD

Environmental conditions experienced during ontogeny may have important and permanent consequences for life-history traits of individuals. The aim of this work was to determine whether conditions experienced during early life, as expressed by prefledgling condition, have any bearing on the volume of eggs subsequently laid by females in a small passerine bird species, the pied flycatcher (Ficedula hypoleuca). I first show a genetic influence on egg volume by dam-offspring regression. The existence of maternal effects is shown by comparing resemblances between average egg volumes of offspring to those of their paternal and maternal grandmothers. Path analysis shows that when controlling for the influence of maternal egg volume, the average volume of eggs produced in a lifetime is positively related to the body condition of a female measured while she is still at the nest. Thus, body condition at fledgling affects egg volume beyond the ability of maternal egg volume to predict offspring egg volume. Although there may be a persistent maternal effect of egg volume on itself or linked to a property correlated with egg volume, the maternal performance trait involved remains unknown, except for maternal egg volume itself. Given the effects that egg volume may have on reproductive success, which are partly determined prior to leaving the nest, maternal effects may have important consequences for lifetime fitness of offspring.     

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

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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.     

The influence of maternal age and mating frequency on egg size and offspring performance in Callosobruchus maculatus (Coleoptera: Bruchidae)

Maternal age influences offspring quality of many species of insects. This observed maternal age influence on offspring performance may be mediated through maternal age effects on egg size, which in turn may be directly influenced by the female's nutritional state. Thus, behaviors that influence a female's nutritional status will indirectly influence egg size, and possibly offspring life histories. Because males provide nutrients to females in their ejaculate, female mating frequency is one behavior which may influence her nutritional status, and thus the size of her eggs and the performance of her offspring. In this paper, I first quantify the influences of maternal age on egg size and offspring performance of the bruchid beetle, Callosobruchus maculatus. I then examine whether nutrients transferred during copulation reduce the magnitude of maternal age effects on egg size and larval performance when mothers are nutrient-stressed. Egg size and egg hatchability decreased, and development time increased, with increasing maternal age. Multiple mating and adult feeding by females both resulted in increased egg size. This increase in egg size of females mated multiply did not translate into reduced development time or increased body size and egg hatchability, but did correlate with improved survivorship of offspring produced by old mothers. Thus, it appears that because the influence of mating frequency on egg size is small relative to the influence of maternal age, the influence of nutrients derived from multiple mating on offspring life history is almost undetectable (detected only as a small influence on survivorship). For C. maculatus, female multiple mating has been demonstrated to increase adult female survivorship (Fox 1993a), egg production (Credland and Wright 1989; Fox 1993a), egg size, and larval survivorship, but, contrary to the suggestion of Wasserman and Asami (1985), multiple mating had no detectable influence on offspring development time or body size.