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.     

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.     

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.     

Larger eggs at lower water temperature as a measure to assure effective hatchling size in the landlocked form of Ayu, <Emphasis Type="Italic">Plecoglossus altivelis</Emphasis>

Egg size is a critical life-history trait in which maternal investment is optimized to maximize maternal fitness. The adaptive significance of variable egg size among spawning groups of Ayu (Plecoglossus altivelis) landlocked in the Lake Biwa system was examined through field investigations and rearing experiments. Observed egg size variations were explained by the water temperature around spawning grounds established near the mouths of inlet streams. Two typical streams with different incubation temperatures showed similar maternal body sizes and hatchling sizes, but eggs attached to the stream bed were larger in the colder stream. An experiment that used eggs from a single clutch showed that a smaller hatchling size was obtained with a lower incubation temperature, indicating that the effect of differences in egg size on hatchling size can be canceled out by variations in incubation temperature. In general, larvae that are less than a certain threshold of effective body size are not expected to be assured of early success among conspecifics competing for foods. It is proposed that environments in which the incubation temperature varies favor variability in egg size to ensure that sufficient food is accessible to larvae.     

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.     

A lengthy solution to the optimal propagule size problem in the large-bodied South American freshwater turtle, <Emphasis Type="Italic">Podocnemis unifilis</Emphasis>

In oviparous vertebrates lacking parental care, resource allocation during reproduction is a major maternal effect that may enhance female fitness. In general, resource allocation strategies are expected to follow optimality models to solve the energy trade-offs between egg size and number. Such models predict that natural selection should optimize egg size while egg number is expected to vary with female size, thus maximizing offspring fitness and consequently, maternal fitness. Deviations from optimality predictions are commonly attributed to morphological constraints imposed by female size, such as reported for small-bodied turtle species. However, whether such anatomical constraints exist in smaller-bodied females within large-bodied clades remains unstudied. Here we tested whether resource allocation of the river turtle Podocnemis unifilis (a relatively smaller member of the large-bodied Podocnemididae) follows optimality theory, and found a pattern of egg elongation in smaller females that provides evidence of morphological constraints and of a reproductive trade-off with clutch size, whereas egg width supports the existence of an optimal egg size and no trade-off. Moreover, larger females laid larger clutches composed of rounder eggs, while smaller females laid fewer and relatively more elongated eggs. Elongated eggs from smaller females have larger volume relative to female size and to round eggs of equal width. We propose that elongated eggs represent a solution to a potential morphological constraint suffered by small females. Our results suggest that larger females may optimize fitness by increasing the number of eggs, while smaller females do so by producing larger eggs. Our data supports the notion that morphological constraints are likely more widespread than previously anticipated, such that they may not be exclusive of small-bodied lineages but may also exist in large-bodied lineages.     

Why does a grasshopper have fewer,larger offspring at its range limits?

Analysis of size of offspring reared through three laboratory generations from populations of the field grasshopper Chorthippus brunneus from 27 sites around the British Isles showed that offspring were larger towards the cooler-wetter conditions in the western and northern limits of the range. This variation had a significant genetic component. There was a trade-off between clutch size and offspring size between and within populations. Under favourable thermal and feeding conditions maternal fitness was optimal when individuals produced the largest clutches of the smallest eggs, but under poor conditions maternal fitness was optimal when individuals produced small clutches of very large offspring. Calculation of geometric mean fitness over time indicated that having larger offspring near to the edge of the range could be advantageous as a conservative risk-spreading strategy. As well as geographic variation in egg size, significant environment-genotype interactions in egg size in relation to temperature were observed.     

Sexual dimorphism of egg size in the European Blackbird Turdus merula

Recently, a number of studies have shown that female birds are able to control the sex of their progeny at the stage of the gamete. There is also some evidence that females adjust their investment in offspring depending on the sex of the embryo during egg formation. Differential maternal investment to the eggs depending on their sex is usually interpreted as an adaptive strategy, by which females can increase competitive abilities of the smaller sex, or preferentially invest towards the sex with the potentially higher fitness returns. Here, we studied variation in egg size in relation to embryo sex and laying order in the European Blackbird Turdus merula. We found male and female eggs to differ in size, with larger eggs containing male embryos, as well as a significant interaction between embryo sex and laying order. This interaction resulted from the fact that egg size increased with the laying sequence among eggs bearing females but did not change with laying order among eggs bearing males. There was no relationship between offspring sex and the laying sequence within a clutch. We suggest that sexual dimorphism in egg size recorded in the European Blackbird may reflect favouritism of the sex which may give higher fitness returns.     

Variation in body size in the giant rhinoceros beetle Trypoxylus dichotomus is mediated by maternal effects on egg size

1. The egg size of insects can vary depending on maternal body size or resource status, and it may influence offspring body size by determining initial resource level. 2. The giant rhinoceros beetle Trypoxylus dichotomus exhibits considerable variation in body size, some of which is attributed to the variation in larval food (humus) quality, although a substantial amount of variation in body size remains unexplained. In the present study, changes in the egg size and offspring body size in response to several maternal variables were examined (i.e. body size, age, and, nutritional status). 3. Nutritional intake of the females during the adult stage did not affect the egg size. Larvae hatched from small eggs partially recovered from the initial disadvantage during their ontogenetic processes by increasing growth rate (i.e. compensatory growth); however, there was still a positive relationship between egg size and pupal body size. 4. Older females produced small eggs, but because of compensatory growth, the pupae were no longer small. By contrast, due to a lack of compensatory growth, small females produced small eggs as well as small pupae. 5. These results suggest that maternal body size affects offspring body size through effects on egg size. This transgenerational effect may account for some of the variation in adult body size of T. dichotomus.     

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.     

The effect of inbreeding on natural selection in a seed‐feeding beetle

Little is known about how inbreeding alters selection on ecologically relevant traits. Inbreeding could affect selection by changing the distribution of traits and/or fitness, or by changing the causal effect of traits on fitness. Here, I test whether selection on egg size varies with the degree of inbreeding in the seed‐feeding beetle, Stator limbatus. There was strong directional selection favoring large eggs for both inbred and outbred beetles; offspring from smaller eggs had lower survivorship on a resistant host. Inbreeding treatment had no effect on the magnitude of selection on egg size; all selection coefficients were between ~0.078 and 0.096, regardless of treatment. However, inbreeding depression declined with egg size; this is because the difference in fitness between inbreds and outbreds did not change, but average fitness increased, with egg size. A consequence of this is that populations that differ in mean egg size should experience different magnitudes of inbreeding depression (all else being equal) and thus should differ in the magnitude of selection on traits that affect mating, simply as a consequence of variation in egg size. Also, maternal traits (such as egg size) that mediate stressfulness of the environment for offspring can mediate the severity of inbreeding depression.     

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.     

Egg size and composition in an ageing capital breeder – consequences for offspring performance

1. Egg size is often used as a proxy of egg quality although size and composition may vary, e.g. in insects egg size usually decreases as female ages. Whether this decrease in size reflects reduced concentrations of essential nutrients such as lipids and proteins of eggs laid by ageing females, or does reduced size per se explain often observed lower fitness of later laid eggs is poorly explored. 2. Egg properties were compared with fitness parameters of offspring laid on the first and fourth night during the oviposition period of a capital breeding moth, Cleorodes lichenaria (Hufnagel). The study aim was to explore whether decreased egg size is caused by decreased provisioning into later laid eggs measured as egg protein and lipid concentration, and whether it results in lower fitness of later laid offspring. 3. The fresh and dry weight of eggs decreased over the oviposition period, but the protein and lipid concentration remained constant. Survival of larvae was lower among the fourth night laid offspring on a low quality host Parmelia sulcata Taylor compared to a high quality host Ramalina fraxinea (L.) Ach. No differences were observed in egg fertility or hatchability, neonate survival without food and pupal mass between the offspring produced on different nights. 4. Decreased survival of offspring produced later was rather attributable to absolute provisioning (i.e. lower weight of eggs) than relative provisioning (i.e. decreased concentrations of nutrients in eggs). It is argued that lower survival of later laid smaller eggs on low quality diet is likely attributable to physical and chemical characteristics of host lichens and/or physical properties of tiny neonate larvae.     

Intergenerational effect of juvenile hormone on offspring in <Emphasis Type="Italic">Pogonomyrmex</Emphasis> harvester ants

Parents can influence the phenotypes of their offspring via a number of mechanisms. In harvester ants, whether female progeny develop into workers or daughter queens is strongly influenced by the age and temperature conditions experienced by their mother, which is associated with variation in maternal ecdysteroid deposition in fertilized eggs. In many insects, juvenile hormone (JH) is antagonistic to ecdysteroid release, suggesting that seasonal and age-based variation in maternal JH titers may explain maternal effects on offspring size and reproductive caste. To test this hypothesis, we artificially increased maternal JH titers with methoprene, a JH analog, in laboratory colonies of two Pogonomyrmex populations exhibiting genetic caste determination. Increasing maternal JH resulted in a 50% increase in worker body size, as well as a sharp reduction in total number of progeny reared, but did not alter the genotype of progeny reared to adulthood. The intergenerational effect of JH manipulation was not mediated by a reduction in ecdysteroid deposition into eggs; instead, changes in egg size, trophic egg availability or brood/worker ratio may have altered the nutritional environment of developing larvae. Egg ecdysteroid content was significantly negatively correlated with natural variation in worker body size, however, suggesting that there are multiple independent routes by which queens can modify offspring phenotypes.     

Fitness consequences of egg-size variation in the lesser snow goose

We investigated the relationship between eggsize variation and (a) egg hatching success, (b) chick survival to fledging and recruitment, and (c) adult female survival, over 12 years in the lesser snow goose (Anser caerulescens caerulescens). By comparing the means and variances of egg size for successful and unsuccessful eggs, our aim was to assess the relative fitness of eggs of different sizes and to determine the type of selection operating on egg size in this species. As both egg size and reproductive success vary with age in the lesser snow goose we controlled for the effects of female age. Egg-size variation is very marked in this population, varying by up to 52% for eggs hatching successfully. However, there was no relationship between egg size and post-hatching survival of goslings to fledging or recruitment, either within or between broods, pooling across years. Egg size varied significantly between successful and unsuccessful clutches in only 2 of 33 individual year comparisons. First-laid eggs surviving to onset of incubation, and eggs hatching successfully, were on average larger than unsuccessful eggs, but this was probably due to the confounding effects of female age-specific and sequence-specific egg survival. Variance of egg size differed significantly between successful and unsuccessful eggs in only 3 of 24, and 0 of 21, individual year comparisons for pre- and post-hatching survival respectively. We therefore found little evidence for a relationship between egg-size variation and offspring fitness, or for strong directional, normalising or diversifying selection operating on egg size, in the lesser snow goose. In addition, there was only weak support for the hypothesis that egg-size variation is maintained by temporal variation in selection pressure (sensu Ankney and Bisset 1973). It is likely that egg-size variation represents the pleiotropic expression of alleles affecting more general physiological or metabolic processes. While this does not rule out the existence of alleles with more direct effects on egg size we suggest that their contribution to heritable egg size is small.     

Geographic variation in offspring size of a widespread lizard (Takydromus septentrionalis): importance of maternal investment

Geographic variation in offspring size is widespread, but the proximate causes of this variation have not yet been explicitly determined. We compared egg size and egg contents among five populations of a lizard (Takydromus septentrionalis, Günther, 1864) along a latitudinal gradient, and incubated eggs at two temperatures to determine the influence of maternal investment and incubation temperature on offspring size. The mean values for female size and egg size were both greater in the two northern populations (Chuzhou and Anji) than in the three southern populations (Lishui, Dongtou, and Ningde). The larger eggs were entirely attributable to the body size of females in the Anji population, but their increased size also stemmed from further enlargement of egg size relative to female body size in Chuzhou, the northernmost population sampled in this study. Eggs of the Chuzhou population contained more yolk and less water than those of southern populations. Despite the lower lipid content in the yolk, eggs from the Chuzhou population had higher energy contents than those from the two southern populations, owing to the larger egg size and increased volume of yolk. Hatchling size was not affected by incubation temperature, but differed significantly among populations, with hatchlings being larger in the Chuzhou population than in the other populations. Our data provide an inference that oviparous reptiles from cold climates may produce larger offspring, not only by increasing egg size but also by investing more energy into their eggs. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 59–67.     

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.     

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.     

Relationships between oviposition date, hatch date, and offspring size in the grasshopper Chorthippus brunneus

Abstract 1. The grasshopper Chorthippus brunneus has been shown to increase egg size with maternal age under constant laboratory conditions, such that late-laid eggs are larger than early laid eggs. In this study, an increase in the size of eggs (and hatchlings from those eggs) was recorded with date of oviposition in a field cage population. This suggests that the relationship between maternal age and egg size, observed previously in the laboratory, also occurs in the field. There was, however, some evidence that the behaviour of the maternal females in field cages was modified by the onset of autumnal weather at the end of the breeding season. Only a small number of eggs was laid in the last 3 weeks of the summer but these yielded relatively small hatchlings.
2. The date on which eggs were laid was correlated positively with their date of hatch in the following year. A consequence of this relationship, and that between oviposition date and egg size, was that size at hatch increased with date of hatch through most of the spring but then declined as the last few eggs hatched. Temporal variation in size at hatch parallelled temporal variation in the maternal females' investment in egg size in the previous year.
3. An undisturbed field population was monitored to assess whether the temporal variation in size at hatch resulted in size variation at eclosion in subsequent developmental stages. There were negative correlations between size at eclosion and date of eclosion at the third and fourth instars, suggesting that despite their smaller size at hatch, early hatchers experienced more favourable conditions for juvenile growth than late hatchers. The larger size at hatch of late hatchers may enhance their survival and compensate (albeit incompletely) for their reduced opportunity for growth. Female reproductive behaviour may represent an adaptive response to a predictable seasonal decline in offspring fitness at hatch.     

Maternal resource variation across the laying sequence in Canada geese Branta canadensis maxima

Variation in maternal investments to offspring presumably reflects an optimization of resource allocation such that a female's fitness is maximized. In birds, both egg size and yolk constituents are examples of resources that can vary among offspring within a clutch. Egg size and maternally-derived steroid hormone concentrations present in yolk have been characterized for many species that lay small clutches or have altricial young, but little information is available for species that lay moderate to large clutches of precocial young. In this study, we recorded laying position, measured fresh egg mass and determined maternally-derived testosterone and estradiol concentrations present in yolks for whole clutches of free-living Canada geese Branta canadensis maxima to assess variation in maternal resources within clutches. We found that egg size varied non-linearly across the laying sequence such that first laid eggs were small, the largest eggs in the clutch occurred in the second and third positions, and size declined in eggs laid in subsequent positions. Concentration of testosterone in the yolk followed a pattern in which the first and second laid eggs have the highest concentrations within a clutch and declining concentrations in subsequently laid eggs. In contrast, maternally-derived yolk estradiol concentrations (measured in a subset of clutches) did not change across the laying sequence.