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.     

Variation in cannibalistic polyphenism between populations in the salamander Hynobius retardatus

Organisms sometimes change their phenotype to maximize fitness according to local environments. If the frequency of the broad-headed "cannibal" morph in the larvae of the salamander Hynobius retardatus has been evolutionarily maintained at a certain level within a population as a result of local adaptation, variations in its frequency should be found among different populations with environmental variation. We investigated whether variations in the frequency of the broad-headed morph were present in 2 different populations, Nopporo (a low-density population) and Erimo (a high-density population), by raising larvae from the respective populations under the same experimental conditions. The occurrence rate of the broad-headed "cannibal" morph was significantly different between the 2 populations when examined with different experimental larval densities. These results suggest that the reaction norm with respect to the frequency of the broad-headed morph is different between the Nopporo and Erimo populations. Because the local populations are assumed to be selected for under different environments, the different reaction norm might have evolved in response to different selection pressures.     

Maternal body condition influences magnitude of anti-predator response in offspring

Organisms exhibit plasticity in response to their environment, but there is large variation even within populations in the expression and magnitude of response. Maternal influence alters offspring survival through size advantages in growth and development. However, the relationship between maternal influence and variation in plasticity in response to predation risk is unknown. We hypothesized that variation in the magnitude of plastic responses between families is at least partly due to maternal provisioning and examined the relationship between maternal condition, egg provisioning and magnitude of plastic response to perceived predation risk (by dragonfly larvae: Aeshna spp.) in northern leopard frogs (Lithobates pipiens). Females in better body condition tended to lay more (clutch size) larger (egg diameter) eggs. Tadpoles responded to predation risk by increasing relative tail depth (morphology) and decreasing activity (behaviour). We found a positive relationship between morphological effect size and maternal condition, but no relationship between behavioural effect size and maternal condition. These novel findings suggest that limitations imposed by maternal condition can constrain phenotypic variation, ultimately influencing the capacity of populations to respond to environmental change.     

A tadpole-induced polyphenism in the salamander Hynobius retardatus

Abstract.— Larvae of the salamander Hynobius retardatus have two distinct morphs: normal and broad-headed, cannibal morphs. We performed three experiments to differentiate among the following hypotheses: The broad-headed morph is induced to allow: (1) feeding on nutritious conspecifics; (2) exclusion of strong competitors for food or space; or (3) feeding on large, tough prey when smaller prey items are unavailable. When newly hatched larvae were reared with a heterospecific, Rana pirica (an anuran amphibian) tadpoles, the broad-headed morph was induced more frequently compared with those reared with conspecifics. The phenotype expressed depended on the size of the tadpoles: The broad-headed morph occurred more frequently with small and the normal morph with large tadpoles. Metamorphosis occurred sooner in larvae fed conspecifics compared with those fed heterospecific tadpoles, and the mean growth rate of larvae fed conspecifics was significantly faster than that of those fed tadpoles, suggesting that the heterospecific tadpoles were less nutritive than the conspecifics. These results do not support the hypotheses that the broad-headed morph evolved for consuming conspecifics because of their better balance of nutrients or for excluding strong competitors for food or space. We tentatively conclude that the morph evolved to eat large, tough prey, including both conspecifics and heterospecific tadpoles. Because H. retardatus usually spawns very early in the spring in small ponds partially covered with ice and snow, newly hatched larvae may starve from the lack of proper food owing to extremely low water temperatures. Thus, the broad-headed morph of H. retardatus may represent a cold-habitat adaptation to overcome the severe circumstance when the only food items available are relatively large conspecifics or heterospecific tadpoles.     

Phenotypic plasticity in growth and fecundity induced by strong population fluctuations affects reproductive traits of female fish

Fish are known for their high phenotypic plasticity in life‐history traits in relation to environmental variability, and this is particularly pronounced among salmonids in the Northern Hemisphere. Resource limitation leads to trade‐offs in phenotypic plasticity between life‐history traits related to the reproduction, growth, and survival of individual fish, which have consequences for the age and size distributions of populations, as well as their dynamics and productivity. We studied the effect of plasticity in growth and fecundity of vendace females on their reproductive traits using a series of long‐term incubation experiments. The wild parental fish originated from four separate populations with markedly different densities, and hence naturally induced differences in their growth and fecundity. The energy allocation to somatic tissues and eggs prior to spawning served as a proxy for total resource availability to individual females, and its effects on offspring survival and growth were analyzed. Vendace females allocated a rather constant proportion of available energy to eggs (per body mass) despite different growth patterns depending on the total resources in the different lakes; investment into eggs thus dictated the share remaining for growth. The energy allocation to eggs per mass was higher in young than in old spawners and the egg size and the relative fecundity differed between them: Young females produced more and smaller eggs and larvae than old spawners. In contrast to earlier observations of salmonids, a shortage of maternal food resources did not increase offspring size and survival. Vendace females in sparse populations with ample resources and high growth produced larger eggs and larvae. Vendace accommodate strong population fluctuations by their high plasticity in growth and fecundity, which affect their offspring size and consequently their recruitment and productivity, and account for their persistence and resilience in the face of high fishing mortality.     

THE EVOLUTIONARY GENETICS OF AN ADAPTIVE MATERNAL EFFECT: EGG SIZE PLASTICITY IN A SEED BEETLE

In many organisms, a female's environment provides a reliable indicator of the environmental conditions that her progeny will encounter. In such cases, maternal effects may evolve as mechanisms for transgenerational phenotypic plasticity whereby, in response to a predictive environmental cue, a mother can change the type of eggs that she makes or can program a developmental switch in her offspring, which produces offspring prepared for the environmental conditions predicted by the cue. One potentially common mechanism by which females manipulate the phenotype of their progeny is egg size plasticity, in which females vary egg size in response to environmental cues. We describe an experiment in which we quantify genetic variation in egg size and egg size plasticity in a seed beetle, Stator limbatus, and measure the genetic constraints on the evolution of egg size plasticity, quantified as the genetic correlation between the size of eggs laid across host plants. We found that genetic variation is present within populations for the size of eggs laid on seeds of two host plants (Acacia greggii and Cercidium floridum; h² ranged between 0.217 and 0.908), and that the heritability of egg size differed between populations and hosts (higher on A. greggii than on C. floridum). We also found that the evolution of egg size plasticity (the maternal effect) is in part constrained by a high genetic correlation across host plants (r_G > 0.6). However, the cross-environment genetic correlation is less than 1.0, which indicates that the size of eggs laid on these two hosts can diverge in response to natural selection and that egg size plasticity is thus capable of evolving in response to natural selection.     

Population consequences of maternal effects: sex‐bias in egg‐laying order facilitates divergence in sexual dimorphism between bird populations

Abstract When costs and benefits of raising sons and daughters differ between environments, parents may be selected to modify their investment into male and female offspring. In two recently colonized environments, breeding female house finches (Carpodacus mexicanus) modified the sex and growth of their offspring in relation to the order in which eggs were laid in a clutch. Here we show that, in both populations, these maternal effects strongly biased frequency distribution of tarsus size of fully grown males and females and ultimately produced population divergence in this trait. Although in each population, male and female offspring show a wide range of growth patterns, maternal modifications of sex‐ratio in relation to egg‐laying order resulted in under‐representation of the morphologies that were selected against and over‐representation of morphologies that were favoured by the local selection on juveniles. The result of these maternal adjustments was fast phenotypic change in sexual size dimorphism within and between populations. Maternal manipulations of offspring morphologies may be especially important at the initial stages of population establishment in the novel environments and may have facilitated recent colonization of much of North America by the house finch.     

Does within-population variation in fish egg size reflect maternal influences on optimal values?

Various models that assume correlations between maternal phenotype and offspring environment predict adaptive variation in egg size within populations. Here we conduct a comparative test of these models using published data on fish egg size. Intrapopulation variation in egg size was most pronounced in fish with demersal eggs and larvae (median coefficient of variation [CV] at family level = 6.5%), where offspring environment is likely influenced by maternal phenotype, and least so in fish with pelagic eggs (CV = 3.6%), which experience a relatively stochastic spatial distribution during incubation. This difference was significant at various taxonomic levels, was robust to variation in mean egg size and habitat (i.e., freshwater or marine), and was mirrored in independent paired contrasts. Fish with demersal eggs and pelagic larvae were not significantly different from those with pelagic eggs (CV = 3.8%), indicating that selection favoring within-population variation in egg size occurs mainly posthatching and that any such selection occurring prehatching may be less intense. These results suggest that patterns of within-population variation in egg size among fish taxa reflect adaptive processes and that maternal effects on the egg size-fitness function may explain apparent discrepancies from the single-optima Smith-Fretwell model.     

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.     

Bigger mothers are better mothers: disentangling size-related prenatal and postnatal maternal effects

Despite a vast literature on the factors controlling adult size, few studies have investigated how maternal size affects offspring size independent of direct genetic effects, thereby separating prenatal from postnatal influences. I used a novel experimental design that combined a cross-fostering approach with phenotypic manipulation of maternal body size that allowed me to disentangle prenatal and postnatal maternal effects. Using the burying beetle Nicrophorus vespilloides as model organism, I found that a mother''s body size affected egg size as well as the quality of postnatal maternal care, with larger mothers producing larger eggs and raising larger offspring than smaller females. However, with respect to the relative importance of prenatal and postnatal maternal effects on offspring growth, only the postnatal effects were important in determining offspring body size. Thus, prenatal effects can be offset by the quality of postnatal maternal care. This finding has implications for the coevolution of prenatal and postnatal maternal effects as they arise as a consequence of maternal body size. In general, my study provides evidence that there can be transgenerational phenotypic plasticity, with maternal size determining offspring size leading to a resemblance between mothers and their offspring above and beyond any direct genetic effects.     

Egg size-dependent expression of growth hormone receptor accompanies compensatory growth in fish

Large egg size usually boosts offspring survival, but mothers have to trade off egg size against egg number. Therefore, females often produce smaller eggs when environmental conditions for offspring are favourable, which is subsequently compensated for by accelerated juvenile growth. How this rapid growth is modulated on a molecular level is still unclear. As the somatotropic axis is a key regulator of early growth in vertebrates, we investigated the effect of egg size on three key genes belonging to this axis, at different ontogenetic stages in a mouthbrooding cichlid (Simochromis pleurospilus). The expression levels of one of them, the growth hormone receptor (GHR), were significantly higher in large than in small eggs, but remarkably, this pattern was reversed after hatching: young originating from small eggs had significantly higher GHR expression levels as yolk sac larvae and as juveniles. GHR expression in yolk sac larvae was positively correlated with juvenile growth rate and correspondingly fish originating from small eggs grew faster. This enabled them to catch up fully in size within eight weeks with conspecifics from larger eggs. This is the first evidence for a potential link between egg size, an important maternal effect, and offspring gene expression, which mediates an adaptive adjustment in a relevant hormonal axis.     

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.     

Quantitative genetic and translocation experiments reveal genotype‐by‐environment effects on juvenile life‐history traits in two populations of Chinook salmon (Oncorhynchus tshawytscha)

Understanding the genetic architecture of phenotypic plasticity is required to assess how populations might respond to heterogeneous or changing environments. Although several studies have examined population‐level patterns in environmental heterogeneity and plasticity, few studies have examined individual‐level variation in plasticity. Here, we use the North Carolina II breeding design and translocation experiments between two populations of Chinook salmon to detail the genetic architecture and plasticity of offspring survival and growth. We followed the survival of 50 800 offspring through the larval stage and used parentage analysis to examine survival and growth through freshwater rearing. In one population, we found that additive genetic, nonadditive genetic and maternal effects explained 25%, 34% and 55% of the variance in larvae survival, respectively. In the second population, these effects explained 0%, 24% and 61% of the variance in larvae survival. In contrast, fry survival was regulated primarily by additive genetic effects, which indicates a shift from maternal to genetic effects as development proceeds. Fry growth also showed strong additive genetic effects. Translocations between populations revealed that offspring survival and growth varied between environments, the degree of which differed among families. These results indicate genetic differences among individuals in their degree of plasticity and consequently their ability to respond to environmental variation.     

Host selection by the pine processionary moth enhances larval performance: An experiment

The development of a phytophagous insect depends on the nutritional characteristics of plants on which it feeds. Offspring from different females, however, may vary in their ability to develop in different host species and therefore females should place their eggs on host plants that result in the highest performance for the insect offspring. Causes underlying the predicted relationships between host selection and offspring performance may be: (1) a genetic association between larval ability to exploit particular hosts and the female insect's host preference; and (2) phenotypic plasticity of larvae that may be due to (a) maternal effects (e.g. differential investment in eggs) or (b) diet. In this work, we analyse the performance (i.e. hatching success and larval size and mortality) of the pine processionary (Thaumetopoea pityocampa) caterpillar developing in Aleppo (Pinus halepensis) or maritime (Pinus pinaster) pines. Larvae of this moth species do not move from the individual pine selected by the mother for oviposition. By means of cross-fostering experiments of eggs batches and silk nests of larvae between these two pine species, we explored whether phenotypic plasticity of offspring traits or genetic correlations between mother and offspring traits account for variation in developmental characteristics of caterpillars. Our results showed that females preferentially selected Aleppo pine for oviposition. Moreover, the offspring had the highest probability of survival and reached a larger body size in this pine species independently of whether or not batches were experimentally cross-fostered. Notably, the interaction between identity of donor and receiver pine species of larvae nests explained a significant proportion of variance of larval size and mortality, suggesting a role of diet-induced phenotypic plasticity of the hatchlings. These results suggest that both female selection of the more appropriate pine species and phenotypic plasticity of larva explain the performance of pine processionary caterpillars.     

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.     

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.     

Cross‐generational costs of compensatory growth in nine‐spined sticklebacks

Compensatory growth (CG) is a form of phenotypic plasticity allowing individuals’ growth trajectories to rebound after a period of resource limitation, but little is known about the reproductive and cross‐generational costs of CG. We studied the potential costs of CG by exposing female nine‐spined sticklebacks Pungitius pungitius to 1) high (favourable), 2) low (stressful), and 3) recovery (initially stressful, subsequently favourable) feeding treatments, and quantified the effects of these treatments on female reproductive traits (clutch, egg and yolk size), and on the size of their offspring. The low feeding treatment reduced female size relative to the high and recovery feeding treatments, which produced equally large females. Hence, females from the recovery treatment demonstrated CG and full growth compensation. Feeding treatments had significant effects on clutch, yolk, egg and larval size, also when the effect of female size was controlled for. However, these effects came about mostly because females from the low feeding treatment produced small clutches with large eggs (containing little yolk) and larvae, whereas females from the recovery feeding treatment produced as large clutches, eggs (with similar amounts of yolk) and larvae as females from the high feeding treatment. Yet, structural equation modelling revealed that while a direct effect of female size on offspring size was positive in the low and high feeding treatments, it was negative in the recovery feeding treatment, independently of egg and clutch size. This indicates a cross‐generational tradeoff between female and offspring sizes in the recovery feeding treatment. Also the tradeoff between clutch and larval size was more pronounced in recovery than in low or high feeding treatments. Hence, apart from demonstrating that environmental influences experienced by females during their development have the potential to influence their size, fecundity and reproductive traits, the results also provide evidence for complex cross‐generational costs of recovery growth.     

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.     

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.     

Population differences in host use by a seed-beetle: local adaptation, phenotypic plasticity and maternal effects

For insects that develop inside discrete hosts, both host size and host quality constrain offspring growth, influencing the evolution of body size and life history traits. Using a two-generation common garden experiment, we quantified the contribution of maternal and rearing hosts to differences in growth and life history traits between populations of the seed-feeding beetle Stator limbatus that use a large-seeded host, Acacia greggii, and a small-seeded host, Pseudosamanea guachapele. Populations differed genetically for all traits when beetles were raised in a common garden. Contrary to expectations from the local adaptation hypothesis, beetles from all populations were larger, developed faster and had higher survivorship when reared on seeds of A. greggii (the larger host), irrespective of their native host. We observed two host plant-mediated maternal effects: offspring matured sooner, regardless of their rearing host, when their mothers were reared on P. guachapele (this was not caused by an effect of rearing host on egg size), and females laid larger eggs on P. guachapele. This is the first study to document plasticity by S. limbatus in response to P. guachapele, suggesting that plasticity is an ancestral trait in S. limbatus that likely plays an important role in diet expansion. Although differences between populations in growth and life history traits are likely adaptations to their host plants, host-associated maternal effects, partly mediated by maternal egg size plasticity, influence growth and life history traits and likely play an important role in the evolution of the breadth of S. limbatus’ diet. More generally, phenotypic plasticity mediates the fitness consequences of using novel hosts, likely facilitating colonization of new hosts, but also buffering herbivores from selection post-colonization. Plasticity in response to novel versus normal hosts varied among our study populations such that disentangling the historical role of plasticity in mediating diet evolution requires the consideration of evolutionary history.