Factors promoting maternal trophic egg provisioning in non-eusocial animals

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

Egg size and the evolution of phenotypic plasticity in larvae of the echinoid genus Strongylocentrotus

Planktotrophic larvae grow by utilizing energy obtained from food gathered in the plankton. Morphological plasticity of feeding structures has been demonstrated in multiple phyla, in which food-limited larvae increase feeding structure size to increase feeding rates. However, before larvae can feed exogenously they depend largely on material contained within the egg to build larval structures and to fuel larval metabolism. Thus, the capacity for plasticity of feeding structures early in development may depend on egg size. Using the congeneric sea urchins Strongylocentrotus franciscanus and S. purpuratus, which differ in egg volume by 5-fold, I tested whether the degree of expression of feeding structure (larval arm length) plasticity is correlated with differences in the size of the egg. I experimentally manipulated egg size of S. franciscanus (the larger-egged species) by separating blastomeres at the 2-cell stage to produce half-sized larvae. I reared half-size and normal-size larvae under high and low food treatments for 20 days. I measured arm and body lengths at multiple ages during development and calculated the degree of plasticity expressed by larvae from all treatments. Control and unmanipulated S. franciscanus larvae (from ∼ 1.0 nl eggs) had significantly longer arms relative to body size and a significantly greater degree of plasticity than half-sized S. franciscanus larvae (from < 0.18 nl eggs), which in turn expressed a significantly greater degree of plasticity than S. purpuratus larvae (from ∼ 0.3 nl eggs). These results indicate that egg size affects larval arm length plasticity in the genus Strongylocentrotus; larger eggs produce more-plastic larvae both in an experimental and a comparative context. However, changes in egg size alone are not sufficient to account for evolved differences in the pattern of plasticity expressed by each species over time and may not be sufficient for the evolutionary transition from feeding to non-feeding.     

The evolutionary genetics of egg size plasticity in a butterfly

Abstract The evolution of phenotypic plasticity requires that it is adaptive, genetically determined, and exhibits sufficient genetic variation. For the tropical butterfly Bicyclus anynana there is evidence that temperature-mediated plasticity in egg size is an adaptation to predictable seasonal change. Here we set out to investigate heritability in egg size and genetic variation in the plastic response to temperature in this species, using a half-sib breeding design. Egg size of individual females was first measured at a high temperature 4 days after eclosion. Females were then transferred to a low temperature and egg size was measured after acclimation periods of 6 and 12 days respectively. Overall, additive genetic variance explained only 3-11% of the total phenotypic variance, whereas maternal effects were more pronounced. Genotype-environment interactions and cross-environmental correlations of less than unity suggest that there is potential for short-term evolutionary change. Our findings strengthen the support for the adaptive nature of temperature-mediated plasticity in egg size.     

Ovarian dynamics, egg size, and egg number in relation to temperature and mating status in a butterfly

Although the temperature‐size rule, that is, an increase in egg (and body) size at lower temperatures, applies almost universally to ectotherms, the developmental mechanisms underlying this consistent pattern of phenotypic plasticity are hitherto unknown. By investigating ovarian dynamics and reproductive output in the tropical butterfly Bicyclus anynana (Butler) (Lepidoptera: Nymphalidae: Satyrinae) in relation to oviposition temperature and mating status, we tested the relevance of several competing hypotheses for temperature‐mediated variation in egg size and number. As expected, females ovipositing at a lower temperature laid fewer but larger eggs than those ovipositing at a higher temperature. Despite pronounced differences in egg‐laying rates, oocyte numbers were equal across temperatures at any given time, while oocyte size increased at the lower temperature. In contrast, there were greatly reduced oocyte numbers in mated compared to virgin females. Our results indicated that temperature‐mediated plasticity in egg size cannot be explained by reduced costs of somatic maintenance at lower temperatures, enabling the allocation of more resources to reproduction (reproductive investment was higher at the higher temperature). Furthermore, there was no indication for delayed oviposition (no accumulation of oocytes at the lower temperature, in contrast to virgin females). Rather, low temperatures greatly reduced the oocyte production (i.e., differentiation) rate and prolonged egg‐maturation time, causing low egg‐laying rates. Our data thus suggested that oocyte growth is less sensitive to temperature than oocyte production, resulting in a lower number of larger eggs at lower temperatures.     

Syntaxin 1A modulates the sexual maturity rate and progeny egg size related to phase changes in locusts

The migratory locust (Locusta migratoria) exhibits clear phenotypic plasticity depending on its population density. Previous studies have explored the molecular mechanisms of body colour, behavior, immunity, and metabolism between high population density gregarious (G) and low population density solitarious (S) locusts. However, the molecular mechanisms underlying differences in reproductive traits remain unknown. G locusts reach sexual maturation much faster and lay larger eggs compared with S locusts. The traits of G locusts decreased significantly with isolation, whereas those of S locusts increased with crowding. Analysis of gene expression in female adults indicated that syntaxin 1A (Syx1A) was expressed significantly higher in G locusts than in S locusts. After silencing Syx1A expression in G locusts by RNA interference (RNAi), their sexual maturity rate and progeny egg size changed towards those of S locusts. Similarly, increment in the traits of S locusts with crowding was blocked by Syx1A interference. Changes in the traits were also confirmed by decrease in the level of vitellogenin, which is regulated by Syx1A. In conclusion, plasticity of the sexual maturity rate and progeny egg size of G and S locusts, which is beneficial for locusts to adapt to environmental changes, is regulated by Syx1A.     

Genetic and environmental sources of egg size, fecundity and body size in the migrant skipper, Parnara guttata guttata (Lepidoptera: Hesperiidae)

Genetic and environmental sources of egg size, fecundity and body size (forewing length) were examined in the butterfly, Parnara guttata guttata. Phenotypic and genetic correlation and heritability were estimated for these traits under different day-length and temperature conditions. Egg size and fecundity had relatively high heritabilities, and body sizes in males and females had moderate and high heritability, respectively. Negative phenotypic and genetic correlations between egg size and fecundity were estimated in treatments corresponding to the natural conditions during larval development of the first and second generations. Phenotypic and genetic correlations between body size and egg size differed considerably between insects reared under long and short day-lengths. Next, genotype–environment interactions were estimated by comparing reaction norms to day-length or temperature of these traits among families. ANOVA analysis revealed significant genotype–environment interactions in egg size and forewing length in both sexes for day-length and temperature. These results suggested that a large additive genetic variance for egg size might have been maintained by a genetic trade-off and/or by genotype–environment interactions in P. g. guttata.     

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.     

Effects of temperature on reproductive output, egg provisioning, juvenile hormone and vitellogenin titres in the butterfly Bicyclus anynana

Environmentally induced phenotypic plasticity is common in nature. Hormones, affecting multiple traits and signaling to a variety of distant target tissues, provide a mechanistic link between environments, genes and trait expression, and may therefore well be involved in the regulation phenotypic plasticity. Here, we investigate whether in the tropical butterfly Bicyclus anynana temperature-mediated plasticity in egg size and number, with fewer but larger eggs produced at lower temperatures and vice versa, is under control of juvenile hormone, and whether different temperatures cause differences in egg composition. Female B. anynana butterflies showed the expected response to temperature, however, we found no evidence for an involvement of juvenile hormone. Neither haemolymph JH II and JH III titres nor vitellogenin levels differed across temperatures. The smaller eggs produced at the higher temperature contained relatively higher amounts of water, free carbohydrates and proteins, but relatively lower amounts of lipids. While these smaller eggs had a lower absolute energy content, total reproductive investment was higher at the higher temperature (due to a higher fecundity). Overall, our study indicates that temperature-mediated plasticity in reproduction in B. anynana is mechanistically related to a biophysical model, with oocyte production (differentiation) and oocyte growth (vitellogenesis) having differential temperature sensitivities.     

Temperature effects on egg size and their fitness consequences in the yellow dung fly Scathophaga stercoraria

Organisms and parts of an organism like eggs or individual cells developing in colder environments tend to grow bigger. A unifying explanation for this Bergmann's rule extended to ectotherms has not been found, and whether this is an adaptive response or a physiological constraint is debated. The dependence of egg and clutch size on the mother's temperature environment were investigated in the yellow dung fly Scathophaga stercoraria. Smaller eggs were laid at warmer temperatures in the field and the laboratory, where possible confounding variables were controlled for. As clutch size at the same time was unaffected by temperature, this effect was not due to a trade-off between egg size and number. Temperature-dependent egg sizes even persisted within individuals: when females were transferred to a cooler (warmer) environment, they laid third-clutch eggs that were larger (smaller) than their first-clutch eggs. The fitness consequences of these temperature-mediated egg sizes were further investigated in two laboratory experiments. Neither egg and pre-adult survivorship nor larval growth rate were maximized, nor was development time minimized, at the ambient temperature corresponding to the mother's temperature environment. This does not support the beneficial acclimation hypothesis. Instead, this study yielded some, but by no means conclusive indications of best performance by offspring from eggs laid at intermediate temperatures, weakly supporting the optimal temperature hypothesis. In one experiment the smaller eggs laid at 24 °C had reduced survivorship at all ambient temperatures tested. Smaller eggs thus generally performed poorly. The most parsimonious interpretation of these results is that temperature-mediated variation in egg size is a maternal physiological response (perhaps even a constraint) of unclear adaptive value. This revised version was published online in November 2006 with corrections to the Cover Date.     

Within- and between-generation effects of temperature on life-history traits in a butterfly

Non-genetic parental effects may largely affect offspring phenotype, and such plasticity is potentially adaptive. Despite its potential importance, little is known about cross-generational effects of temperature, at least partly because parental effects were frequently considered a troublesome nuisance, rather than a target of experimental studies. We here investigate effects of parental, developmental and acclimation temperature on life-history traits in the butterfly Bicyclus anynana. Higher developmental temperatures reduced development times and egg size, increased egg number, but did not affect pupal mass. Between-generation temperature effects on larval time, pupal time, larval growth rate and egg size were qualitatively very similar to effects of developmental temperature, and additionally affected pupal mass but not egg number. Parental effects are important mediators of phenotypic plasticity in B. anynana, and partly yielded antagonistic effects on different components of fitness, which may constrain the evolution of cross-generational adaptive plasticity.     

Energetics of embryonic development: effects of temperature on egg and hatchling composition in a butterfly

Phenotypic plasticity may allow an organism to adjust its phenotype to environmental needs. However, little is known about environmental effects on offspring biochemical composition and turnover rates, including energy budgets and developmental costs. Using the tropical butterfly Bicyclus anynana and employing a full-factorial design with two oviposition and two developmental temperatures, we explore the consequences of temperature variation on egg and hatchling composition, and the associated use and turnover of energy and egg compounds. At the lower temperature, larger but fewer eggs were produced. Larger egg sizes were achieved by provisioning these eggs with larger quantities of all compounds investigated (and thus more energy), whilst relative egg composition was rather similar to that of smaller eggs laid at the higher temperature. Turnover rates during embryonic development differed across developmental temperatures, suggesting an emphasis on hatchling quality (i.e. protein content) at the more stressful lower temperature, but on storage reserves (i.e. lipids) at the higher temperature. These differences may represent adaptive maternal effects. Embryonic development was much more efficient at the lower temperature, providing a possible mechanism underlying the temperature-size rule.     

Effects of egg size reduction and larval feeding on juvenile quality for a species with facultative-feeding development

In free-spawning marine invertebrates, larval development typically proceeds by one of two modes: planktotrophy (obligate larval feeding) from small eggs or lecithotrophy (obligate non-feeding) from relatively large eggs. In a rare third developmental mode, facultative planktotrophy, larvae can feed, but do not require particulate food to complete metamorphosis. Facultative planktotrophy is thought to be an intermediate condition that results from an evolutionary increase in energy content in the small eggs of a planktotrophic ancestor. We tested whether an experimental reduction in egg size is sufficient to restore obligate planktotrophy from facultative planktotrophy and whether the two sources of larval nutrition (feeding and energy in the egg) differentially influence larval survival and juvenile quality. We predicted, based on its large egg size, that a reduction in egg size in the echinoid echinoderm Clypeaster rosaceus would affect juvenile size but not time to metamorphosis. We reduced the effective size of whole (W) zygotes by separating blastomeres at the two- or four-cell stages to create half- (H) or quarter-size (Q) “zygotes” and reared larvae to metamorphosis, both with and without particulate food. Larvae metamorphosed at approximately the same time regardless of food or egg size treatment. In contrast, juveniles that developed from W zygotes were significantly larger, had higher organic content and had longer and more numerous spines than juveniles from H or Q zygotes. Larvae from W, H and Q zygotes were able to reach metamorphosis without feeding, suggesting that the evolution of facultative planktotrophy in C. rosaceus was accompanied by more than a simple increase in egg size. In addition, our results suggest that resources lost by halving egg size have a larger effect on larval survival and juvenile quality than those lost by withholding particulate food.     

Temperature effects during development on a polyembryonic parasitoid and its host

Ambient temperature can influence development through effects on metabolic rate and by inducing physiological stress. In this study, we assessed temperature effects on a host–parasitoid interaction and on the body size and brood size of emerging wasps. By examining the development at two different temperatures of the koinobiont parasitoid, Copidosoma bakeri, and its host, Agrotis ipsilon, we asked: (1) Does the growth response to temperature by A. ipsilon depend on whether the moth caterpillar is parasitized? (2) Does the allocation pattern of body size and brood size in C. bakeri change with temperature? To answer these questions, we exposed A. ipsilon larvae parasitized by C. bakeri to high or low non-lethal temperatures when A. ipsilon was in early or late larval stages and measured their development time and body mass for all four treatment combinations. We also examined the brood size and body mass of emerging wasps. Whether parasitized or not, A. ipsilon larvae decreased development time, but generally did not decrease final body mass, at the higher temperature. When parasitized A. ipsilon was exposed to the higher temperature only late in their development, enlargement of the host by the parasitoid was reduced. C. bakeri brood size significantly increased when the higher temperature was applied early in host development. We did not detect a shift with temperature in the allocation pattern of the size–number trade-off for wasp offspring, suggesting that this trade-off relationship may be under selection strong enough to yield insensitivity to temperature.     

Fitness consequences of variation in developmental temperature in a butterfly

We explored the adaptive significance of developmental plasticity in the tropical butterfly Bicyclus anynana using two experiments including temperature changes during ontogeny. In contrast to previous findings on adult acclimation, we could not find any evidence in support of adaptive developmental plasticity, as survival until adulthood was not enhanced when larval rearing temperatures matched the temperatures experienced during prepupal or pupal development. Extreme temperatures substantially reduced survival, supporting the ‘optimal developmental temperature’ hypothesis. Metamorphosis was more efficient at the higher rearing temperature of 27 °C, where egg hatching success was also higher, indicating that the lower temperature of 20 °C is already slightly stressful for this tropical butterfly.     

Sex differences in phenotypic plasticity of a mechanism that controls body size: implications for sexual size dimorphism

The degree and/or direction of sexual size dimorphism (SSD) varies considerably among species and among populations within species. Although this variation is in part genetically based, much of it is probably due to the sexes exhibiting differences in body size plasticity. Here, we use the hawkmoth, Manduca sexta, to test the hypothesis that moths reared on different diet qualities and at different temperatures will exhibit sex-specific body size plasticity. In addition, we explore the proximate mechanisms that potentially create sex-specific plasticity by examining three physiological variables known to regulate body size in this insect: the growth rate, the critical weight (which measures the cessation of juvenile hormone secretion from the corpora allata) and the interval to cessation of growth (ICG; which measures the time interval between the critical weight and the secretion of the ecdysteroids that regulate pupation and metamorphosis). We found that peak larval mass of males and females did not exhibit sex-specific plasticity in response to diet or temperature. However, the sexes did exhibit sex-specific plasticity in the mechanism that controls size; males and females exhibited sex-specific plasticity in the growth rate and the critical weight in response to both diet and temperature, whereas the ICG only exhibited sex-specific plasticity in response to diet. Our results suggest it is important for the sexes to maintain the same degree of SSD across environments and that this is accomplished by the sexes exhibiting differential sensitivity of the physiological factors that determine body size to environmental variation.     

Environmental,parental and adaptive variation in egg size of Tengmalm's owls under fluctuating food conditions

We studied egg size variation of Tengmalm's owls in western Finland during 1981–1990. The owls fed on voles whose population fluctuated in a predictable manner: low (1981, 1984, 1987, 1990), increase (1982, 1985, 1988) and peak (1983, 1986, 1986) phases of the cycle occurred every third year. Eggs were largest in the increase phase of the vole cycle, even though that voles were more abundant and egg-laying started earlier in the peak phase than in the increase phase. This suggests that owls invest mostly in egg size when vole abundance increases along with survival chances of offspring. Territory quality and female age had no effects on egg size, but egg size decreased with laying data in the increase phase of the vole cycle. Egg size was significantly positively related to the male age in the increase phase, but the opposite relationship was significant in the peak phase of the vole cycle. The partners of adult males also decreased their egg volume from the increase to the peak phase, whereas the partners of yearling males produced their largest eggs in the peak phase of the vole cycle. This suggests the importance of experience in prevailing food fluctuations. Possibly male Tengmalm's owls can adjust the intensity of courtship feeding not only in relation to the food abundance on their territories at the time of egg laying, but also to the survival prospects of their offspring. Phenotypic plasticity seems to play a substantial role, as the egg size repeatabilities of individual females and partners of individual males were low. Obviously, under cyclic food conditions, predictability and inter-generational trade-offs are important to life history traits.     

Maternal effects on phenotypic plasticity in larvae of the salamander <Emphasis Type="Italic">Hynobius retardatus</Emphasis>

Maternal effects are widespread and influence a variety of traits, for example, life history strategies, mate choice, and capacity to avoid predation. Therefore, maternal effects may also influence phenotypic plasticity of offspring, but few studies have addressed the relationship between maternal effects and phenotypic plasticity of offspring. We examined the relationship between a maternally influenced trait (egg size) and the phenotypic plasticity of the induction rate of the broad-headed morph in the salamander Hynobius retardatus. The relationship between egg size and the induction of the broad-headed morph was tested across experimental crowding conditions (densities of low conspecifics, high conspecifics, and high heterospecific anuran), using eggs and larvae from eight natural populations with different larval densities of conspecifics and heterospecifics. The broad-headed morph has a large mouth that enables it to consume either conspecifics or heterospecifics, and this ability gives survival advantages over the normal morph. We have determined that there is phenotypic plasticity in development, as shown by an increase in the frequency of broad-headed morph in response to an increase in the density of conspecifics and heterospecifics. This reaction norm differed between populations. We also determined that the frequency of the broad-headed morph is affected by egg size in which larger egg size resulted in expression of the broad-headed morph. Furthermore, we determined that selection acting on the propensity to develop the broad-headed morph has produced a change in egg size. Lastly, we found that an increase in egg size alters the reaction norm to favor development of the broad-headed morph. For example, an equal change in experimental density produces a greater change in the frequency of the broad-headed morph in larvae developing from large eggs than it does in larvae developing from small eggs. Population differences in plasticity might be the results of differences in egg size between populations, which is caused by the adaptive integration of the plasticity and egg size. Phenotypic plasticity can not evolve independently of maternal effects.     

Phenotypic plasticity in the reproductive traits of a parasitoid

Organisms show phenotypic plasticity - the capacity for a given genotype to express different phenotypes - in response to changes in the environment. Among the several factors that can cause phenotypic plasticity, nutritional constraints during development can affect the size of organisms and, consequently, affect most life-history traits, including reproductive traits. As their larvae are restricted by the amount of food contained in their host, parasitoids are a good model to study phenotypic plasticity related to size. The phenotypic plasticity of reproductive traits was investigated in the egg parasitoid Trichogramma euproctidis (Hymenoptera: Trichogrammatidae) by using host species of different sizes. Adult size, sperm storage organs (seminal vesicles and spermatheca), number of sperm stored and gamete size (sperm and oocyte) are all influenced by the host species; larger individuals have larger organs which contain more sperm, and both sperm and oocytes are correlated with adult size. However, while females become larger than males and mature larger oocytes in larger hosts, increase in sperm length stops after a given threshold.     

Reproductive response of Euterpina acutifrons in two estuaries of the Basque Country (Bay of Biscay) with contrasting nutritional environment

The reproductive response involving egg number and size was studied for the egg carrying copepod Euterpina acutifrons in two estuaries with different nutritional environment (Bilbao and Mundaka). To characterise the available food for copepods, the concentration of particulate organic matter (POM), the combined concentration (PGL) and proportion of particulate protein, carbohydrate and lipids and the concentration of chlorophyll a were measured in the <20 μm seston fraction. Data on female size (prosome length) and abiotic factors, such as temperature, salinity and oxygen saturation in water, were also obtained to relate them to reproductive and nutritional variables. Correlation and stepwise regression analyses indicated that temperature via female size was the main factor controlling brood volume in a temporal context, whilst the nutritional environment had a secondary role. Nevertheless, the nutritional environment caused noticeable between-estuary differences in the reproductive response of this species. ANOVA tests showed that E. acutifrons clutch size and brood volume were significantly bigger in the estuary of Bilbao, which was richer in both total (POM) and labile (PGL) organic particulate matter than the estuary of Mundaka. In contrast, egg size, female size and phytoplanktonic food quantity did not differ significantly between estuaries. These results suggest that the organic enrichment with particles of detritical-heterotrophic origin enhanced E. acutifrons clutch size and brood volume in Bilbao. Egg size was closely related to phytoplankton in both estuaries, but a clear trade-off between egg size and number per clutch was observed only in Mundaka. Thus, we suggest that the reduction of egg number in order to increase egg size might happen only under food-limiting conditions, but not in organically rich and quite constant nutritional environments such as found those in Bilbao.