Maternal effects and their consequences for offspring fitness in the Yellow Dung Fly

1. Maternal adult diet and body size influence the fecundity of a female and possibly the quality and the performance of her offspring via egg size or egg quality. In laboratory experiments, negative effects in the offspring generation have often been obscured by optimal rearing conditions.
2. To estimate these effects in the Yellow Dung Fly, Scathophaga stercoraria , how maternal body size and adult nutritional status affected her fecundity, longevity and egg size were first investigated.
3. Second, it was investigated how female age and adult nutritional experience, mediated through the effects of egg size or egg quality, influenced the performance of offspring at different larval densities.
4. Maternal size was less important than maternal adult feeding in increasing reproductive output. Without food restriction, large females had larger clutch sizes and higher oviposition rates, whereas under food restriction this advantage was reversed in favour of small females.
5. Offspring from mothers reared under nutritional stress experienced reduced fitness in terms of egg mortality and survival to adult emergence. If the offspring from low-quality eggs survived, the transmitted maternal food deficiency only affected adult male body size under stressful larval environments.
6. Smaller egg sizes due to maternal age only slightly affected the performance of the offspring under all larval conditions.     

Effects of food stress and density in different life stages on reproduction in a butterfly

Availability of adequate nutrition and (rearing) density are among the most important factors affecting growth, development and reproduction in animals. In holometabolous insects diets and energetic needs change between life stages, with storing of larval resources, adult feeding and reproduction being linked strategies. Nevertheless, studies investigating nutritional (and density) effects across metamorphic boundaries are largely lacking. We aim at disentangling the functional basis of reproductive patterns by independently manipulating larval and adult (1) density and (2) access to food, respectively, in the tropical butterfly, Bicyclus anynana. (1) A high larval rearing density had, contrary to common wisdom, very little impact on body size, but reduced larval development time through increased growth rates. The latter is thought to be an adaptation to high densities, driven by the risk of larval food resources becoming exhausted before reaching metamorphosis. Larval density and male company during oviposition (i.e. adult density) had no detectable effects on female reproduction. (2) Larval food stress prolonged larval development time and reduced larval growth rate, body size, fecundity and reproductive investment. Detrimental effects on female reproduction were mediated through a reduction in body size. Additional negative effects of adult food stress on fecundity were largely confined to females being fed as larvae ad libitum, while those being previously starved showed reduced performance regardless of adult income. Effects on egg size were inconsistent and, overall, marginal. Our results show that restricted food access in different developmental stages may set different limits to reproduction, either posed by shortage of larval‐derived storage reserves (i.e. nitrogenous compounds) or adult income (i.e. carbohydrates). Thus, one should be cautious when stating that one or the other type of nutrients is ultimately limiting to reproduction. Rather, our findings highlight the importance of resource congruence and of considering both, larval‐ and adult‐derived resources for reproduction.     

Fitness advantage from nuptial gifts in female fireflies

Abstract 1. In many insects, males provide nuptial gifts to females in the form of spermatophores, sperm-containing structures produced by male accessory glands.
2. The work reported here examined the influence of both spermatophore number and spermatophore size on female reproductive output in two related firefly beetles, Photinus ignitus and Ellychnia corrusca (Coleoptera: Lampyridae). Based on differences in adult diet, male spermatophores were predicted to increase female reproductive output to a greater extent in P. ignitus than in E. corrusca .
3. Female fecundity was significantly higher in triply mated females than in singly mated females in both species, with no difference between mating treatments in female lifespan or egg hatching success. No effects of second male spermatophore size on fecundity, lifespan, or egg hatching success were detected in either species.
4. These results suggest a direct fitness advantage from multiple mating for females in both species, although enhanced fecundity may be due either to allocation of spermatophore nutrients to eggs or to other substances transferred within the spermatophore acting as oviposition stimulants.     

Effects of Increased Flight on the Energetics and Life History of the Butterfly Speyeria mormonia

Movement uses resources that may otherwise be allocated to somatic maintenance or reproduction. How does increased energy expenditure affect resource allocation? Using the butterfly Speyeria mormonia, we tested whether experimentally increased flight affects fecundity, lifespan or flight capacity. We measured body mass (storage), resting metabolic rate and lifespan (repair and maintenance), flight metabolic rate (flight capacity), egg number and composition (reproduction), and food intake across the adult lifespan. The flight treatment did not affect body mass or lifespan. Food intake increased sufficiently to offset the increased energy expenditure. Total egg number did not change, but flown females had higher early-life fecundity and higher egg dry mass than control females. Egg dry mass decreased with age in both treatments. Egg protein, triglyceride or glycogen content did not change with flight or age, but some components tracked egg dry mass. Flight elevated resting metabolic rate, indicating increased maintenance costs. Flight metabolism decreased with age, with a steeper slope for flown females. This may reflect accelerated metabolic senescence from detrimental effects of flight. These effects of a drawdown of nutrients via flight contrast with studies restricting adult nutrient input. There, fecundity was reduced, but flight capacity and lifespan were unchanged. The current study showed that when food resources were abundant, wing-monomorphic butterflies living in a continuous meadow landscape resisted flight-induced stress, exhibiting no evidence of a flight-fecundity or flight-longevity trade-off. Instead, flight changed the dynamics of energy use and reproduction as butterflies adopted a faster lifestyle in early life. High investment in early reproduction may have positive fitness effects in the wild, as long as food is available. Our results help to predict the effect of stressful conditions on the life history of insects living in a changing world.     

Selection on body size and sexual size dimorphism differs between host species in a seed-feeding beetle

Sexual size dimorphism varies substantially among populations and species but we have little understanding of the sources of selection generating this variation. We used path analysis to study how oviposition host affects selection on body size in a seed-feeding beetle (Stator limbatus) in which males contribute large ejaculates (nuptial gifts) to females. Females use nutrients in these ejaculates for egg production. Male body size, which affects ejaculate size, affects female fecundity and is thus under fecundity selection similar in magnitude to the fecundity selection on female body size. We show that when eggs are laid on a host on which larval mortality is low (seeds of Acacia greggii) fecundity predicts fitness very well and fecundity selection is the major source of selection on both male and female adult size. In contrast, when eggs are laid on a host on which larval mortality is high (seeds of Parkinsonia florida) fecundity poorly predicts fitness such that fecundity selection is relaxed on both male and female size. However, because egg size affects larval mortality on this poor host (P. florida) there is selection on female size via the female size --> egg size --> fitness path; this selection via egg size offsets the reduction in fecundity selection on female, but not male, body size. Thus, differences in host suitability (due to differences in larval mortality) affect the relative importance of two sources of selection on adult body size; fecundity selection on both male and female body size is lower on the poor quality host (P. florida) relative to the high quality host (A. greggii) whereas selection on female body size via effects of egg size on offspring survival (body size --> egg size --> fitness) is greater on the poor quality host relative to the high quality host. Because selection via the egg size path affects only females the difference in larval survival between hosts shifts the relative magnitude of selection on female vs. male size. Researchers working on other study systems should be alerted to the possible importance of subtle, but consequential, indirect selection on their study organisms.     

Effects of adult-derived carbohydrates, amino acids and micronutrients on female reproduction in a fruit-feeding butterfly

It is generally believed that butterflies (and other holometabolous insects) rely primarily on reserves accumulated during the larval stage for reproduction, whereas the carbohydrate-rich adult diet is thought to mainly cover energy requirements. In at least some species though, realization of the full reproductive potential is extensively affected by post-eclosion nutrition. While the importance of carbohydrates is fairly well understood, the role of adult-derived amino acids and micronutrients is controversial and largely unknown, respectively. We here focus on the effects of different adult diets on female reproduction in the tropical, fruit-feeding butterfly Bicyclus anynana (Nymphalidae). Carbohydrates were the most important adult-derived nutrients affecting reproduction. Adding amino acids, vitamins or minerals to sucrose-based solutions did not yield a reproductive output equivalent to that of fruit-fed females, which showed the highest performance throughout. This suggests that either not yet identified compounds of fruit substantially contribute to reproduction, or that resource congruence (the use of nutrient types in a specified ratio) rather than any specific nutrient component is of key importance. Apart from adult income, realized fecundity depended on egg size and longevity, with the former dominating when dietary quality was low, but the latter when quality was high. Thus, the egg size-number trade-off seems to be affected by female nutrition.     

Host strain specific sex pheromone variation in Spodoptera frugiperda

Background

In the Lepidoptera it was historically believed that adult butterflies rely primarily on larval-derived nutrients for reproduction and somatic maintenance. However, recent studies highlight the complex interactions between storage reserves and adult income, and that the latter may contribute significantly to reproduction. Effects of adult diet were commonly assessed by determining the number and/or size of the eggs produced, whilst its consequences for egg composition and offspring viability were largely neglected (as is generally true for insects). We here specifically focus on these latter issues by using the fruit-feeding tropical butterfly Bicyclus anynana, which is highly dependent on adult-derived carbohydrates for reproduction.

Results

Adult diet of female B. anynana had pronounced effects on fecundity, egg composition and egg hatching success, with butterflies feeding on the complex nutrition of banana fruit performing best. Adding vitamins and minerals to a sucrose-based diet increased fecundity, but not offspring viability. All other groups (plain sucrose solution, sucrose solution enriched with lipids or yeast) had a substantially lower fecundity and egg hatching success compared to the banana group. Differences were particularly pronounced later in life, presumably indicating the depletion of essential nutrients in sucrose-fed females. Effects of adult diet on egg composition were not straightforward, indicating complex interactions among specific compounds. There was some evidence that total egg energy and water content were related to hatching success, while egg protein, lipid, glycogen and free carbohydrate content did not seem to limit successful development.

Conclusion

The patterns shown here exemplify the complexity of reproductive resource allocation in B. anynana, and the need to consider egg composition and offspring viability when trying to estimate the effects of adult nutrition on fitness in this butterfly and other insects.     

The effect of male mating history on paternal investment, fecundity and female remating in the seed beetle Callosobruchus maculatus

1. In many organisms, males provide nutrients to females via ejaculates that can influence female fecundity, longevity and mating behaviour. The effect of male mating history on male ejaculate size, female fecundity, female longevity and female remating behaviour in the seed beetle Callosobruchus maculatus was determined.
2. The quantity of ejaculate passed to females declined dramatically with successive matings. Despite the decline, a male's ability to fertilize a female fully did not appear to decline substantially until his fourth mating.
3. When females multiply mated with males of a particular mated status, the pattern of egg production was cyclic, with egg production increasing after mating. Females multiply mated to virgins had higher fecundity than females mated to non-virgins, and females mated to twice-mated males had disproportionately increased egg production late in their life.
4. Females that mated to multiple virgins, and consequently laid more eggs, experienced greater mortality than females mated only once or mated to non-virgins, suggesting that egg production is costly, and rather than ameliorating these costs, male ejaculates may increase them by allowing or stimulating females to lay more eggs.
5. Females mating with non-virgin males remated more readily than did females mated to virgins. Females given food supplements were less likely to remate than females that were nutritionally stressed, suggesting that females remate in part to obtain additional nutrients.     

Lifetime allocation of juvenile and adult nutritional resources to egg production in a holometabolous insect.

In holometabolous insects reproductive success is strongly determined by the nutritional resources available to the females. In addition to nutrients derived from adult feeding, resources for egg production may come from the limited reserves accumulated during the larval stages. The pattern of allocation of these larval reserves to egg production is expected to be strongly linked to the nutritional ecology of the adult. We investigate the temporal pattern of allocation of larval reserves to reproduction in a host-feeding parasitoid wasp. As predicted by the dynamics of allocation of an adult meal, larval reserves are the main source of nutrients for four or five days after emergence. However, despite the high frequency of host feeding and the high nutrient content of a haemolymph meal, which we predicted would lead to larval reserves being conserved in the event of host deprivation, larval reserves contribute to egg production throughout the lifetime of the female. We propose several mechanistic and adaptive explanations for our results, including the possible existence of a limiting or key nutrient for egg production of exclusively larval origin. We make further predictions concerning the pattern of allocation of larval resources in parasitoids with different adult nutritional requirements.     

Adult dietary protein has age‐ and context‐dependent effects on male post‐copulatory performance

The highly conserved effect of dietary protein restriction on lifespan and ageing is observed in both sexes and across a vast range of taxa. This extension of lifespan is frequently accompanied by a reduction in female fecundity, and it has been hypothesized that individuals may reallocate resources away from reproduction and into somatic maintenance. However, effects of dietary protein restriction on male reproduction are less consistent, suggesting that these effects may depend on other environmental parameters. Using the neriid fly, Telostylinus angusticollis, we examined age‐specific effects of adult dietary protein restriction on male post‐copulatory reproductive performance (fecundity and offspring viability). To explore the context dependence of these effects, we simultaneously manipulated male larval diet and adult mating history. We found that protein‐restricted males sired less viable offspring at young ages, but offspring viability increased with paternal age and eventually exceeded that of fully fed males. The number of eggs laid by females was not affected by male dietary protein, whereas egg hatching success was subject to a complex interaction of male adult diet, age, larval diet and mating history. These findings suggest that effects of protein restriction on male reproduction are highly context dependent and cannot be explained by a simple reallocation of resources from reproduction to somatic maintenance. Rather, these effects appear to involve changes in the scheduling of male reproductive investment with age.     

Larval population density affects female weight and fecundity in the dung beetle Aphodius ater

1. Competition for food at high densities during larval development leads to reduced adult weight in the northern temperate dung beetle Aphodius ater. 2. Analysis of female beetles caught in the field showed that numbers of eggs and total egg load per female were correlated positively with beetle size. 3. Female beetles reared at different population densities during larval development in the laboratory were analysed with regard to their lifetime fecundity and reproductive lifespan. 4. High population densities during development had a negative influence on the number of eggs per female and on reproductive lifespan. Lifetime fecundity was correlated positively with female weight. 5. It was concluded that competition during larval development in the first generation of offspring will result in a lower number of offspring in the second generation in Aphodius ater, and thereby reduce parental fitness.     

Does reproductive investment change with age in tsetse flies, Glossina morsitans morsitans (Diptera: Glossinidae)?

1. Viviparous insects such as tsetse ( Glossina spp.) provide unusual opportunities to compare age-related changes in the proportion of maternal resources transferred to offspring.
2. In laboratory populations of Glossina morsitans morsitans the survival of females was high for the first 60 days of adult life but declined rapidly thereafter.
3. Average longevity did not differ significantly between mated and unmated females (93·6 and 90 days, respectively).
4. Nutritional state in terms of fat content and residual dry mass did not decline with adult female age.
5. The fecundity of mated females was constant for the first 60 days of adult life and declined only slightly thereafter.
6. Offspring size did not change towards the end of the adult female lifespan and there was no evidence of an increase in the allocation of resources to reproduction in older females.
7. Results contrast with those obtained recently for vertebrates and may indicate that age-related changes in offspring size in Glossina are not adaptive, or that so few females reach old age under natural conditions that there is no selection for a strategy of terminal investment.     

Female size and fitness in the leaf-cutter bee Megachile apicalis

1. The effects of female size on fitness of the leaf-cutter bee Megachile apicalis Spinola (Hymenoptera: Megachilidae) were examined using artificial nesting sites in the field.
2. Although female size had no significant effect on female longevity or sex ratio of progeny, it did have a significant effect on fecundity; larger females attained greater realized fecundity than did smaller females.
3. This significant effect of female size on fecundity occurred because larger females produced cells faster than did smaller females.
4. Female size also had a significant effect on egg size; larger females laid larger eggs than did smaller females.
5. Female size had a significant effect on the size of investment in each progeny. The size of investment estimated by brood cell weight was greater for larger females than for smaller females. This pattern was largely absent, however, when the size of investment was estimated by adult progeny weight.
6. Female size had a significant effect on nest usurpation behaviour; larger females had a higher capacity to usurp nests than did smaller females.     

Mating frequency influences nectar amino acid preference of Pieris napi

It is generally assumed that butterflies, as is the case with many holometabolous insects, rely primarily on nutrients gathered by larval feeding for somatic maintenance and fecundity. These reserves can be supplemented by adult feeding and in some cases by nuptial gifts passed from the males to the females during mating. Recent findings indicate that female butterflies detect and prefer nectar with high levels of amino acids, thus calling new attention to this nutritive source. Polyandrous species can further supplement their larval stores with additional nuptial gifts. This study examined how mating frequency of the polyandrous butterfly Pieris napi affects the female's preference for nectar amino acids. Females of this species generally detect and prefer nectar mimics containing amino acids. However, nectar amino acid preference is significantly lower in mated females. Furthermore, nectar amino acid preference increases when females are not allowed to remate, whereas the preference of twice-mated females remains constant at a lower level. These results indicate a versatile response of females to nectar amino acids, depending on their nutritional status; they may even switch their source of amino acids between adult feeding and nuptial gifts.     

Size Effects on Mating and Egg Production in the Miami Blue Butterfly

Body size is often related to reproductive success in insects, but the direction and strength of this relationship differs greatly among systems. We studied the effects of adult size on probability of mating and egg production in the Miami blue butterfly. We found that likelihood of mating was invariant with respect to size. Larger females lived longer, and both size and lifespan positively influenced egg production. However, neither the number of copulations nor the size of male mates had any effect on female fecundity. We discuss these results in the context of butterfly mating systems, larval growth strategies and the possible effects of captive conditions on reproductive behavior.     

Dietary glycerol and adult access to water: effects on fecundity and longevity in the almond moth

The quality of food eaten by larval insects will affect traits such as gamete production, fat reserves, muscle bulk and body size in the adult. Moreover, larvae also depend on high moisture content in the diet for survival. The almond moth (Ephestia cautella) (W.) (Lepidoptera; Pyralidae) does not feed as an adult although it continues to drink water. We tested the idea that an almond moth could compensate for a low-water diet as a larva by increasing its water intake as an adult. We reared larvae on two different food sources with different moisture regimes; standard laboratory diet with glycerol (relatively wet) and standard diet without glycerol (relatively dry). Half the adult moths from each treatment were given water to drink before their first and only mating. Our results show that wet larval diets (i.e. containing glycerol) significantly decreased fecundity (total number of eggs laid and the proportion of hatched larvae), whilst it significantly increased male and female longevity. The interaction effect of water access for adult males and females was significant, independent of the glycerol in the larval diet. Longevity in females that were not presented with water as adults was slightly higher if mated with a male that had had access to water, suggesting a mating donation of water. However, females that received water as adults showed a decreased longevity if mated with a male who had also had access to water as an adult, indicating a negative effect of water if received by both males and females. In addition, when the larval diet included glycerol, increased number of eggs laid decreased female longevity, whilst an absence of glycerol in the larval diet resulted in low female longevity that was unlinked with fecundity. Glycerol is used in many artificial insect diets and the fact that it shows a strong effect on key life-history traits (reproductive output and longevity in this species), merits careful re-examination of its effects on these important traits in other laboratory models. We also discuss the possibility that larval diet can affect female reproductive decisions.     

Egg maturation and oviposition strategy of a capital breeder,Cleorodes lichenaria,feeding on lichens at the larval stage

Abstract 1. Capital breeders rely solely on resources acquired before breeding, whereas income breeders may obtain considerable amounts of resources following the commencement of reproduction. In income breeders oviposition occurs over a longer time period with a small number of eggs ready to be laid at the start of adult life, whereas capital breeders reproduce more rapidly and contain higher numbers of mature eggs at eclosion relative to potential fecundity. 2. This study explored egg maturation and oviposition strategy of a nocturnal geometrid moth, Cleorodes lichenaria. It was predicted, based on the long larval period of C. lichenaria and the known biology of other geometrids, that this lichen‐feeding geometrid moth concentrates egg production at the beginning of its breeding period and that external nutrients have a limited role on its fecundity. 3. Approximately 46% of eggs were ready to be laid in newly hatched females and approximately 40% of their potential fecundity was realised during the first night, after which the number and the weight of eggs decreased steadily. Feeding or drinking did not increase the fecundity of females. Pupal mass correlated positively with realised fecundity and ovigeny index. 4. Reproduction of C. lichenaria is based solely on larval‐derived resources. It is suggested that females are able to resorb thoracic tissues to increase fecundity and that this ability is probably linked to relatively long lifespan and low ovigeny index of this species, characteristics rarely observed in other geometrid moths.     

Resource allocation to reproduction and soma in Drosophila: a stable isotope analysis of carbon from dietary sugar

Metabolic resources in adults of holometabolous insects may derive either from larval or adult feeding. In Drosophila melanogaster, reproduction and lifespan are differently affected by larval vs. adult resource availability, and it is unknown how larval vs. adult acquired nutrients are differentially allocated to somatic and reproductive function. Here we describe the allocation of carbon derived from dietary sugar in aging female D. melanogaster. Larval and adult flies were fed diets contrasting in sucrose (13)C/(12)C, from which we determined the extent to which carbon acquired at each stage contributed to adult somatic tissue and to egg manufacture. Dietary sugar is very important in egg provisioning; at every age, roughly one half of the carbon in eggs was derived from sugar, which turned over from predominantly larval to entirely adult dietary sources. Sucrose provided approximately 40% of total somatic carbon, of which adult dietary sucrose came to supply approximately 75%. Unlike in eggs, however, adult acquired sucrose did not entirely replace the somatic carbon from larvally acquired sucrose. Because carbon from larval sucrose appears to be fairly "replaceable", larval sucrose cannot be a limiting substrate in resource allocation between reproduction and lifespan.     

A field study of size–fitness relationships in the parasitoid Asobara tabida

1. Many evolutionary models of parasitoid behaviour assume a positive correlation between size and fitness. In this paper we study the size–fitness relationship in the laboratory and in the field using females of the solitary parasitoid Asobara tabida (Hymenoptera: Braconidae).
2. In the laboratory, fecundity, fat reserves and longevity without food were positively correlated with size.
3. Release–recapture experiments in the field showed that dispersal diminishes fat reserves. Dispersal ability is size-dependent: larger females, with larger fat reserves, disperse over larger distances than smaller females.
4. The form of the relationship between size and fitness in the field was estimated in two ways: one based on a comparison of the size distribution of released and recaptured females; the other based on the egg load and fat reserves of wild-caught females. Both showed an accelerating increase of fitness with size.
5. The majority of females appeared to be time-limited. Therefore, the increase in fitness with size is predominantly due to a larger dispersal ability and not to a higher egg load.     

Density reductions by predatory trout increase adult size and fecundity of surviving caddisfly larvae in a detritus-based stream food web

1. In some situations, individuals surviving in environments where predation is intense can grow faster because the benefits of release from intraspecific competition outweigh costs associated with anti-predator responses. Whether these 'thinning' effects of predation occur in detritus-based food webs where resource renewal occurs independently of consumption by consumers was studied. We investigated how effects of predatory brown trout ( Salmo trutta ) on the larvae of the detritivorous stream caddisfly, Zelandopsyche ingens , influenced the size and fecundity of the caddisfly adults.
2. Trout substantially reduced the abundance of Z. ingens larvae, but adult male and female Z. ingens were significantly larger in trout streams compared to fishless streams. Females in trout streams had 33% more eggs than fishless stream females, and egg sizes were not significantly different. In mesocosms, Z. ingens larvae in low density treatments reflecting trout stream abundances grew significantly faster than larvae in high density treatments that were characteristic of fishless stream abundances. Non-lethal trout presence did not influence case building behaviour, feeding rates or growth or Z. ingens larvae, indicating non-lethal effects of predators were negligible.
3. Increased adult size and fecundity associated with trout stream individuals were probably a result of predator thinning of larval density indirectly releasing surviving Z. ingens from intraspecific competition. Thus, predator thinning did influence interactions between larvae in this detritus-based food web as larval growth was strongly density-dependent. However, extrapolating the total number of eggs potentially produced indicates the increased fecundity of females in trout streams would not compensate for losses of larvae to trout predation.