Intraspecific variability in egg maturation patterns and associated life‐history trade‐offs in a polyembryonic parasitoid wasp

1. Life‐history theory predicts a trade‐off between the resources allocated to reproduction and those allocated to survival. Early maturation of eggs (pro‐ovigeny) is correlated with small body size and low adult longevity in interspecific comparisons among parasitoids, demonstrating this trade‐off. The handful of studies that have tested for similar correlations within species produced conflicting results. 2. Egg maturation patterns and related life‐history traits were studied in the polyembryonic parasitoid wasp, Copidosoma koehleri (Hymenoptera: Encyrtidae). Although the genus Copidosoma was previously reported to be fully pro‐ovigenic, mean egg loads of host‐deprived females almost doubled within their first 6 days of adulthood. 3. The initial egg‐loads of newly emerged females were determined and age‐specific realised fecundity curves were constructed for their clone‐mate twins. The females' initial egg loads increased with body size, but neither body size nor initial egg load was correlated with longevity and fecundity. 4. The variation in initial egg loads was lowest among clone‐mates, intermediate among non‐clone sisters and highest among non‐sister females. The within‐clone variability indicates environmental influences on egg maturation, while the between‐clone variation may be genetically based. 5. Ovaries of host‐deprived females contained fewer eggs at death (at ～29 days) than on day 6. Their egg loads at death were negatively correlated with life span, consistent with reduced egg production and/or egg resorption. Host deprivation prolonged the wasps' life span, suggesting a survival cost to egg maturation and oviposition. 6. It is concluded that adult fecundity and longevity were not traded off with pre‐adult egg maturation.     

Evaluating the life‐history trade‐off between dispersal capability and reproduction in wing dimorphic insects: a meta‐analysis

A life‐history trade‐off exists between flight capability and reproduction in many wing dimorphic insects: a long‐winged morph is flight‐capable at the expense of reproduction, while a short‐winged morph cannot fly, is less mobile, but has greater reproductive output. Using meta‐analyses, I investigated specific questions regarding this trade‐off. The trade‐off in females was expressed primarily as a later onset of egg production and lower fecundity in long‐winged females relative to short‐winged females. Although considerably less work has been done with males, the trade‐off exists for males among traits primarily related to mate acquisition. The trade‐off can potentially be mitigated in males, as long‐winged individuals possess an advantage in traits that can offset the costs of flight capability such as a shorter development time. The strength and direction of trends differed significantly among insect orders, and there was a relationship between the strength and direction of trends with the relative flight capabilities between the morphs. I discuss how the trade‐off might be both under‐ and overestimated in the literature, especially in light of work that has examined two relevant aspects of wing dimorphic species: (1) the effect of flight‐muscle histolysis on reproductive investment; and (2) the performance of actual flight by flight‐capable individuals.     

Temperature‐sensitive fitness cost of insecticide resistance in Chinese populations of the diamondback moth Plutella xylostella

Alleles conferring a higher adaptive value in one environment may have a detrimental impact on fitness in another environment. Alleles conferring resistance to pesticides and drugs provide textbook examples of this trade‐off as, in addition to conferring resistance to these molecules, they frequently decrease fitness in pesticide/drug‐free environments. We show here that resistance to chlorpyrifos, an organophosphate (OP), in Chinese populations of the diamondback moth, Plutella xylostella, is conferred by two mutations of ace1 – the gene encoding the acetylcholinesterase enzyme targeted by OPs – affecting the amino acid sequence of the corresponding protein. These mutations were always linked, consistent with the segregation of a single resistance allele, ace1R, carrying both mutations, in the populations studied. We monitored the frequency of ace1R (by genotyping more than 20 000 adults) and the level of resistance (through bioassays on more than 50 000 individuals) over several generations. We found that the ace1R resistance allele was costly in the absence of insecticide and that this cost was likely recessive. This fitness costs involved a decrease in fecundity: females from resistant strains laid 20% fewer eggs, on average, than females from susceptible strains. Finally, we found that the fitness costs associated with the ace1R allele were greater at high temperatures. At least two life history traits were involved: longevity and fecundity. The relative longevity of resistant individuals was affected only at high temperatures and the relative fecundity of resistant females – which was already affected at temperatures optimal for development – decreased further at high temperatures. The implications of these findings for resistance management are discussed.     

Sexually dimorphic immune response in the harem polygynous Wellington tree weta Hemideina crassidens

Abstract Adult males are often less immunocompetent than females. One explanation for this is that intense sexual selection causes males to trade‐off investment in immunity with traits that increase mating success. This hypothesis is tested in the Wellington tree weta (Hemideina crassidens), a large, sexually dimorphic orthopteran insect in which males possess enormous mandibular weaponry used during fights for access to female mates. Field‐collected males have a significantly greater immune response (greater melanotic encapsulation) than females, suggesting that body condition, longevity or an allied trait is important to male fitness, or that females require materials for egg production that would otherwise be used to boost immunity. Although immunity is expected to trade‐off against reproductive traits in both sexes, there is no significant relationship between immune response and weapon or testes size in males, nor fecundity in females.     

Effects of multiple mating on the fecundity of an invasive pest (Octodonta nipae): the existence of an intermediate optimal female mating rate

Multiple mating is found in many insect taxa where both of the sexes can mate more than once. For males, this leads to the advantage of increasing their paternity by fertilizing more females. However, there is a trade‐off of resource allocation between reproduction and other life‐history characters. In the present study, the impact of increased mating rate on reproductive fitness of the invasive nipa palm hispid beetle Octodonta nipae Maulik (Coleoptera: Chrysomelidae) is investigated. A series of mating frequencies (i.e. 1, 5, 10, 15, 20 times) is selected from video frame playback, ranking from the minimum to maximum mating rate observed under laboratory conditions over a given time period. Fecundity parameters such as lifetime egg production, egg‐hatching rate, effective oviposition period and longevity are investigated for the evaluation of reproductive efficiency. For female O. nipae, increased fecundity is correlated with the mating frequency. Females mating 15 times lay the largest number of eggs (138.82 ± 6.87) and have a hatching rate of 47.43 ± 4.08%. After mating 20 times, females suffer significant declines in oviposition (90.31 ± 8.38 eggs) and egg‐hatching rate (34.16 ± 4.93%). Moreover, the population growth rate reaches a maximum in the females that mate 15 times. The results show that multiple matings in O. nipae have an intermediate optimal range within which female reproductive success is enhanced, providing empirical evidence for the existence of a trade‐off between costs and benefits during copulation based on resource allocation.     

Female Gryllus vocalis Field Crickets Gain Diminishing Returns from Increasing Numbers of Matings

Although female insects generally gain reproductive benefits from mating frequently, females do not mate unlimited numbers of times. This study asks whether the limit on female mating rate is imposed by trade‐offs between reproduction and survival. Female Gryllus vocalis were given the opportunity to mate 5, 10, or 15 times with novel males, and the effects on daily fecundity (egg production), fertility (proportion of eggs that were fertilized), and female post‐experimental longevity were measured. Females that mated 10 times laid more eggs and had a higher proportion of fertile eggs than females that mated 5 times. However, females that mated 15 times did not lay significantly more eggs or have a higher proportion of fertile eggs than females that mated 10 times. Although number of matings did not affect the date that females laid their last egg, mating more times was associated with a prolonged period of laying fertile eggs. Number of matings did not affect female post‐experimental longevity. Thus, there was no trade‐off between female reproductive effort and survival, even when females mated very large numbers of times. When females were allowed to mate ad libitum, the average number of times that females mated was greater than the number of times that confers maximal fitness. The lack of cost to mating explains why females might be willing to mate beyond the point of diminishing reproductive returns.     

Impaired sperm quality,delayed mating but no costs for offspring fitness in crickets winning a fight

The outcome of male–male contest competition is known to affect male mating success and is believed to confer fitness benefits to females through preference for dominant males. However, by mating with contest winners, females can incur significant costs spanning from decreased fecundity to negative effects on offspring. Hence, identifying costs and benefits of male dominance on female fitness is crucial to unravel the potential for a conflict of interests between the sexes. Here, we investigated males' pre‐ and post‐copulatory reproductive investment and its effect on female fitness after a single contest a using the field cricket Gryllus bimaculatus. We allowed males to fight and immediately measured their mating behaviour, sperm quality and offspring viability. We found that males experiencing a fight, independently of the outcome, delayed matings, but their courtship effort was not affected. However, winners produced sperm of lower quality (viability) compared to losers and to males that did not experience fighting. Results suggest a trade‐off in resource allocation between pre‐ and post‐mating episodes of sexual selection. Despite lower ejaculate quality, we found no fitness costs (fecundity and viability of offspring) for females mated to winners. Overall, our findings highlight the importance of considering fighting ability when assessing male reproductive success, as winners may be impaired in their competitiveness at a post‐mating level.     

Survival costs of reproduction are mediated by parasite infection in wild Soay sheep

A trade‐off between current and future fitness potentially explains variation in life‐history strategies. A proposed mechanism behind this is parasite‐mediated reproductive costs: individuals that allocate more resources to reproduction have fewer to allocate to defence against parasites, reducing future fitness. We examined how reproduction influenced faecal egg counts (FEC) of strongyle nematodes using data collected between 1989 and 2008 from a wild population of Soay sheep in the St. Kilda archipelago, Scotland (741 individuals). Increased reproduction was associated with increased FEC during the lambing season: females that gave birth, and particularly those that weaned a lamb, had higher FEC than females that failed to reproduce. Structural equation modelling revealed future reproductive costs: a positive effect of reproduction on spring FEC and a negative effect on summer body weight were negatively associated with overwinter survival. Overall, we provide evidence that parasite resistance and body weight are important mediators of survival costs of reproduction.     

Mating experience weakens starvation tolerance in the seed bug Togo hemipterus (Heteroptera: Lygaeidae)

Organisms are exposed to various stresses caused by environmental fluctuations. One of the most common stresses is the shortage of food. Individuals of many species must survive periods of starvation. There appears to be a trade‐off between reproduction and survival. When residual reproductive value declines for an individual, life‐history theory predicts an increase in current reproductive investment. Current reproductive investment differs between virgin and mated individuals. It is likely that mating experience influences starvation tolerance. However, few studies have investigated sex differences in the effect of mating experience on starvation tolerance or clarified the causes of reductions in starvation tolerance in both sexes. In the present study, these questions are investigated using the seed bug Togo hemipterus (Heteroptera: Lygaeidae).The results of the present study demonstrate that mating is costly for both sexes. Mated males show very short survival times and a daily reduction in weight, and daily energy expenditures are significantly greater in mated males than in virgin males. It is possible that starvation increases the mating effort of males, such as behavioural activities and the amount of time spent searching for females. A trade‐off between survival duration and lifetime fecundity is found in virgin females. However, there is no trade‐off in mated females, which have very short survival times. Whether male seminal substances contribute to the short survival times of mated females is considered. This is the first report demonstrating the influence of sex and mating experience on starvation tolerance. Sex‐specific causes for reductions in starvation tolerance are discussed.     

Flight during oviposition reduces maternal egg provisioning and influences offspring development in Pararge aegeria (L.)

As a result of increased habitat fragmentation in anthropogenic landscapes, flying insects may be required to travel over larger distances in search of resources such as suitable host plants for oviposition. The oögenesis–flight syndrome hypothesis predicts that physiological constraints caused by an overlap in the resources used by thoracic muscles during flight and during oögenesis (e.g. carbohydrates, lipids and water) result in a resource trade‐off, with any resources used during flight no longer available for reproduction. Increased flight costs could therefore potentially result in a decrease in maternal provisioning of eggs. In the present study, the speckled wood butterfly Pararge aegeria (L.) is used to investigate whether increased flight during oviposition results in changes in maternal investment in eggs and whether this contributes to variation in the development of offspring in subsequent life stages. Forcing females to fly during oviposition directly influences egg size and embryonic development time, and indirectly influences (through changes in egg size) egg hatching success and larval development time. These effects are mediated through ‘selfish maternal effects’, with mothers forced to fly maximizing their fecundity at the expense of investment to individual egg size. The present study demonstrates that a change in maternal provisioning as a result of increased flight during oviposition has the potential to exert nongenetic cross‐generational fitness effects in P. aegeria. This could have important consequences for population dynamics, particularly in fragmented anthropogenic landscapes.     

Clutch size in frugivorous insects as a function of host firmness: the case of the tephritid fly Anastrepha ludens

Abstract. 1. Optimal clutch size theory predicts that individuals will oviposit the number of eggs that increases their fitness. In Anastrepha ludens Loew (Diptera: Tephritidae), females oviposit larger clutches in unripe (firm) fruits than in ripe (soft) fruits. The following hypotheses were tested: (1) Using fruit firmness as an indicator of fruit quality, A. ludens females vary the number of eggs per clutch every time they reach an oviposition decision. (2) Maximising offspring survival with respect to either unripe or ripe fruit requires placing large clutches in firm fruit and smaller clutches in soft fruit. 2. Agar spheres were used as artificial hosts. Three agar concentrations resulted in three degrees of firmness. Mango fruits Mangifera indica L. served as natural hosts. Ripe and unripe fruits were used to test soft and firm host conditions respectively. Females laid significantly larger clutches in the firmer artificial hosts than in the softer hosts. They also laid significantly more eggs in artificial hosts without sugar than in hosts with sugar. Firm (unripe) mangoes also received significantly larger clutches than soft (ripe) mangoes. 3. When an individual female was first presented with a firm artificial host, it laid a large clutch. If subsequently offered a soft host, the female laid a significantly smaller clutch. Finally, if again offered a firm host, clutch size was increased significantly. 4. Possible trade‐offs in offspring fitness were explored in ripe and unripe mangoes by measuring offspring egg‐to‐adult survival, pupal weight, mean adult longevity, and fecundity. Despite the fact that larval survival was greater in soft fruit than in firm fruit, parameters such as pupal weight, mean longevity, and fecundity of adults stemming from both fruit types did not differ significantly. 5. A probable trade‐off between high offspring mortality caused by host unsuitability and low offspring and adult mortality caused by parasitism and predation is discussed as the reason for the exploitation of sub‐optimal hosts.     

Parasite resistance predicts fitness better than fecundity in a natural population of the freshwater snail Potamopyrgus antipodarum

The cost of males should give asexual females an advantage when in competition with sexual females. In addition, high‐fecundity asexual genotypes should have an advantage over low‐fecundity clones, leading to reduction in clonal diversity over time. To evaluate fitness components in a natural population, we measured the annual reproductive rate of individual sexual and asexual female Potamopyrgus antipodarum, a New Zealand freshwater snail, in field enclosures that excluded competitors and predators. We used allozyme genotyping to assign the asexual females to particular clonal genotypes. We found that the most fecund asexual clones had similar or higher fecundity as the top 10% of sexual families, suggesting that fecundity selection, even without the cost of males, would lead to replacement of the sexual population by clones. Consequently, we expected that the clones with the highest fecundity would dominate the natural population. Counter to this prediction, we found that high annual reproductive rates did not correlate with the frequency of clones in the natural population. When we exposed the same clones to parasites in the laboratory, we found that resistance to infection was positively correlated with the frequency of clones in the population. The correlation between fecundity and parasite resistance was negative, suggesting a trade‐off between these two traits. Our results thus suggest that parasite resistance is an important short‐term predictor of the success of asexual P. antipodarum in this population.     

The trade‐off between clutch size and egg mass in tree swallows Tachycineta bicolor is modulated by female body mass

Egg production is a costly component of reproduction for female birds in terms of energy expenditure and maternal investment. Because resources are typically limited, clutch size and egg mass are expected to be constrained, and this putative trade‐off between offspring number and size is at the core of life history theory. Nevertheless, empirical evidence for this trade‐off is equivocal at best, as individual heterogeneity in resource acquisition and allocation may hamper the detection of the negative correlation between egg number and mass within populations. Here, we investigated how female body mass and landscape composition influences clutch size, egg mass, and the relationship between these two traits. To do so, we fitted linear mixed models using data from tree swallows Tachycineta bicolor breeding in a network of 400 nestboxes located along a gradient of agricultural intensity between 2004 and 2011. Our dataset comprised 1463 broods for clutch size analyses and 4371 eggs (from 847 broods laid between 2005–2008) for egg mass analyses. Our results showed that agricultural intensity negatively impacted clutch size, but not egg mass nor the relationship between these two traits. Female mass, on the other hand, modulated the trade‐off between clutch size and egg mass. For heavier females, both traits increased jointly, without evidence of a trade‐off. However, for lighter females, there was a clear negative relationship between clutch size and egg mass. This work shows that accounting for individual heterogeneity in body mass allows the detection of a clutch size/egg mass trade‐off that would have remained undetected otherwise. Identifying habitat and individual effects on resource allocation towards reproductive traits may help bridging the gap between predictions from theory and empirical evidence on life history trade‐offs.     

Fecundity compensation in the three‐spined stickleback Gasterosteus aculeatus infected by the diphyllobothriidean cestode Schistocephalus solidus

Causal explanations for host reproductive phenotypes influenced by parasitism fit into three broad evolutionary models: (1) non‐adaptive side effect; (2) adaptive parasitic manipulation; and (3) adaptive host defence. This study demonstrates fecundity compensation, an adaptive non‐immunological host defence, in the three‐spined stickleback fish (Gasterosteus aculeatus) infected by the diphyllobothriidean cestode Schistocephalus solidus. Both infected and uninfected female sticklebacks produced egg clutches at the same age and size. The reproductive capacity of infected females decreased rapidly with increased parasite : host body mass ratio. Body condition was lower in infected females than uninfected females and decreased with increasing parasite : host mass ratio. Females with clutches had greater body condition than those without clutches. A point biserial correlation showed that there was a body condition threshold necessary for clutch production to occur. Host females apparently had the capacity to produce egg clutches until the prolonged effects of nutrient theft by the parasite and the drain on resources from reproduction precluded clutch formation. Clutch mass, adjusted for female body mass, did not differ significantly between infected and uninfected females. Infected females apparently maintained the same level of reproductive allotment (egg mass as proportion of body mass) as uninfected females. Infected females produced larger clutches of smaller eggs than uninfected females, revealing a trade‐off between egg mass and egg number, consistent with the fecundity compensation hypothesis. The rapid loss of reproductive capacity with severity of infection probably reflects the influence of the parasite combined with a trade‐off between current and future reproduction in the host. Inter‐annual differences in reproductive performance may have reflected ecological influences on host pathology and/or intra‐annual seasonal changes. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Variation in resource acquisition and use among host clones creates key epidemiological trade‐offs

Parasites can certainly harm host fitness. Given such virulence, hosts should evolve strategies to resist or tolerate infection. But what governs those strategies and the costs that they incur? This study illustrates how a fecundity‐susceptibility trade‐off among clonally reared genotypes of a zooplankton (Daphnia dentifera) infected by a fungal parasite (Metschnikowia) arises due to variation in resource acquisition and use by hosts. To make these connections, we used lab experiments and theoretical models that link feeding with susceptibility, energetics, and fecundity of hosts. These feeding‐based mechanisms also produced a fecundity‐survivorship trade‐off. Meanwhile, a parasite spore yield–fecundity trade‐off arose from variation in juvenile growth rate among host clones (another index of resource use), a result that was readily anticipated and explained by the models. Thus, several key epidemiological trade‐offs stem from variation in resource acquisition and use among clones. This connection should catalyze the creation of new theory that integrates resource‐ and gene‐based responses of hosts to disease.     

Antagonistic pleiotropy can maintain fitness variation in annual plants

Antagonistic pleiotropy (AP) is a genetic trade‐off between different fitness components. In annual plants, a trade‐off between days to flower (DTF) and reproductive capacity often determines how many individuals survive to flower in a short growing season, and also influences the seed set of survivors. We develop a model of viability and fecundity selection informed by many experiments on the yellow monkeyflower, Mimulus guttatus, but applicable to many annual species. A viability/fecundity trade‐off maintains stable polymorphism under surprisingly general conditions. We also introduce both spatial heterogeneity and temporal stochasticity in environmental parameters. Neither is necessary for polymorphism, but spatial heterogeneity allows polymorphism while also generating the often observed non‐negative correlations in fitness components.     

Egg maturation strategy and its associated trade-offs: a synthesis focusing on Lepidoptera

Abstract. 1. Insects vary considerably between and within orders, and even within the same genus, in the degree to which the female's lifetime potential egg complement is mature when she emerges as an adult. 2. The ‘ovigeny index’ (OI) – the number of eggs females have ready to lay divided by the lifetime potential fecundity – quantifies variation in the degree of early life concentration of egg production, and also variation in initial reproductive effort. 3. Here, an integrated set of hypotheses is presented, based on a conceptual model of resource allocation and acquisition, concerning trade‐offs at the interspecific level between initial investment in egg production (as measured by OI) and other life‐history traits in holometabolous insects. 4. The evidence supporting each of these hypotheses is reviewed, and particular attention is paid to the Lepidoptera, as relevant life‐history data are rapidly accumulating for this ecologically and economically important group. 5. There is evidence at the interspecific level supporting: (i) a link between OI and a trade‐off between soma and non‐soma in Trichoptera and Hymenoptera (the proportionate allocation to soma decreases with increasing OI); (ii) a negative correlation between OI and dependency on external nutrient inputs (via adult feeding) in Hymenoptera and in Lepidoptera; (iii) a negative correlation between OI and the degree of polyandry (and nuptial gift, i.e. spermatophore, use) in Lepidoptera; (iv) negative correlations between OI and resource re‐allocation capabilities (egg and thoracic musculature resorption) in Hymenoptera and in Lepidoptera; (v) a negative correlation between lifespan and OI in Trichoptera, Hymenoptera, and Lepidoptera, indicating a cost of reproduction; (vi) a link between winglessness and an OI of one in Lepidoptera; (vii) a negative correlation between OI and the degree of female mobility in winged Lepidoptera; and (viii) a negative correlation between OI and larval diet breadth (as mediated by oviposition strategy) in Lepidoptera.     

Life‐history trade‐offs under different larval diets in Drosophila suzukii (Diptera: Drosophilidae)

Most larval drosophilids eat the microorganisms that develop in rotting fruit, a relatively protein‐rich resource. By contrast, the spotted‐wing Drosophila suzukii Matsumara (Diptera: Drosophilidae) uniquely develops in ripening fruit, a protein‐poor, carbohydrate‐rich resource. This shift in larval nutritional niche has led to D. suzukii being a significant agricultural pest in the U.S.A. and Europe. Although occupying a new niche may benefit a species by reducing competition, adaptation in host use may generate trade‐offs affecting fitness. To test the hypothesis that fitness trade‐offs will change with adaptation to novel larval diets, D. suzukii larval development on either a diet of a fresh, ripe blueberry (a natural host) or standard artificial Drosophila media (protein‐rich) is compared and the effect of diet on development time from egg to adult, adult body size and male wing spot area, and female fecundity is assessed. Larval development time differs, with larvae on the blueberry emerging as adults earlier than those on the artificial medium, although other fitness measures do not vary between the two diets. In addition, the faster development time on a blueberry does not trade off with body size as expected, although early fecundity is delayed in females that develop on blueberries. Thus, adaptation to a novel larval diet environment does not come at a cost to the ability to develop in protein‐rich resources.     

Effects of pathogen exposure on life‐history variation in the gypsy moth (Lymantria dispar)

Investment in host defences against pathogens may lead to trade‐offs with host fecundity. When such trade‐offs arise from genetic correlations, rates of phenotypic change by natural selection may be affected. However, genetic correlations between host survival and fecundity are rarely quantified. To understand trade‐offs between immune responses to baculovirus exposure and fecundity in the gypsy moth (Lymantria dispar), we estimated genetic correlations between survival probability and traits related to fecundity, such as pupal weight. In addition, we tested whether different virus isolates have different effects on male and female pupal weight. To estimate genetic correlations, we exposed individuals of known relatedness to a single baculovirus isolate. To then evaluate the effect of virus isolate on pupal weight, we exposed a single gypsy moth strain to 16 baculovirus isolates. We found a negative genetic correlation between survival and pupal weight. In addition, virus exposure caused late‐pupating females to be identical in weight to males, whereas unexposed females were 2–3 times as large as unexposed males. Finally, we found that female pupal weight is a quadratic function of host mortality across virus isolates, which is likely due to trade‐offs and compensatory growth processes acting at high and low mortality levels, respectively. Overall, our results suggest that fecundity costs may strongly affect the response to selection for disease resistance. In nature, baculoviruses contribute to the regulation of gypsy moth outbreaks, as pathogens often do in forest‐defoliating insects. We therefore argue that trade‐offs between host life‐history traits may help explain outbreak dynamics.