Stress,drugs and the evolution of reproductive restraint in malaria parasites

Life-history theory predicts that sexually reproducing organisms have evolved to resolve resource-allocation trade-offs between growth/survival versus reproduction, and current versus future reproduction. Malaria parasites replicate asexually in their vertebrate hosts, but must reproduce sexually to infect vectors and be transmitted to new hosts. As different specialized stages are required for these functions, the division of resources between these life-history components is a fundamental evolutionary problem. Here, we test how drug-sensitive and drug-resistant isolates of the human malaria parasite Plasmodium falciparum resolve the trade-off between in-host replication and between-host transmission when exposed to treatment with anti-malarial drugs. Previous studies have shown that parasites increase their investment in sexual stages when exposed to stressful conditions, such as drugs. However, we demonstrate that sensitive parasites facultatively decrease their investment in sexual stages when exposed to drugs. In contrast to previous studies, we tested parasites from a region where treatment with anti-malarial drugs is common and transmission is seasonal. We hypothesize that when exposed to drugs, parasites invest in their survival and future transmission by diverting resources from reproduction to replication. Furthermore, as drug-resistant parasites did not adjust their investment when exposed to drugs, we suggest that parasites respond to changes in their proliferation (state) rather the presence of drugs.     

Host cell preference and variable transmission strategies in malaria parasites

Malaria and other haemosporin parasites must undergo a round of sexual reproduction in their insect vector in order to produce stages that can be transmitted to vertebrate hosts. Consequently, it is crucial that parasites produce the sex ratio (proportion of male sexual stages) that will maximize the number of fertilization and thus, transmission to new vertebrate hosts. There is some evidence to show that, consistent with evolutionary theory, the sex ratios of malaria parasites are negatively correlated to their inbreeding rate. However, recent theory has shown that when fertilization success is compromised, parasites should respond by increasing their investment in sexual stages or by producing a less female biased ration than predicted by their inbreeding rate alone. Here, we show that two species of rodent malaria, Plasmodium chabaudi and Plasmodium vinckei petteri, adopt different strategies in response to host anaemia, a factor though to compromise transmission success: P. chabaudi increases investment in sexual stages, whereas P. vinckei produces a less female biased sex ratio. We suggest that these different transmission strategies may be due to marked differences in host cell preference.     

Malaria and trypanosome transmission: different parasites, same rules?

African trypanosomes produce different specialized stages for within-host replication and between-host transmission and therefore face a resource allocation trade-off between maintaining the current infection (survival) and investment into transmission (reproduction). Evolutionary theory predicts the resolution of this trade-off will significantly affect virulence and infectiousness. The application of life history theory to malaria parasites has provided novel insight into their strategies for survival and reproduction; how this framework can now be applied to trypanosomes is discussed. Specifically, predictions for how parasites trade-off investment in survival and transmission in response to variation in the within-host environment are outlined. An evolutionary approach has the power to explain why patterns of investment vary between strains and during infections, giving important insights into parasite biology.     

Does a trade‐off between current reproductive success and survival affect the honesty of male signalling in species with male parental care?

Recent theory predicted that male advertisement will reliably signal investment in paternal care in species where offspring survival requires paternal care and males allocate resources between advertisement and care. However, the predicted relationship between care and advertisement depended on the marginal gains from investment in current reproductive traits. Life history theory suggests that these fitness gains are also subject to a trade‐off between current and future reproduction. Here, we investigate whether male signalling remains a reliable indicator of parental care when males allocate resources between current advertisement, paternal care and survival to future reproduction. We find that advertisement is predicted to remain a reliable signal of male care but that advertisement may cease to reliably indicate male quality because low‐quality males are predicted to invest in current reproduction, whereas higher‐quality males are able to invest in both current reproduction and survival to future reproduction.     

Predicting optimal transmission investment in malaria parasites

In vertebrate hosts, malaria parasites face a tradeoff between replicating and the production of transmission stages that can be passed onto mosquitoes. This tradeoff is analogous to growth‐reproduction tradeoffs in multicellular organisms. We use a mathematical model tailored to the life cycle and dynamics of malaria parasites to identify allocation strategies that maximize cumulative transmission potential to mosquitoes. We show that plastic strategies can substantially outperform fixed allocation because parasites can achieve greater fitness by investing in proliferation early and delaying the production of transmission stages. Parasites should further benefit from restraining transmission investment later in infection, because such a strategy can help maintain parasite numbers in the face of resource depletion. Early allocation decisions are predicted to have the greatest impact on parasite fitness. If the immune response saturates as parasite numbers increase, parasites should benefit from even longer delays prior to transmission investment. The presence of a competing strain selects for consistently lower levels of transmission investment and dramatically increased exploitation of the red blood cell resource. While we provide a detailed analysis of tradeoffs pertaining to malaria life history, our approach for identifying optimal plastic allocation strategies may be broadly applicable.     

Age at mating and male quality influence female patterns of reproductive investment and survival

The trade‐off between the allocation of resources toward somatic maintenance or reproduction is one of the fundamentals of life history theory and predicts that females invest in offspring at the expense of their longevity or vice versa. Mate quality may also affect life history trade‐offs through mechanisms of sexual conflict; however, few studies have examined the interaction between mate quality and age at first mating in reproductive decisions. Using house crickets (Acheta domesticus), this study examines how survival and reproductive trade‐offs change based on females’ age at first reproduction and exposure to males of varying size. Females were exposed to either a large (presumably high‐quality) or small male at an early (young), middle (intermediate), or advanced (old) age, and longevity and reproductive investment were subsequently tracked. Females mated at a young age had the largest number of eggs but the shortest total lifespans while females mated at older ages produced fewer eggs but had longer total lifespans. The trade‐off between age at first mating and eggs laid appears to be mediated through higher egg‐laying rates and shorter postmating lifespans in females mated later in life. Exposure to small males resulted in shorter lifespans and higher egg‐laying rates for all females indicating that male manipulation of females, presumably through spermatophore contents, varies with male size in this species. Together, these data strongly support a trade‐off between age at first reproduction and lifespan and support the role of sexual conflict in shaping patterns of reproduction.     

Recovery and immune priming modulate the evolutionary trajectory of infection‐induced reproductive strategies

In response to parasite exposure, organisms from a variety of taxa undergo a shift in reproductive investment that may trade off with other life‐history traits including survival and immunity. By suppressing reproduction in favour of somatic and immunological maintenance, hosts can enhance the probability of survival and recovery from infection. By plastically enhancing reproduction through terminal investment, on the other hand, hosts under the threat of disease‐induced mortality could enhance their lifetime reproductive fitness through reproduction rather than survival. However, we know little about the evolution of these strategies, particularly when hosts can recover and even bequeath protection to their offspring. In this study, we develop a stochastic agent‐based model that competes somatic maintenance and terminal investment strategies as they trade off differentially with lifespan, parasite resistance, recovery and transgenerational immune priming. Our results suggest that a trade‐off between reproduction and recovery can drive directional selection for either terminal investment or somatic maintenance, depending on the cost of reproduction to lifespan. However, some conditions, such as low virulence with a high cost of reproduction to lifespan, can favour diversifying selection for the coexistence of both strategies. The introduction of transgenerational priming into the model favours terminal investment when all strategies are equally likely to produce primed offspring, but favours somatic maintenance if it confers even a slight priming advantage over terminal investment. Our results suggest that both immune priming and recovery may modulate the evolution of reproductive shift diversity and magnitude upon exposure to parasites.     

Effects of parental care on resource allocation into immune defense and buccal microbiota in mouthbrooding cichlid fishes*

Sexual dimorphism is founded upon a resource allocation trade‐off between investments in reproduction versus other life‐history traits including the immune system. In species with conventional parental care roles, theory predicts that males maximize their lifetime reproductive success by allocating resources toward sexual selection, while females achieve this through prolonging their lifespan. Here, we examine the interrelation between sexual dimorphism and parental care strategies in closely related maternal and biparental mouthbrooding cichlid fishes from East African Lake Tanganyika. We measured cellular immune parameters, examined the relative expression of 28 immune system and life history‐related candidate genes and analyzed the microbiota composition in the buccal cavity. According to our predictions, maternal mouthbrooders are more sexually dimorphic in immune parameters than biparental mouthbrooders, which has possibly arisen through a differential resource allocation into parental care versus secondary sexual traits. Biparental mouthbrooders, on the other hand, which share the costs of parental care, feature an upregulated adaptive immune response and stronger antiviral properties, while their inflammation response is reduced. Overall, our results suggest a differential resource allocation trade‐off between the two modes of parental investment.     

Host condition as a constraint for parasite reproduction

Environmental stress has been suggested to increase host susceptibility to infections and reduce host ability to resist parasite growth and reproduction, thus benefiting parasites. This prediction stems from expected costs of immune defence; hosts in poor condition should have less resources to be allocated to immune function. However, the alternative hypothesis for response to environmental stress is that hosts in poor condition provide less resources for parasites and/or suffer higher mortality, leading to reduced parasite growth, reproduction and survival. We contrasted these alternative hypotheses in a trematode–snail ( Diplostomum spathaceum – Lymnaea stagnalis ) system by asking: (1) how host condition affects parasite reproduction (amount and quality of produced transmission stages) and (2) how host condition affects the survival of infected host individuals. We experimentally manipulated host condition by starving the snails, and found that parasites produced fewer and poorer quality transmission stages in stressed hosts. Furthermore, starvation increased snail mortality. These findings indicate that in well-established trematode infections, reduced ability of immune allocation has no effect on host exploitation by parasites. Instead, deteriorating resources for the snail host can directly limit the amount of resources available for the parasite. This, together with increased host mortality, may have negative effects on parasite populations in the wild.     

青藏高原东缘块茎堇菜鳞茎分配的个体大小依赖性

块茎堇菜(Viola tuberifera)为青藏高原特有两型闭锁花植物,属多年生草本,具独特的混和交配系统,既可通过早春开放花异花受精和夏季地上地下闭锁花自花受精有性繁殖,还可通过秋季新鳞茎无性繁殖产生后代。高山环境下,异花受精常因花粉限制而无法正常进行,自花受精和克隆繁殖成为保障植物种群正常繁衍的不二之选,而克隆繁殖更能在植株资源消耗最小的情况下保障子代的存活。该文以青藏高原东缘高寒草甸的混合繁育植物块茎堇菜为研究对象,探索其生长期内鳞茎分配的个体大小依赖性,以及植株如何权衡鳞茎的资源分配以适应个体大小的变化。结果表明：块茎堇菜生活史阶段的鳞茎分配具有个体大小依赖性,鳞茎分配与个体大小呈极显著负幂指数相关关系(P<0.01),个体越大,鳞茎分配越小;反之,个体越小,鳞茎分配越高。即块茎堇菜对鳞茎的资源投入受个体大小的制约,通过鳞茎分配比例的高低响应植株自身资源状况的变化,保障在高寒环境下植物种群的生存和繁衍。该研究结果为高山植物克隆繁殖的生活史进化提供了依据。     

Population density and structure drive differential investment in pre‐ and postmating sexual traits in frogs

Sexual selection theory predicts a trade‐off between premating (ornaments and armaments) and postmating (testes and ejaculates) sexual traits, assuming that growing and maintaining these traits is costly and that total reproductive investments are limited. The number of males in competition, the reproductive gains from investing in premating sexual traits, and the level of sperm competition are all predicted to influence how males allocate their finite resources to these traits. Yet, empirical examination of these predictions is currently scarce. Here, we studied relative expenditure on pre‐ and postmating sexual traits among frog species varying in their population density, operational sex ratio, and the number of competing males for each clutch of eggs. We found that the intensifying struggle to monopolize fertilizations as more and more males clasp the same female to fertilize her eggs shifts male reproductive investment toward sperm production and away from male weaponry. This shift, which is mediated by population density and the associated level of male–male competition, likely also explains the trade‐off between pre‐ and postmating sexual traits in our much broader sample of anuran species. Our results highlight the power of such a multilevel approach in resolving the evolution of traits and allocation trade‐offs.     

Testing the effect of early‐life reproductive effort on age‐related decline in a wild insect

The disposable soma theory of ageing predicts that when organisms invest in reproduction they do so by reducing their investment in body maintenance, inducing a trade‐off between reproduction and survival. Experiments on invertebrates in the lab provide support for the theory by demonstrating the predicted responses to manipulation of reproductive effort or lifespan. However, experimental studies in birds and evidence from observational (nonmanipulative) studies in nature do not consistently reveal trade‐offs. Most species studied previously in the wild are mammals and birds that reproduce over multiple discrete seasons. This contrasts with temperate invertebrates, which typically have annual generations and reproduce over a single season. We expand the taxonomic range of senescence study systems to include life histories typical of most temperate invertebrates. We monitored reproductive effort, ageing, and survival in a natural field cricket population over ten years to test the prediction that individuals investing more in early‐reproduction senesce faster and die younger. We found no evidence of a trade‐off between early‐life reproductive effort and survival, and only weak evidence for a trade‐off with phenotypic senescence. We discuss the possibility that organisms with multiple discrete breeding seasons may have greater opportunities to express trade‐offs between reproduction and senescence.     

Stress promotes changes in resource allocation to growth and reproduction in a simultaneous hermaphrodite with indeterminate growth

In iteroparous animals, investment in growth is compromised by investment in reproduction, especially in species with indeterminate growth. Life‐history theory predicts that growth should be favoured over reproduction, assuming size‐related fecundity or survival. Hence, increase body condition represents an increase in reproductive potential. Simultaneous hermaphrodites should adjust their resource allocation to each sex function in response to current conditions but, recently, it has been suggested that, in hermaphrodites, gender allocation should be considered as a three‐way trade‐off, including the investment in somatic growth. Due to the higher costs involved, the female function is affected to a greater extent by environmentally stressful conditions rather than the male function. To examine this, we induced stress in the hermaphroditic earthworm Eisenia fetida (Savigny, 1826) and looked for changes in resource allocation in nonreproductive and reproductive individuals. Experimental stress was induced by using tweezers to elicit contractile escape movements. We predicted that stressed earthworms would preferentially allocate resources to growth. In nonreproductive individuals, however, stress had a negative effect on growth, although weight recovery was rapid once manipulation ceased, indicating the importance of body condition, as well as the existence of mechanisms of compensatory growth for growth trajectories in this earthworm species. The response of reproductive individuals was consistent with our expectation: (1) stressed worms maintained their growth rate at the expense of current reproduction and (2) stressed earthworms laid 25% fewer cocoons, which were 30% lighter than cocoons laid by control earthworms. The present results suggest that E. fetida regulates its reproductive effort and that future reproduction has more impact on its fitness than current reproduction. The trade‐off between current and future reproduction should be taken into consideration in models of sex allocation in simultaneous hermaphrodites. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91 , 593–600.     

Clutch size and malarial parasites in female great tits

life-history models predict an evolutionary trade-off in theallocation of resources to current versus future reproduction.This corresponds, at the physiological level, to a trade-offin the allocation of resources to current reproduction or tothe immune system, which will enhance survival and thereforefuture reproduction. For clutch size, life-history models predicta positive correlation between current investment in eggs andthe subsequent parasite load. In a population of great tits,we analyzed the correlation between natural clutch size of femalesand the subsequent prevalence of Plasmodium spp., a potentiallyharmful blood parasite. Females that showed, 14 days after hatchingof the nestlings, an infection with Plasmodium had a significantlylarger clutch (9.3 eggs ± 0.5 SE, n = 18) than uninfectedfemales (8.0 eggs ± 0.2 SE, n = 80), as predicted bythe allocation trade-off. Clutch size was positively correlatedwith the prevalence of Plasmodium, but brood size 14 days afterhatching was not. This suggests that females incur higher costsduring laying the clutch than during rearing nestlings. Infectionstatus of some females changed between years, and these changeswere significantly correlated with a change in clutch size aspredicted by the trade-off. The link between reproductive effortand parasitism may represent a possible mechanism by which thecost of egg production is mediated into future survival andmay thereby be an important selective force in the shaping ofclutch size     

Body size and the timing of egg production in parasitoid wasps

In insects several key fitness-related variables are positively correlated with intraspecific variation in body size, but little is known about size-related variation in the timing of egg production within species. Female insects are known to vary in the degree to which they concentrate egg production into the early part of life. This variation has been quantified as the ovigeny index, defined as the proportion of the maximum potential lifetime complement of eggs that is mature following emergence from the pupa. We tested the hypothesis that the timing of egg production depends both on body size and on host availability, by means of a dynamic programming model that predicted optimal resource allocation to reproduction and survival together with the resulting ovigeny index, in non-feeding synovigenic parasitoids of different sizes. As body size increases, the proportionate increase in resource allocation to initial egg load is less than the proportionate increase in allocation to lifetime fecundity and potential life span, leading to a deferred investment in reproduction as shown by a decrease in ovigeny index. High habitat quality and high habitat stochasticity in reproductive opportunities have a significant effect on the optimal allocation of resources to reproduction and survival, and thus select for early reproduction, i.e. an increased ovigeny index. The ovigeny concept – ovigeny index together with its life-history correlates – enables understanding of the general occurrence of size-related deferment of reproductive investment in parasitoid wasps and also helps explain a significant part of the considerable life-history variation found among such insects.     

Genetic variation and evolutionary trade-offs for sexual and asexual reproductive modes in Allium vineale (Liliaceae)

Populations of Allium vineale commonly include individuals with very different allocation patterns to three modes of reproduction: sexual flowers, aerially produced asexual bulbils, and belowground asexual offsets. If selection is currently acting to maintain these different allocation patterns there must be a genetic basis for variation in allocation to these three reproductive modes. In addition, negative genetic correlations between reproductive traits would imply evolutionary trade-offs among reproductive strategies. We evaluated the heritability of these allocation patterns by growing 16 clones from a single population in the greenhouse at two levels of fertilization. Bulb mass and the mass and number of bulbils, offsets, and flowers were used as response variables, in addition to the proportion allocated to each reproductive mode. We found evidence of substantial heritable variation in allocation to sexual reproduction and in allocation within the two modes of asexual reproduction, indicating high sensitivity of these allocation patterns to natural selection. We also found evidence of strong negative genetic correlations between bulbil and flower traits, as well as between bulbil and offset traits, with one group of genotypes allocating greater resources to aerial asexual bulbils and the second group allocating more resources to belowground asexual offsets and aerial flowers. Phenotypic plasticity in allocation to above- vs. belowground asexual reproduction and sexual vs. asexual aerial reproduction was limited, indicating that plants are unlikely to change reproductive mode in response to nutrient availability. Together, then, we have demonstrated strong heritability for, and trade-offs in, the reproductive allocation patterns within this plant population.     

Consequences of hierarchical allocation for the evolution of life-history traits

Resource allocation within individuals may often be hierarchical, and this may have important effects on genetic correlations and on trait evolution. For example, organisms may divide energy between reproduction and somatic growth and then subdivide reproductive resources. Genetic variation in allocation to pathways early in such hierarchies (e.g., reproduction) can cause positive genetic correlations between traits that trade off (e.g., offspring size and number) because some individuals invest more resources in reproduction than others. We used quantitative-genetic models to explore the evolutionary implications of allocation hierarchies. Our results showed that when variation in allocation early in the hierarchy exceeds subsequent variation in allocation, genetic covariances and initial responses to selection do not reflect trade-offs occurring at later levels in the hierarchy. This general pattern was evident for many starting allocations and optima and for whether traits contributed multiplicatively or additively to fitness. Finally, artificial selection on a single trait revealed masked trade-offs when variation in early allocation was comparable to subsequent variation in allocation. This result confirms artificial selection as a powerful, but not foolproof, method of detecting trade-offs. Thus, allocation hierarchies can profoundly affect life-history evolution by causing traits to evolve in the opposite direction to that predicted by trade-offs.     

The role of vegetative spread and seed dispersal for optimal life histories of clonal plants: a simulation study

Sexual and vegetative reproduction of clonal plants phenotypically differ in dispersal distance, in the phenology of offspring production and establishment, and in the success of establishment. We applied a combination of analytical and of spatially explicit individual-based simulation modelling to calculate long-term fitness. We predicted optimal clonal plant life histories in a parameter space spanned by stolon number, stolon internode length, and relative allocation to sexual and vegetative reproduction. For a given allocation to sexual reproduction and number of stolons, fitness was optimised for rather short internode lengths under small disturbances, and for the longest possible internodes under larger disturbances. A trade-off between length and number of vegetative spacers drew parameters away from their unrestricted optima. Now, intermediate length and number of spacers led to maximum fitness under large disturbances. Simultaneous trade-offs between sexual and vegetative reproduction and between the length and number of spacers could also lead to fitness optima at intermediate parameter values, depending on the success of seedling establishment. We demonstrated that spatial habitat structure (1) selects for an efficient use of available space either by optimum internode length or by investment into seeds, which disperse farther than vegetative spacers, and (2) leads to an interaction between trade-offs. We conclude, that dispersal distance, i.e. a spatial life-history component, and trade-offs must be included in considerations on adaptive evolution of clonal life histories.     

Partitioning the influence of ecology across scales on parasite evolution

Vector‐borne parasites must succeed at three scales to persist: they must proliferate within a host, establish in vectors, and transmit back to hosts. Ecology outside the host undergoes dramatic seasonal and human‐induced changes, but predicting parasite evolutionary responses requires integrating their success across scales. We develop a novel, data‐driven model to titrate the evolutionary impact of ecology at multiple scales on human malaria parasites. We investigate how parasites invest in transmission versus proliferation, a life‐history trait that influences disease severity and spread. We find that transmission investment controls the pattern of host infectiousness over the course of infection: a trade‐off emerges between early and late infectiousness, and the optimal resolution of that trade‐off depends on ecology outside the host. An expanding epidemic favors rapid proliferation, and can overwhelm the evolutionary influence of host recovery rates and mosquito population dynamics. If transmission investment and recovery rate are positively correlated, then ecology outside the host imposes potent selection for aggressive parasite proliferation at the expense of transmission. Any association between transmission investment and recovery represents a key unknown, one that is likely to influence whether the evolutionary consequences of interventions are beneficial or costly for human health.     

Female reproduction bears no survival cost in captivity for gray mouse lemurs

The survival cost of reproduction has been revealed in many free‐ranging vertebrates. However, recent studies on captive populations failed to detect this cost. Theoretically, this lack of survival/reproduction trade‐off is expected when resources are not limiting, but these studies may have failed to detect the cost, as they may not have fully accounted for potential confounding effects, in particular interindividual heterogeneity. Here, we investigated the effects of current and past reproductive effort on later survival in captive females of a small primate, the gray mouse lemur. Survival analyses showed no cost of reproduction in females; and the pattern was even in the opposite direction: the higher the reproductive effort, the higher the chances of survival until the next reproductive event. These conclusions hold even while accounting for interindividual heterogeneity. In agreement with aforementioned studies on captive vertebrates, these results remind us that reproduction is expected to be traded against body maintenance and the survival prospect only when resources are so limiting that they induce an allocation trade‐off. Thus, the cost of reproduction has a major extrinsic component driven by environmental conditions.