No apparent cost of evolved immune response in Drosophila melanogaster

Maintenance and deployment of the immune system are costly and are hence predicted to trade‐off with other resource‐demanding traits, such as reproduction. We subjected this longstanding idea to test using laboratory experimental evolution approach. In the present study, replicate populations of Drosophila melanogaster were subjected to three selection regimes—I (Infection with Pseudomonas entomophila), S (Sham‐infection with MgSO₄), and U (Unhandled Control). After 30 generations of selection flies from the I regime had evolved better survivorship upon infection with P. entomophila compared to flies from U and S regimes. However, contrary to expectations and previous reports, we did not find any evidence of trade‐offs between immunity and other life history related traits, such as longevity, fecundity, egg hatchability, or development time. After 45 generations of selection, the selection was relaxed for a set of populations. Even after 15 generations, the postinfection survivorship of populations under relaxed selection regime did not decline. We speculate that either there is a negligible cost to the evolved immune response or that trade‐offs occur on traits such as reproductive behavior or other immune mechanisms that we have not investigated in this study. Our research suggests that at least under certain conditions, life‐history trade‐offs might play little role in maintaining variation in immunity.     

Evolution of Drosophila resistance against different pathogens and infection routes entails no detectable maintenance costs

Pathogens exert a strong selective pressure on hosts, entailing host adaptation to infection. This adaptation often affects negatively other fitness‐related traits. Such trade‐offs may underlie the maintenance of genetic diversity for pathogen resistance. Trade‐offs can be tested with experimental evolution of host populations adapting to parasites, using two approaches: (1) measuring changes in immunocompetence in relaxed‐selection lines and (2) comparing life‐history traits of evolved and control lines in pathogen‐free environments. Here, we used both approaches to examine trade‐offs in Drosophila melanogaster populations evolving for over 30 generations under infection with Drosophila C Virus or the bacterium Pseudomonas entomophila, the latter through different routes. We find that resistance is maintained after up to 30 generations of relaxed selection. Moreover, no differences in several classical life‐history traits between control and evolved populations were found in pathogen‐free environments, even under stresses such as desiccation, nutrient limitation, and high densities. Hence, we did not detect any maintenance costs associated with resistance to pathogens. We hypothesize that extremely high selection pressures commonly used lead to the disproportionate expression of costs relative to their actual occurrence in natural systems. Still, the maintenance of genetic variation for pathogen resistance calls for an explanation.     

PATHOGEN LIFE‐HISTORY TRADE‐OFFS REVEALED IN ALLOPATRY

Trade‐offs in life‐history traits is a central tenet in evolutionary biology, yet their ubiquity and relevance to realized fitness in natural populations remains questioned. Trade‐offs in pathogens are of particular interest because they may constrain the evolution and epidemiology of diseases. Here, we studied life‐history traits determining transmission in the obligate fungal pathogen, Podosphaera plantaginis, infecting Plantago lanceolata. We find that although traits are positively associated on sympatric host genotypes, on allopatric host genotypes relationships between infectivity and subsequent transmission traits change shape, becoming even negative. The epidemiological prediction of this change in life‐history relationships in allopatry is lower disease prevalence in newly established pathogen populations. An analysis of the natural pathogen metapopulation confirms that disease prevalence is lower in newly established pathogen populations and they are more prone to go extinct during winter than older pathogen populations. Hence, life‐history trade‐offs mediated by pathogen local adaptation may influence epidemiological dynamics at both population and metapopulation levels.     

OXIDATIVE STRESS AND THE EVOLUTION OF SEX DIFFERENCES IN LIFE SPAN AND AGEING IN THE DECORATED CRICKET,GRYLLODES SIGILLATUS

The Free Radical Theory of Ageing (FRTA) predicts that oxidative stress, induced when levels of reactive oxygen species exceed the capacity of antioxidant defenses, causes ageing. Recently, it has also been argued that oxidative damage may mediate important life‐history trade‐offs. Here, we use inbred lines of the decorated cricket, Gryllodes sigillatus, to estimate the genetic (co)variance between age‐dependent reproductive effort, life span, ageing, oxidative damage, and total antioxidant capacity within and between the sexes. The FRTA predicts that oxidative damage should accumulate with age and negatively correlate with life span. We find that protein oxidation is greater in the shorter lived sex (females) and negatively genetically correlated with life span in both sexes. However, oxidative damage did not accumulate with age in either sex. Previously we have shown antagonistic pleiotropy between the genes for early‐life reproductive effort and ageing rate in both sexes, although this was stronger in females. In females, we find that elevated fecundity early in life is associated with greater protein oxidation later in life, which is in turn positively correlated with the rate of ageing. Our results provide mixed support for the FRTA but suggest that oxidative stress may mediate sex‐specific life‐history strategies in G. sigillatus.     

Evolutionary genetics of Drosophila ananassae: evidence for trade-offs among several fitness traits

Correlated responses to bi‐directional selection on thorax length, examined on several life‐history traits and chromosome inversion polymorphisms, have revealed apparent novel trade‐offs in Drosophila ananassae. We provide evidence of trade‐offs between hatching time and pupal period, pupal period and egg‐pupa development time, and pupal period and larval development time (LDT). Body size shows positive correlations with ovariole number, LDT and DT (egg–fly). We provide evidence of sexual dimorphism for trade‐offs between longevity and body size and starvation and longevity in females only. Trade‐offs between wing/thorax (W/T) ratio and longevity, W/T ratio and starvation, and DT (egg‐ fly) and longevity are evident in males only. Sexual dimorphism is also evident for inversion polymorphism with body size and longevity. A longevity assay suggests that low line females outlived high line females whereas high line males outlived low line males. The mean longevity in males is negatively correlated with the 2L‐ST and 3R‐ST arrangement frequencies whereas the 3L‐ST arrangement frequency is positively correlated with the mean longevity in males but opposite arrangements are found in females. Absolute starvation resistance is negatively correlated with 2L‐ST and 3R‐ST chromosome arrangements and results in a trade‐off between longevity and absolute starvation resistance in females. Analyses of fecundity, hatchability, and viabilities based on age intervals in both G₁₀ and G₁₃ suggest that the early reproduction is favoured in D. ananassae. The productivity percentage is highest in the high line and there is no effect of late reproduction on it. Overall, we provide some unravelled trade‐offs and striking sex differences, which may help in understanding the life‐history evolution of the species. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90 , 669–685.     

THE JACK OF ALL TRADES IS MASTER OF NONE: A PATHOGEN'S ABILITY TO INFECT A GREATER NUMBER OF HOST GENOTYPES COMES AT A COST OF DELAYED REPRODUCTION

A trade‐off between a pathogen's ability to infect many hosts and its reproductive capacity on each host genotype is predicted to limit the evolution of an expanded host range, yet few empirical results provide evidence for the magnitude of such trade‐offs. Here, we test the hypothesis for a trade‐off between the number of host genotypes that a fungal pathogen can infect (host genotype range) and its reproductive capacity on susceptible plant hosts. We used strains of the oat crown rust fungus that carried widely varying numbers of virulence (avr) alleles known to determine host genotype range. We quantified total spore production and the expression of four pathogen life‐history stages: infection efficiency, time until reproduction, pustule size, and spore production per pustule. In support of the trade‐off hypothesis, we found that virulence level, the number of avr alleles per pathogen strain, was correlated with significant delays in the onset of reproduction and with smaller pustule sizes. Modeling from our results, we conclude that trade‐offs have the capacity to constrain the evolution of host genotype range in local populations. In contrast, long‐term trends in virulence level suggest that the continued deployment of resistant host lines over wide regions of the United States has generated selection for increased host genotype range.     

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.     

Competition strategies and correlated selection on responses to polyandry in the seed beetle Callosobruchus maculatus

Abstract Polyandry reflected in multiple mating with different mates is regarded as favoured by natural selection in males but not necessarily in females, where conflicting effects on fitness components can occur. The present study aims to provide empirical evidence to predict which fitness components may be affected in this sexual conflict using a species that demonstrates potential between‐population variation in their resolution: the cowpea weevil Callosobruchus maculatus. Two strains showing contrasting competition outcomes (scramble × contest) and contrasting life‐history strategies based on trade‐offs between longevity and fecundity are crossed for subsequent selection based on larval‐competition strategy, expecting the production of a correlated response to multiple (polyandrous) mating. Such a response is expected because the scramble strain shows high fecundity (and lower longevity) and would benefit from multiple mating, in contrast with the contest strain, which shows high juvenile mortality. The scramble‐selected lines would evolve a response of increased fecundity and reduced longevity under multiple and potentially polyandrous mating but the contest‐selected lines would not respond to multiple (polyandrous) mating. Instead, both scramble‐ and contest‐selected lines show increased fecundity and reduced longevity with multiple (polyandrous) matings, which did not affect egg weight. Indirect benefits of multiple (polyandrous) mating appear to be relevant for lines showing contest competition among juveniles.     

Dose‐dependent effects of an immune challenge at both ultimate and proximate levels in Drosophila melanogaster

Immune responses are highly dynamic. The magnitude and efficiency of an immune response to a pathogen can change markedly across individuals, and such changes may be influenced by variance in a range of intrinsic (e.g. age, genotype, sex) and external (e.g. abiotic stress, pathogen identity, strain) factors. Life history theory predicts that up‐regulation of the immune system will come at a physiological cost, and studies have confirmed that increased investment in immunity can reduce reproductive output and survival. Furthermore, males and females often have divergent reproductive strategies, and this might drive the evolution of sex‐specific life history trade‐offs involving immunity, and sexual dimorphism in immune responses per se. Here, we employ an experiment design to elucidate dose‐dependent and sex‐specific responses to exposure to a nonpathogenic immune elicitor at two scales – the ‘ultimate’ life history and the underlying ‘proximate’ immune level in Drosophila melanogaster. We found dose‐dependent effects of immune challenges on both male and female components of reproductive success, but not on survival, as well as a response in antimicrobial activity. These results indicate that even in the absence of the direct pathogenic effects that are associated with actual disease, individual life histories respond to a perceived immune challenge – but with the magnitude of this response being contingent on the initial dose of exposure. Furthermore, the results indicate that immune responses at the ultimate life history level may indeed reflect underlying processes that occur at the proximate level.     

The role of fecundity and reproductive effort in defining life‐history strategies of North American freshwater mussels

Selection is expected to optimize reproductive investment resulting in characteristic trade‐offs among traits such as brood size, offspring size, somatic maintenance, and lifespan; relative patterns of energy allocation to these functions are important in defining life‐history strategies. Freshwater mussels are a diverse and imperiled component of aquatic ecosystems, but little is known about their life‐history strategies, particularly patterns of fecundity and reproductive effort. Because mussels have an unusual life cycle in which larvae (glochidia) are obligate parasites on fishes, differences in host relationships are expected to influence patterns of reproductive output among species. I investigated fecundity and reproductive effort (RE) and their relationships to other life‐history traits for a taxonomically broad cross section of North American mussel diversity. Annual fecundity of North American mussel species spans nearly four orders of magnitude, ranging from < 2000 to 10 million, but most species have considerably lower fecundity than previous generalizations, which portrayed the group as having uniformly high fecundity (e.g. > 200000). Estimates of RE also were highly variable, ranging among species from 0.06 to 25.4%. Median fecundity and RE differed among phylogenetic groups, but patterns for these two traits differed in several ways. For example, the tribe Anodontini had relatively low median fecundity but had the highest RE of any group. Within and among species, body size was a strong predictor of fecundity and explained a high percentage of variation in fecundity among species. Fecundity showed little relationship to other life‐history traits including glochidial size, lifespan, brooding strategies, or host strategies. The only apparent trade‐off evident among these traits was the extraordinarily high fecundity of Leptodea, Margaritifera, and Truncilla, which may come at a cost of greatly reduced glochidial size; there was no relationship between fecundity and glochidial size for the remaining 61 species in the dataset. In contrast to fecundity, RE showed evidence of a strong trade‐off with lifespan, which was negatively related to RE. The raw number of glochidia produced may be determined primarily by physical and energetic constraints rather than selection for optimal output based on differences in host strategies or other traits. By integrating traits such as body size, glochidial size, and fecundity, RE appears more useful in defining mussel life‐history strategies. Combined with trade‐offs between other traits such as growth, lifespan, and age at maturity, differences in RE among species depict a broad continuum of divergent strategies ranging from strongly r‐selected species (e.g. tribe Anodontini and some Lampsilini) to K‐selected species (e.g. tribes Pleurobemini and Quadrulini; family Margaritiferidae). Future studies of reproductive effort in an environmental and life‐history context will be useful for understanding the explosive radiation of this group of animals in North America and will aid in the development of effective conservation strategies.     

Immunological larval polyphenism in the map butterfly Araschnia levana reveals the photoperiodic modulation of immunity

The bivoltine European map butterfly (Araschnia levana) displays seasonal polyphenism characterized by the formation of two remarkably distinct dorsal wing phenotypes: The spring generation (A. levana levana) is predominantly orange with black spots and develops from diapause pupae, whereas the summer generation (A. levana prorsa) has black, white, and orange bands and develops from subitaneous pupae. The choice between spring or summer imagoes is regulated by the photoperiod during larval and prepupal development, but polyphenism in the larvae has not been investigated before. Recently, it has been found that the prepupae of A. levana display differences in immunity‐related gene expression, so we tested whether larvae destined to become spring (short‐day) or summer (long‐day) morphs also display differences in innate immunity. We measured larval survival following the injection of a bacterial entomopathogen (Pseudomonas entomophila), the antimicrobial activity in their hemolymph and the induced expression of selected genes encoding antimicrobial peptides (AMPs). Larvae of the short‐day generation died significantly later, exhibited higher antibacterial activity in the hemolymph, and displayed higher induced expression levels of AMPs than those of the long‐day generation. Our study expands the seasonal polyphenism of A. levana beyond the morphologically distinct spring and summer imagoes to include immunological larval polyphenism that reveals the photoperiodic modulation of immunity. This may reflect life‐history traits that manifest as trade‐offs between immunity and fecundity.     

Healthier or bigger? Trade‐off mediating male dimorphism in the black scavenger fly Sepsis thoracica (Diptera: Sepsidae)

1. Life history trade‐offs emerge when limited resources are allocated to multiple functions of an organism. Under highly competitive conditions trade‐offs can result in alternative phenotypes that differ morphologically and physiologically. Such is the case in insect species that grow under high densities, where competition for resources but also the risk of disease contagion is high, prompting important adjustments in immune response and melanic cuticular pigmentation, with consequent sacrifices in other fitness‐related traits. 2. In the present study, the potential trade‐offs between total‐ and active phenoloxidase (PO), body size and body pigmentation in Sepsis thoracica black scavenger flies that show alternative male morphs differing in cuticular pigmentation, and body size were evaluated. 3. As expected, small/dark (obsidian) males showed higher total‐PO activity than larger/orange (amber) males. A negative relationship was found between total‐PO activity and body size in females and obsidian but not amber males, suggesting that growth and immunity are more costly for the former. In contrast, density did not affect PO activity, as predicted by the density‐dependent prophylaxis hypothesis, which had not been tested in dipterans before. However, rearing density did affect the body size negatively in females and amber but not obsidian males, showing that male morph is largely determined by condition‐dependent plasticity rather than genes. 4. This study provides good evidence that trade‐offs between different life‐history traits can result in alternative resource allocation strategies, even within one species. These strategies can produce strikingly different alternative phenotypes, evincing that there is not only one optimal solution to address fitness optimisation.     

Life‐history trade‐offs vary with resource availability across the geographic range of a widespread plant

• Trade‐offs between reproduction, growth and survival arise from limited resource availability in plants. Environmental stress is expected to exacerbate these negative correlations, but no studies have evaluated variation in life‐history trade‐offs throughout species geographic ranges. Here we analyse the costs of growth and reproduction across the latitudinal range of the widespread herb Plantago coronopus in Europe.
• We monitored the performance of thousands of individuals in 11 populations of P. coronopus, and tested whether the effects of growth and reproduction on a set of vital rates (growth, probability of survival, probability of reproduction and fecundity) varied with local precipitation and soil fertility. To account for variation in internal resources among individuals, we analysed trade‐offs correcting for differences in size.
• Growth was negatively affected by previous growth and reproduction. We also found costs of growth and reproduction on survival, reproduction probability and fecundity, but only in populations with low soil fertility. Costs also increased with precipitation, possibly due to flooding‐related stress. In contrast, growth was positively correlated with subsequent survival, and there was a positive covariation in reproduction between consecutive years under certain environments, a potential strategy to exploit temporary benign conditions.
• Overall, we found both negative and positive correlations among vital rates across P. coronopus geographic range. Trade‐offs predominated under stressful conditions, and positive correlations arose particularly between related traits like reproduction investment across years. By analysing multiple and diverse fitness components along stress gradients, we can better understand life‐history evolution across species’ ranges, and their responses to environmental change.

     

Effects of macronutrient intake on the lifespan and fecundity of the marula fruit fly,Ceratitis cosyra (Tephritidae): Extreme lifespan in a host specialist

In insects, lifespan and reproduction are strongly associated with nutrition. The ratio and amount of nutrients individuals consume affect their life expectancy and reproductive investment. The geometric framework (GF) enables us to explore how animals regulate their intake of multiple nutrients simultaneously and determine how these nutrients interact to affect life‐history traits of interest. Studies using the GF on host‐generalist tephritid flies have highlighted trade‐offs between longevity and reproductive effort in females, mediated by the protein‐to‐carbohydrate (P:C) ratio that individuals consume. Here, we tested how P and C intake affect lifespan (LS) in both sexes, and female lifetime (LEP), and daily (DEP) egg production, in Ceratitis cosyra, a host‐specialist tephritid fly. We then determined the P:C ratio that C. cosyra defends when offered a choice of foods. Female LS was optimized at a 0:1 P:C ratio, whereas to maximize their fecundity, females needed to consume a higher P:C ratio (LEP = 1:6 P:C; DEP = 1:2.5 P:C). In males, LS was also optimized at a low P:C ratio of 1:10. However, when given the opportunity to regulate their intake, both sexes actively defended a 1:3 P:C ratio, which is closer to the target for DEP than either LS or LEP. Our results show that female C. cosyra experienced a moderate trade‐off between LS and fecundity. Moreover, the diets that maximized expression of LEP and DEP were of lower P:C ratio than those required for optimal expression of these traits in host‐generalist tephritids or other generalist insects.     

Trade‐offs in osmoregulation and parallel shifts in molecular function follow ecological transitions to freshwater in the Alewife

Adaptation to freshwater may be expected to reduce performance in seawater because these environments represent opposing selective regimes. We tested for such a trade‐off in populations of the Alewife (Alosa pseudoharengus). Alewives are ancestrally anadromous, and multiple populations have been independently restricted to freshwater (landlocked). We conducted salinity challenge experiments, whereby juvenile Alewives from one anadromous and multiple landlocked populations were exposed to freshwater and seawater on acute and acclimation timescales. In response to acute salinity challenge trials, independently derived landlocked populations varied in the degree to which seawater tolerance has been lost. In laboratory‐acclimation experiments, landlocked Alewives exhibited improved freshwater tolerance, which was correlated with reductions in seawater tolerance and hypo‐osmotic balance, suggesting that trade‐offs in osmoregulation may be associated with local adaptation to freshwater. We detected differentiation between life‐history forms in the expression of an ion‐uptake gene (NHE3), and in gill Na⁺/K⁺‐ATPase activity. Trade‐offs in osmoregulation, therefore, may be mediated by differentiation in ion‐uptake and salt‐secreting pathways.     

Interactions between host sex and age of exposure modify the virulence–transmission trade‐off

The patterns of immunity conferred by host sex or age represent two sources of host heterogeneity that can potentially shape the evolutionary trajectory of disease. With each host sex or age encountered, a pathogen's optimal exploitative strategy may change, leading to considerable variation in expression of pathogen transmission and virulence. To date, these host characteristics have been studied in the context of host fitness alone, overlooking the effects of host sex and age on the fundamental virulence–transmission trade‐off faced by pathogens. Here, we explicitly address the interaction of these characteristics and find that host sex and age at exposure to a pathogen affect age‐specific patterns of mortality and the balance between pathogen transmission and virulence. When infecting age‐structured male and female Daphnia magna with different genotypes of Pasteuria ramosa, we found that infection increased mortality rates across all age classes for females, whereas mortality only increased in the earliest age class for males. Female hosts allowed a variety of trade‐offs between transmission and virulence to arise with each age and pathogen genotype. In contrast, this variation was dampened in males, with pathogens exhibiting declines in both virulence and transmission with increasing host age. Our results suggest that differences in exploitation potential of males and females to a pathogen can interact with host age to allow different virulence strategies to coexist, and illustrate the potential for these widespread sources of host heterogeneity to direct the evolution of disease in natural populations.     

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.     

Experimental evolution for generalists and specialists reveals multivariate genetic constraints on thermal reaction norms

Theory predicts the emergence of generalists in variable environments and antagonistic pleiotropy to favour specialists in constant environments, but empirical data seldom support such generalist–specialist trade‐offs. We selected for generalists and specialists in the dung fly Sepsis punctum (Diptera: Sepsidae) under conditions that we predicted would reveal antagonistic pleiotropy and multivariate trade‐offs underlying thermal reaction norms for juvenile development. We performed replicated laboratory evolution using four treatments: adaptation at a hot (31 °C) or a cold (15 °C) temperature, or under regimes fluctuating between these temperatures, either within or between generations. After 20 generations, we assessed parental effects and genetic responses of thermal reaction norms for three correlated life‐history traits: size at maturity, juvenile growth rate and juvenile survival. We find evidence for antagonistic pleiotropy for performance at hot and cold temperatures, and a temperature‐mediated trade‐off between juvenile survival and size at maturity, suggesting that trade‐offs associated with environmental tolerance can arise via intensified evolutionary compromises between genetically correlated traits. However, despite this antagonistic pleiotropy, we found no support for the evolution of increased thermal tolerance breadth at the expense of reduced maximal performance, suggesting low genetic variance in the generalist–specialist dimension.     

Reproductive and post‐reproductive life history of wild‐caught Drosophila melanogaster under laboratory conditions

The life history of the fruit fly (Drosophila melanogaster) is well understood, but fitness components are rarely measured by following single individuals over their lifetime, thereby limiting insights into lifetime reproductive success, reproductive senescence and post‐reproductive lifespan. Moreover, most studies have examined long‐established laboratory strains rather than freshly caught individuals and may thus be confounded by adaptation to laboratory culture, inbreeding or mutation accumulation. Here, we have followed the life histories of individual females from three recently caught, non‐laboratory‐adapted wild populations of D. melanogaster. Populations varied in a number of life‐history traits, including ovariole number, fecundity, hatchability and lifespan. To describe individual patterns of age‐specific fecundity, we developed a new model that allowed us to distinguish four phases during a female's life: a phase of reproductive maturation, followed by a period of linear and then exponential decline in fecundity and, finally, a post‐ovipository period. Individual females exhibited clear‐cut fecundity peaks, which contrasts with previous analyses, and post‐peak levels of fecundity declined independently of how long females lived. Notably, females had a pronounced post‐reproductive lifespan, which on average made up 40% of total lifespan. Post‐reproductive lifespan did not differ among populations and was not correlated with reproductive fitness components, supporting the hypothesis that this period is a highly variable, random ‘add‐on’ at the end of reproductive life rather than a correlate of selection on reproductive fitness. Most life‐history traits were positively correlated, a pattern that might be due to genotype by environment interactions when wild flies are brought into a novel laboratory environment but that is unlikely explained by inbreeding or positive mutational covariance caused by mutation accumulation.     

Exposure to natural pathogens reveals costly aphid response to fungi but not bacteria

Immune responses are costly, causing trade‐offs between defense and other host life history traits. Aphids present a special system to explore the costs associated with immune activation since they are missing several humoral and cellular mechanisms thought important for microbial resistance, and it is unknown whether they have alternative, novel immune responses to deal with microbial threat. Here we expose pea aphids to an array of heat‐killed natural pathogens, which should stimulate immune responses without pathogen virulence, and measure changes in life‐history traits. We find significant reduction in lifetime fecundity upon exposure to two fungal pathogens, but not to two bacterial pathogens. This finding complements recent genomic and immunological studies indicating that pea aphids are missing mechanisms important for bacterial resistance, which may have important implications for how aphids interact with their beneficial bacterial symbionts. In general, recent exploration of the immune systems of non‐model invertebrates has called into question the generality of our current picture of insect immunity. Our data highlight that taking an ecological approach and measuring life‐history traits to a broad array of pathogens provides valuable information that can complement traditional approaches.