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Reproduction can reduce energy allocation to other life-history traits such as survival and growth. Resource constraints give rise to (co)variation in life-history traits and to heterogeneity in energy acquisition and allocation. At each reproductive opportunity, females face a choice between allocation to current reproduction or to maintenance. Many studies compare reproductive trade-offs between two consecutive years, but few account for the cumulative effects of reproduction over multiple years, a crucial factor in understanding life-history evolution in long-lived iteroparous species. We compared short- (interannual) and long-term (cumulative) reproductive trade-offs with a 14-year capture-mark-recapture study of eastern grey kangaroos, where females can have substantial skeletal growth for several years after maturation. We used a multivariate approach to compare how interannual and multi-annual cumulative reproduction affected growth (n = 378 measurements), mass change (n = 376 measurements) and subsequent reproduction (n = 388 measurements), and to quantify (co)variation between these traits among individuals (n = 107) and years (n = 14). Interannually, young females that reproduced experienced decreased skeletal growth compared to young females that did not reproduce. Reproductive females of all ages experienced reduced mass gain and weaning probability in the following year. The cumulative effects of multiple reproductions included decreased skeletal growth, mass gain and weaning probability in the following year. These effects increased with age and reproductive rate. We found positive trait correlations between mass change, leg growth and subsequent reproduction among individuals and years, though weaker at the cumulative than interannual level. Females experience dynamic interannual and cumulative trade-offs. Our analyses of cumulative costs of reproduction revealed long-term trade-offs as well as cumulative costs that were not apparent when estimating interannual costs. Trait correlations suggested heterogeneity in growth and reproduction among females. Years of increased growth were followed by years of increased reproduction, and years of poor growth were followed by years of poor reproduction. Our exploration of both interannual and cumulative costs of reproduction underscores the need to account for long-term reproductive histories to better understand reproductive trade-offs in long-lived iteroparous species.

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Male and female birds have different roles in reproduction and, thereby in their reproductive investment, which in turn may increase negative effects of poorer breeding conditions caused by e.g., climate change or ecosystem regime shifts. By using a 33-year time series of resightings of Atlantic puffins Fratercula arctica individually colour-ringed as breeders in previous years, we showed that the difference in colony attendance of male and female birds depended on the environmental conditions for raising young, proxied by the average duration of the chick period and size of the herring Clupea harengus fed to the chicks in the colony each year. The longer the chick period, the more was the sex ratio of adults sitting visibly in the colony biased in favour of males. An increase in herring size, indicating better feeding conditions for raising chicks, led to more observations of both sexes. Additionally, we found that birds were observed less with age and females more so than males. We discuss the results in relation to general life-history theory on sexual differences in trade-offs between individual investment in breeding and own survival. Our results suggest that females are increasingly more willing than males to invest in provisioning for the chick the more and longer the chick needs such care.

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Advancing male age is often hypothesized to reduce both male fertility and offspring quality due to reproductive senescence. However, the effects of advancing male age on reproductive output and offspring quality are not always deleterious. For example, older fathers might buffer the effects of reproductive senescence by terminally investing in reproduction. Similarly, males that survive to reproduce at an old age might carry alleles that confer high viability (viability selection), which are then inherited by offspring, or might have high reproductive potential (selective disappearance). Differentiating these mechanisms requires an integrated experimental study of paternal survival and reproductive performance, as well as offspring quality, which is currently lacking. Using a cross-sectional study in Drosophila melanogaster, we test the effects of paternal age at conception (PAC) on paternal survival and reproductive success, and on the lifespans of sons. We discover that mating at an old age is linked with decreased future male survival, suggesting that mating-induced mortality is possibly due to old fathers being frail. We find no evidence for terminal investment and show that reproductive senescence in fathers does not onset until their late-adult life. Additionally, we find that as a father's lifespan increases, his probability of siring offspring increases for older PAC treatments only. Lastly, we show that sons born to older fathers live longer than those born to younger fathers due to viability selection. Collectively, our results suggest that advancing paternal age is not necessarily associated with deleterious effects for offspring and may even lead to older fathers producing longer-lived offspring.

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Many genes and signalling pathways within plant and animal taxa drive the expression of multiple organismal traits. This form of genetic pleiotropy instigates trade-offs among life-history traits if a mutation in the pleiotropic gene improves the fitness contribution of one trait at the expense of another. Whether or not pleiotropy gives rise to conflict among traits, however, likely depends on the resource costs and timing of trait deployment during organismal development. To investigate factors that could influence the evolutionary maintenance of pleiotropy in gene networks, we developed an agent-based model of co-evolution between parasites and hosts. Hosts comprise signalling networks that must faithfully complete a developmental programme while also defending against parasites, and trait signalling networks could be independent or share a pleiotropic component as they evolved to improve host fitness. We found that hosts with independent developmental and immune networks were significantly more fit than hosts with pleiotropic networks when traits were deployed asynchronously during development. When host genotypes directly competed against each other, however, pleiotropic hosts were victorious regardless of trait synchrony because the pleiotropic networks were more robust to parasite manipulation, potentially explaining the abundance of pleiotropy in immune systems despite its contribution to life history trade-offs.

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Sexual dimorphism, the divergence in morphological traits between males and females of the same species, is often accompanied by sex-biased gene expression. However, the majority of research has focused on species with conventional sex roles, where females have the highest energy burden with both egg production and parental care, neglecting the diversity of reproductive roles found in nature. We investigated sex-biased gene expression in Syngnathus typhle, a sex-role reversed species with male pregnancy, allowing us to separate two female traits: egg production and parental care. Using RNA sequencing, we examined gene expression across organs (brain, head kidney and gonads) at various life stages, encompassing differences in age, sex and reproductive status. While some gene groups were more strongly associated with sex roles, such as stress resistance and immune defence, others were driven by biological sex, such as energy and lipid storage regulation in an organ- and age-specific manner. By investigating how genes regulate and are regulated by changing reproductive roles and resource allocation in a model system with an unconventional life-history strategy, we aim to better understand the importance of sex and sex role in regulating gene expression patterns, broadening the scope of this discussion to encompass a wide range of organisms.

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BACKGROUND: Optimal management of voluntary energy expenditure is crucial to the survival and reproductive success of wild animals. Nevertheless, a growing appreciation of inter-individual variation in the internal state driving movement suggests that individuals may follow different, yet equally optimal tactics under the same environmental conditions. However, few studies in wild populations have investigated the occurrence and demographic context of different contemporaneous energetic expenditure tactics. Here, we explore this neglected aspect of energy budgeting in order to determine the effect of life-history traits such as age and reproductive status on the co-occurrence of different energy-budgeting tactics in wild populations. METHODS: We investigated inter-individual heterogeneity in energy expenditure within a wild population of European badgers (Meles meles) by quantifying individual overall dynamic body acceleration (ODBA, from tri-axial accelerometry collars) and total daily energy expenditure (DEE, from doubly-labelled water) during 6-9 day deployments and dosing periods over six different seasons (spring, summer, and autumn) in 2018-2019. We obtained ODBA values for 41 deployments (24 unique badgers) and DEE measurements for 41 dosings (22 unique badgers). We then evaluated correlations between these energetic metrics and computed individual ratios of ODBA/DEE as a proxy for the proportion of total energy spent on activity. We measured the impact of alternative ODBA/DEE ratios on body condition, and use survival models constructed using 29 years of demographic data from the same population to situate body-condition changes in the context of age and reproductive status. RESULTS: Both ODBA and DEE were highly variable between individuals and exhibited season-specific relationships with individual body condition and life-history factors. DEE scaled allometrically with body weight, but only in summer and autumn; post-reproductive female badgers were lighter than other badgers during the spring but expended on average 350 kJ/day more than predicted from allometric scaling. Older badgers expended significantly less energy on movement during the summer than did younger adults. The ratio of ODBA to DEE (OD) provides a measure of proportional investment into movement. This ratio correlated more significantly with next-season body condition than either energetic metric did independently. However, the majority of individuals with high OD ratios were either younger badgers or reproductive females, for which lower body condition typically presented less of a mortality risk in previous analyses of this population. CONCLUSIONS: Within a single population under the same environmental conditions, we found wide inter-individual variation in both mechanical and total energy expenditure. The adoption of different tactics aligns with relationships between life-history parameters and mortality risk previously studied within the population. Crucially, younger badgers and reproductive females appeared able to tolerate energy expenditure tactics that depleted their body condition more than other badgers. These findings provide a mechanism by which differences in individual energetic context set by life history can maintain heterogeneity in wild populations, providing a wide range of potential energetic tactics under changing environmental conditions.

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Life history (LH) strategies are results of trade-offs that species must make due to inhabiting certain ecological niches. Although it is assumed that, through the process of developmental plasticity, similar trade-offs are made by individuals in response to a certain level of harshness and unpredictability of their local environments, the study results on this matter are not consistent. In LH-oriented psychological research, such inconsistencies are often explained as a consequence of significant individual differences in phenotypical quality and owned resources, which make studying trade-offs difficult due to different costs and benefits of the same behaviors taken by different individuals. To verify if traditional LH patterns can be found among individuals with more comparable qualities, than in the general population, the current study was conducted on a group of male criminal offenders, who are typically associated with a fast LH strategy. Our results did not show any support for either LH trade-offs or unidimensional character of LH strategies in the criminal group studied. The traditional biodemographic LH traits, that we used to assess a LH strategy, merged into three well-known LH dimensions (mating, parenting, and somatic effort) that yet turned out to be entirely independent from each other. Moreover, each LH dimension turned out to be uniquely related to a different aspect of the developmental environment. The implications of the obtained results are discussed.

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Lifetime fitness and its determinants are an important topic in the study of behavioral ecology and life-history evolution. Early life conditions comprise some of these determinants, warranting further investigation into their impact. In some mammals, babies born lighter tend to have lower life expectancy than those born heavier, and some of these life-history traits are passed on to offspring, with lighter-born females giving birth to lighter offspring. We investigated how weight at weaning, the relative timing of birth in the season, maternal weight, and maternal age affected the longevity and lifetime reproductive success (LRS) of female Columbian ground squirrels (Urocitellus columbianus). We hypothesized that early life conditions such as offspring weight would not only have lifetime fitness consequences but also intergenerational effects. We found that weight at weaning had a significant impact on longevity, with heavier individuals living longer. The relative timing of an individual's birth did not have a significant association with either longevity or LRS. Individuals born to heavier mothers were found to have significantly higher LRS than those born to lighter mothers. Finally, maternal age was found to be significantly associated with their offspring's LRS, with older mothers having less successful offspring. Our results provide evidence that early life conditions do have lifelong fitness and sometimes intergenerational consequences for Columbian ground squirrels.

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Macronutrient intake impacts physiology, behavior, and gene expression in a wide range of organisms. We used the response surface methodology to compare how life history traits, lifespan, and reproduction differ as a function of protein and carbohydrate intakes under choice and no-choice feeding regimens in the fruit fly, Drosophila melanogaster. We found that when offered a choice of nutritionally complementary foods mated female flies regulated toward a protein to carbohydrate ratio (P:C) that was associated with shortened lifespan and maximal egg production when compared to response surfaces derived from flies fed 1 of a range of fixed diets differing in P:C (no-choice regimen). This difference in lifespan between choice and no-choice feeding was not seen in males or virgin flies, reflecting the fact that increased protein intake is triggered by mating to support egg production. However, whereas in mated females a higher P:C intake was associated with greater egg production under both choice and no-choice feeding, contrary to expectations, choice-fed mated flies laid fewer eggs than no-choice flies on equivalent macronutrient intakes, perhaps reflecting that they had to ingest twice the volume of food to attain an equivalent intake of nutrients than no-choice flies on a diet of equivalent P:C ratio.

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Telomere length and telomere shortening are thought to be critical cellular attributes and processes that are related to an individual's life span and fitness. The general pattern across most taxa is that after birth telomere length gradually decreases with age. Telomere protection and restoration mechanisms are usually assumed to reduce the rate of shortening or at most keep telomere length constant. However, here we have compiled a list of 26 articles showing that there is an increasing number of studies reporting apparent elongation of telomeres (i.e., a net increase in TL from timet to timet+1) often in a considerable proportion of the individuals studied. Moreover, the few studies which have studied telomere elongation in detail show that increases in telomere length are unlikely to be due to measurement error alone. In this article, we argue that episodes of telomere elongation deserve more attention as they could reflect individual strategies to optimise life histories and maximise fitness, which may not be reflected in the overall telomere dynamics patterns. We propose that patterns of telomere (net) elongation may be partly determined by other factors than those causing telomere shortening, and therefore deserve analyses specifically targeted to investigate the occurrence of telomere elongation. We elaborate on two ecological hypotheses that have been proposed to explain patterns of telomere elongation (the 'excess resources elongation' and the 'last resort elongation' hypothesis) and we discuss the current evidence for (or against) these hypotheses and propose ways to test them.

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Many genes and signaling pathways within plant and animal taxa drive the expression of multiple organismal traits. This form of genetic pleiotropy instigates trade-offs among life-history traits if a mutation in the pleiotropic gene improves the fitness contribution of one trait at the expense of another. Whether or not pleiotropy gives rise to conflict among traits, however, likely depends on the resource costs and timing of trait deployment during organismal development. To investigate factors that could influence the evolutionary maintenance of pleiotropy in gene networks, we developed an agent-based model of co-evolution between parasites and hosts. Hosts comprise signaling networks that must faithfully complete a developmental program while also defending against parasites, and trait signaling networks could be independent or share a pleiotropic component as they evolved to improve host fitness. We found that hosts with independent developmental and immune networks were significantly more fit than hosts with pleiotropic networks when traits were deployed asynchronously during development. When host genotypes directly competed against each other, however, pleiotropic hosts were victorious regardless of trait synchrony because the pleiotropic networks were more robust to parasite manipulation, potentially explaining the abundance of pleiotropy in immune systems despite its contribution to life history trade-offs.

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Immune responses benefit organismal fitness by clearing parasites but also exact costs associated with immunopathology and energetic investment. Hosts manage these costs by tightly regulating the induction of immune signaling to curtail excessive responses and restore homeostasis. Despite the theoretical importance of turning off the immune response to mitigate these costs, experimentally connecting variation in the negative regulation of immune responses to organismal fitness remains a frontier in evolutionary immunology. In this study, we used a dose-response approach to manipulate the RNAi-mediated knockdown efficiency of cactus (IκBα), a central regulator of Toll pathway signal transduction in flour beetles (Tribolium castaneum). By titrating cactus activity along a continuous gradient, we derived the shape of the relationship between immune response investment and traits associated with host fitness, including infection susceptibility, lifespan, fecundity, body mass, and gut homeostasis. Cactus knock-down increased the overall magintude of inducible immune responses and delayed their resolution in a dsRNA dose-dependent manner, promoting survival and resistance following bacterial infection. However, these benefits were counterbalanced by dsRNA dose-dependent costs to lifespan, fecundity, body mass, and gut integrity. Our results allowed us to move beyond the qualitative identification of a trade-off between immune investment and fitness to actually derive its functional form. This approach paves the way to quantitatively compare the evolution and impact of distinct regulatory elements on life-history trade-offs and fitness, filling a crucial gap in our conceptual and theoretical models of immune signaling network evolution and the maintenance of natural variation in immune systems.

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Ecological carryover effects, or delayed effects of the environment on an organism's phenotype, are central predictors of individual fitness and a key issue in conservation biology. Climate change imposes increasingly variable environmental conditions that may be challenging to early life-history stages in animals with complex life histories, leading to detrimental physiological and fitness effects in later life. Yet, the latent nature of carryover effects, combined with the long temporal scales over which they can manifest, means that this phenomenon remains understudied and is often overlooked in short-term studies limited to single life-history stages. Herein, we review evidence for the physiological carryover effects induced by elevated ultraviolet radiation (UVR; 280-400 nm) as a potential contributor to recent amphibian population declines. UVR exposure causes a suite of molecular, cellular and physiological consequences known to underpin carryover effects in other taxa, but there is a lack of research linking embryonic and larval UVR exposures to fitness consequences post-metamorphosis in amphibians. We propose that the key impacts of UVR on disease-related amphibian declines are facilitated through carryover effects that bridge embryonic and larval UVR exposure with potential increased disease susceptibility post-metamorphosis. We conclude by identifying a practical direction for the study of ecological carryover effects in amphibians that could guide future ecological research in the broader field of conservation physiology. Only by addressing carryover effects can many of the mechanistic links between environmental change and population declines be elucidated.

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Interlocus sexual conflict (IRSC) occurs because of shared interactions that have opposite effects on male and female fitness. Typically, it is assumed that loci involved in IRSC have sex-limited expression and are thus not directly affected by selective pressures acting on the other sex. However, if loci involved in IRSC have pleiotropic effects in the other sex, intersexual selection can shape the evolutionary dynamics of conflict escalation and resolution, as well as the evolution of reproductive traits linked to IRSC loci, and vice versa. Here we used an artificial selection approach in Japanese quail (Coturnix japonica) to test if female-limited selection on reproductive investment affects the amount of harm caused by males during mating. We found that males originating from lines selected for high female reproductive investment caused more oxidative damage in the female reproductive tract than males originating from lines selected for low female reproductive investment. This male-induced damage was specific to the oviduct and not found in other female tissues, suggesting that it was ejaculate-mediated. Our results suggest that intersexual selection shapes the evolution of IRSC and that male-induced harm may contribute to the maintenance of variation in female reproductive investment.

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AbstractHost-parasite coevolution is expected to drive the evolution of genetic diversity because the traits used in arms races-namely, host range and parasite resistance-are hypothesized to trade off with traits used in resource competition. We therefore tested data for several trade-offs among 93 isolates of bacteriophage λ and 51 Escherichia coli genotypes that coevolved during a laboratory experiment. Surprisingly, we found multiple trade-ups (positive trait correlations) but little evidence of several canonical trade-offs. For example, some bacterial genotypes evaded a trade-off between phage resistance and absolute fitness, instead evolving simultaneous improvements in both traits. This was surprising because our experimental design was predicted to expose resistance-fitness trade-offs by culturing E. coli in a medium where the phage receptor, LamB, is also used for nutrient acquisition. On reflection, LamB mediates not one but many trade-offs, allowing for more complex trait interactions than just pairwise trade-offs. Here, we report that mathematical reasoning and laboratory data highlight how trade-ups should exist whenever an evolutionary system exhibits multiple interacting trade-offs. Does this mean that coevolution should not promote genetic diversity? No, quite the contrary. We deduce that whenever positive trait correlations are observed in multidimensional traits, other traits may trade off and so provide the right circumstances for diversity maintenance. Overall, this study reveals that there are predictive limits when data account only for pairwise trait correlations, and it argues that a wider range of circumstances than previously anticipated can promote genetic and species diversity.

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Actuarial senescence, the decline of survival with age, is well documented in the wild. Rates of senescence vary widely between taxa, to some extent also between sexes, with the fastest life histories showing the highest rates of senescence. Few studies have investigated differences in senescence among populations of the same species, although such variation is expected from population-level differences in environmental conditions, leading to differences in vital rates and thus life histories. We predict that, within species, populations differing in productivity (suggesting different paces of life) should experience different rates of senescence, but with little or no sexual difference in senescence within populations of monogamous, monomorphic species where the sexes share breeding duties. We compared rates of actuarial senescence among three contrasting populations of the Atlantic puffin Fratercula arctica. The dataset comprised 31 years (1990-2020) of parallel capture-mark-recapture data from three breeding colonies, Isle of May (North Sea), Røst (Norwegian Sea) and Hornøya (Barents Sea), showing contrasting productivities (i.e. annual breeding success) and population trends. We used time elapsed since first capture as a proxy for bird age, and productivity and the winter North Atlantic Oscillation Index (wNAO) as proxies for the environmental conditions experienced by the populations within and outside the breeding season, respectively. In accordance with our predictions, we found that senescence rates differed among the study populations, with no evidence for sexual differences. There was no evidence for an effect of wNAO, but the population with the lowest productivity, Røst, showed the lowest rate of senescence. As a consequence, the negative effect of senescence on the population growth rate (λ) was up to 3-5 times smaller on Røst (Δλ = -0.009) than on the two other colonies. Our findings suggest that environmentally induced differences in senescence rates among populations of a species should be accounted for when predicting effects of climate variation and change on species persistence. There is thus a need for more detailed information on how both actuarial and reproductive senescence influence vital rates of populations of the same species, calling for large-scale comparative studies.

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Maximization of life-history traits is under constraints due to both, limitations of resource acquisition and the restricted pathways of resource allocation. Drosophila melanogaster has served as an excellent model organism to not only unravel various trade-offs among life history traits but also numerous aspects of host immune response. Drosophila larvae are semi-aquatic that live, feed and excrete inside the food source-often over-ripe fruits and vegetables that are rich in both commensal and pathogenic microbiota that can impact the larval survival. In this study, we have used six populations of D. melanogaster, three of which are selected for faster pre-adult development and extended adult longevity, and their three ancestral controls, to explore the impact of selection on the basal immune activity in the larval stage. The larvae from selected populations had nearly significantly upregulated plasmatocyte density, significantly higher percent phagocytosis, phagocytic index and higher transcript levels of Tep3, eater and NimC1. Selected populations also had significantly upregulated crystal cell number along with higher transcript of PPO2. Out of seven tested AMPs level, Drosomycin was significantly upregulated in selected populations while Drosocin was significantly higher in control populations. ROS levels were comparable in the selected and control populations. Our results strongly suggest that enhanced basal immune activity during larval stage manages the faster development and could be responsible for comparable larval survival of selected and control populations.

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Studies investigating the trade-off between current and future reproduction often find that increased allocation to current reproduction is associated with a reduction in the number or quality of future offspring. In species that provide parental care, this effect on future offspring may be mediated through a reduced future ability to provide care. Here, we test this idea in the burying beetle Nicrophorus vespilloides, a species in which parents shift the cost of reproduction toward future offspring and provide elaborate parental care. We manipulated brood size to alter the costs females experienced in association with current reproduction and measured the level of parental care during a subsequent breeding attempt. Given that these beetles breed on carcasses of small vertebrates, it is important to consider confounding effects due to benefits associated with resource access during breeding. We, therefore, manipulated access to carrion and measured the level of parental care during a subsequent breeding attempt. We found that females provided the same level of care regardless of previous brood size and resource access, suggesting that neither affected future ability to provide care. This may reflect that parents feed on carrion during breeding, which may buffer against any costs of previous breeding attempts. Our results show that increased allocation to current reproduction is not necessarily associated with a reduction in future ability to provide care. Nevertheless, this may reflect unique aspects of our study system, and we encourage future work on systems where parents do not have access to a rich resource during breeding.

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Early-life conditions have profound effects on many life-history traits, where early-life diet affects both juvenile development, and adult survival and reproduction. Early-life diet also has consequences for the ability of adults to withstand environmental challenges such as starvation, temperature and desiccation. However, it is less well known how early-life diet influences the consequences of infection in adults. Here we test whether varying the larval diet of female Drosophila melanogaster (through altering protein to carbohydrate ratio, P:C) influences the long-term consequences of injury and infection with the bacterial pathogen Pseudomonasentomophila. Given previous work manipulating adult dietary P:C, we predicted that adults from larvae raised on higher P:C diets would have increased reproduction, but shorter lifespans and an increased rate of ageing, and that the lowest larval P:C diets would be particularly detrimental for adult survival in infected individuals. For larval development, we predicted that low P:C would lead to a longer development time and lower viability. We found that early-life and lifetime egg production were highest at intermediate to high larval P:C diets, but this was independent of injury and infection. There was no effect of larval P:C on adult survival. Larval development was quickest on intermediate P:C and egg-to-pupae and egg-to-adult viability were slightly higher on higher P:C. Overall, despite larval P:C affecting several measured traits, we saw no evidence that larval P:C altered the consequence of infection or injury for adult survival or early-life and lifetime reproduction. Taken together, these data suggest that larval diets appear to have a limited impact on the adult life history consequences of infection.

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