Life-history Trade-offs Research Articles

Termites and other social insects as emerging model organisms of ageing research: how to achieve a long lifespan and a high fecundity

ABSTRACT Social insects (termites, ants and some bees and wasps) are emerging model organisms of ageing research. In this Commentary, I outline which advantages they offer compared with other organisms. These include the co-occurrence of extraordinarily long-lived, highly fecund queens together with short-lived workers within colonies that share the same genetic background. I then summarize which new insights have been gained so far from social insect studies. Research on social insects has led to the development of a universal mechanistic framework underlying the regulation of ageing and other life-history trade-offs in insects: the TI-J-LiFe network (short for TOR/IIS–juvenile hormone–lifespan/fecundity). Because of its conservative nature, this network can be extended to also incorporate vertebrates. Current data for social insect models suggest that molecular re-wirings along the I-J-Fe (IIS–juvenile hormone–fecundity) axis of the network can explain the concurrent long lifespans and high fecundity of queens. During social evolution, pathways that foster a high fecundity have apparently been uncoupled from mechanisms that shorten lifespan in solitary insects. Thus, fecundity-related vitellogenesis is uncoupled from life-shortening high juvenile hormone (JH)-titres in the honeybee and from insulin/insulin-like growth factor signalling (IIS) activity in ants. In termites, similarly, vitellogenesis seems tissue-specifically unlinked from JH signalling and IIS activity might have lost life-shortening consequences. However, as in solitary animals, the downstream processes (Li of the TI-J-LiFe network) that cause actual ageing (e.g. oxidative stress, transposable element activity, telomere attrition) seem to differ between species and environments. These results show how apparently hard-wired mechanisms underlying life-history trade-offs can be overcome during evolution.

The Age of Snakes: a comparison of three Canadian species at their northern peripheries

ABSTRACT Aging animals enables an understanding of life-history strategies, population dynamics, and conservation concerns. Such information is particularly wanting for reptiles at their range peripheries where life-history trade-offs make body size an unreliable surrogate for age. Using skeletochronology we quantified the ages of three species sampled near their northern range limits (Common gartersnake – Thamnophis sirtalis, Western Rattlesnake – Crotalus oreganus, Great Basin Gophersnake – Pituophis catenifer). Considerable range in length was seen for snakes of the same age, and the relationship between age and size was stronger in males. Male gartersnakes reached a size associated with sexual maturity in about half the time of females, but for the other two species there was no significant difference between sexes. The oldest snakes sampled were 10–12 years, with one outlier gartersnake estimated at 15 years. Given that females in northern populations cannot reproduce annually, our estimated ages of these snakes suggest reproductive bouts occur only a small number of times during their lifespan, reflecting the precarious existence of northern snake populations. Age data improves our understanding of how life-history varies with locations (including latitude), and further studies that collect contemporary and widespread data on this basic population parameter are required.

Increased Reproductive Output and Telomere Shortening Following Calcium Supplementation in a Wild Songbird.

Life history theory predicts increased parental investment comes with fitness costs, often expressed as negative effects on survival and future reproduction. To better understand the costs of reproduction and life history trade-offs, we evaluated calcium supplementation at a high-elevation site in Colorado as a novel approach to experimentally alter reproductive investment in nesting female Tachycineta bicolor (tree swallow). Calcium is a nutrient critical to avian reproduction as the intake of natural calcium is essential for egg production, embryo development, and nestling growth. Altering calcium availability exclusively during the breeding season allowed examination of individual biological responses to experimental modification of reproduction, as well as the reproductive costs associated with egg production and laying an entire clutch. As a functional endpoint and proxy for fitness and longevity, telomere length was measured at the beginning and end of each breeding season. Telomeres-protective "caps" at the ends of chromosomes-have been shown to shorten with aging and a variety of stressors, including higher reproductive output. Results demonstrate that tree swallow mothers supplemented with calcium during the breeding season experience higher reproductive output and produce offspring with longer telomeres, which came at the cost of relatively shorter telomeres during the reproductive season. These findings provide additional support for reproductive trade-offs, and also challenge previous calcium supplementation studies that suggest excess calcium reduces the cost of reproduction.

Animal personality in multiple stressor environments: the evolutionary ecology of among-individual differences in responses to stressor suites.

Animal personality differences may have evolved as alternative strategies for negotiating multiple stressor landscapes. Indeed, ecologists are increasingly recognizing that interactions among multiple stressors can transform selective landscapes and behavioural and physiological responses to stress regimes. Yet, evaluating this hypothesis poses challenges, as most studies involving relationships between personality variation and the environment consider single stressors. Here, we review the literature to explore the theory and evidence that multiple stressor environments may mediate personality variation. We consider effects on evolution of personality variation, as influenced by life-history, energetic and behavioural trade-offs, and effects on phenotypic expression of personality traits. We then explore how personality variation may modulate behavioural and physiological responses to multiple stressors, and how differential responses may be affected by personality-dependent movement ecology and cognitive strategies. Among-individual differences in responses to multiple stressors are critical to elucidate, as multi-stress interactions may transform animal behavioural and physiological responses relative to those predicted under single stressor scenarios, and because among-individual variation comprises the basis for evolutionary shifts in stress responsiveness and population resiliency to global environmental change.

The fecundity costs of building domed nests in birds.

Animal nests provide a beneficial environment for offspring development and as such contribute to fitness. Gathering and transporting materials to construct nests is energetically costly, but the life history trade-offs associated with the types of nests built are largely unknown. Who contributes to building the nest could also mediate these trade-offs, as building a nest as a couple is expected to be less costly per individual than building alone. Using a comparative analysis on 227 songbird species globally, we found a fecundity cost associated with the type of nest a species builds. Species that build domed nests produce fewer broods per year than species building cups or platforms. Dome nesting species also have larger clutch sizes than open nesting species, but only when the nest is built by a couple and not when females build nests alone. This suggests that building domed nests represents a trade-off with investment in young, especially when females are solely responsible for nest building. More broadly, our results could explain macroevolutionary patterns, such as the recent finding that females, building on their own, more often build open cup rather than domed nests.

The battle of the sexes in humans is highly polygenic

Sex-differential selection (SDS), which occurs when the fitness effects of alleles differ between males and females, can have profound impacts on the maintenance of genetic variation, disease risk, and other key aspects of natural populations. Because the sexes mix their autosomal genomes each generation, quantifying SDS is not possible using conventional population genetic approaches. Here, we introduce a method that exploits subtle sex differences in haplotype frequencies resulting from SDS acting in the current generation. Using data from 300K individuals in the UK Biobank, we estimate the strength of SDS throughout the genome. While only a handful of loci under SDS are individually significant, we uncover highly polygenic signals of genome-wide SDS for both viability and fecundity. Selection coefficients of [Formula: see text] may be typical. Despite its ubiquity, SDS may impose a mortality load of less than 1%. An interesting life-history tradeoff emerges: Alleles that increase viability more strongly in females than males tend to increase fecundity more strongly in males than in females. Finally, we find marginal evidence of SDS on fecundity acting on alleles affecting arm fat-free mass. Taken together, our findings connect the long-standing evidence of SDS acting on human phenotypes with its impact on the genome.

Dynamic soaring decouples dynamic body acceleration and energetics in albatrosses.

Estimates of movement costs are essential for understanding energetic and life-history trade-offs. Although overall dynamic body acceleration (ODBA) derived from accelerometer data is widely used as a proxy for energy expenditure (EE) in free-ranging animals, its utility has not been tested in species that predominately use body rotations or exploit environmental energy for movement. We tested a suite of sensor-derived movement metrics as proxies for EE in two species of albatrosses, which routinely use dynamic soaring to extract energy from the wind to reduce movement costs. Birds were fitted with a combined heart-rate, accelerometer, magnetometer and GPS logger, and relationships between movement metrics and heart rate-derived V̇O2, an indirect measure of EE, were analyzed during different flight and activity modes. When birds were exclusively soaring, a metric derived from angular velocity on the yaw axis provided a useful proxy of EE. Thus, body rotations involved in dynamic soaring have clear energetic costs, albeit considerably lower than those of the muscle contractions required for flapping flight. We found that ODBA was not a useful proxy for EE in albatrosses when birds were exclusively soaring. As albatrosses spend much of their foraging trips soaring, ODBA alone was a poor predictor of EE in albatrosses. Despite the lower percentage of time flapping, the number of flaps was a useful metric when comparing EE across foraging trips. Our findings highlight that alternative metrics, beyond ODBA, may be required to estimate energy expenditure from inertial sensors in animals whose movements involve extensive body rotations.

Progressing beyond colonization strategies to understand arbuscular mycorrhizal fungal life history.

Knowledge of differential life-history strategies in arbuscular mycorrhizal (AM) fungi is relevant for understanding the ecology of this group and its potential role in sustainable agriculture and carbon sequestration. At present, AM fungal life-history theories often focus on differential investment into intra- vs extraradical structures among AM fungal taxa, and its implications for plant benefits. With this Viewpoint we aim to expand these theories by integrating a mycocentric economics- and resource-based life-history framework. As in plants, AM fungal carbon and nutrient demands are stoichiometrically coupled, though uptake of these elements is spatially decoupled. Consequently, investment in morphological structures for carbon vs nutrient uptake is not in competition. We argue that understanding the ecology and evolution of AM fungal life-history trade-offs requires increased focus on variation among structures foraging for the same element, that is within intra- or extraradical structures (in our view a 'horizontal' axis), not just between them ('vertical' axis). Here, we elaborate on this argument and propose a range of plausible life-history trade-offs that could lead to the evolution of strategies in AM fungi, providing testable hypotheses and creating opportunities to explain AM fungal co-existence, and the context-dependent effects of AM fungi on plant growth and soil carbon dynamics.

Detecting context dependence in the expression of life history trade-offs.

Life history trade-offs are one of the central tenets of evolutionary demography. Trade-offs, depicting negative covariances between individuals' life history traits, can arise from genetic constraints, or from a finite amount of resources that each individual has to allocate in a zero-sum game between somatic and reproductive functions. While theory predicts that trade-offs are ubiquitous, empirical studies have often failed to detect such negative covariances in wild populations. One way to improve the detection of trade-offs is by accounting for the environmental context, as trade-off expression may depend on environmental conditions. However, current methodologies usually search for fixed covariances between traits, thereby ignoring their context dependence. Here, we present a hierarchical multivariate 'covariance reaction norm' model, adapted from Martin (2023), to help detect context dependence in the expression of life-history trade-offs using demographic data. The method allows continuous variation in the phenotypic correlation between traits. We validate the model on simulated data for both intraindividual and intergenerational trade-offs. We then apply it to empirical datasets of yellow-bellied marmots (Marmota flaviventer) and Soay sheep (Ovis aries) as a proof-of-concept showing that new insights can be gained by applying our methodology, such as detecting trade-offs only in specific environments. We discuss its potential for application to many of the existing long-term demographic datasets and how it could improve our understanding of trade-off expression in particular, and life history theory in general.

Reproductive consequences of the interaction Trypanosoma cruzi − Triatoma infestans and its trade-off with survival

Relative little is known about fitness effects and life history trade-off of Trypanosoma cruzi in Triatoma infestans, the main vector of Chagas disease in Argentina. Previous studies revealed some costs related to development, excretion, and toxicology or their possible trade-offs, but none address effects on reproduction. To study the effect of T. cruzi infection on reproductive efficiency and survival of T. infestans we set up four treatments: both genders uninfected, both genders infected, female infected – males uninfected and female uninfected − males infected. The infection was induced during the third, fourth, and fifth nymphal instars. Reproductive efficiency and longevity variables were recorded. Our results showed that the infection by T. cruzi increased reproductive efficiency and reduced survival of T. infestans. Pairs where one or both individuals were infected presented a greater percentage copulation, of egg-laying females, the onset of copulation and oviposition occurred earlier, and age-specific fecundity was notably higher. Regarding fertility, infected females displayed higher rates irrespective of the infective status of the male counterpart. A reduction in longevity was observed in infected males and females. These findings highlighted that the infection significantly alters the trade-off reproductive efficiency-survival of T. infestans, with the impact differing according to the infection status of each gender, suggesting a complex interplay rather than a simple additive effect. This response corresponds to the reproductive compensation hypothesis.

Eco-evolutionary dynamics of structured populations in periodically fluctuating environments: a G function approach.

Understanding the ecological and evolutionary dynamics of populations is critical for both basic and applied purposes in a variety of biological contexts. Although several modeling frameworks have been developed to simulate eco-evolutionary dynamics, many fewer address how to model structured populations. In a prior paper, we put forth the first modeling approach to simulate eco-evolutionary dynamics in structured populations under the G function modeling framework. However, this approach does not allow for accurate simulation under fluctuating environmental conditions. To address this limitation, we draw on the study of periodic differential equations to propose a modified approach that uses a different definition of fitness more suitable for fluctuating environments. We illustrate this method with a simple toy model of life history trade-offs. The generality of this approach allows it to be used in a variety of biological contexts.

Does the development environment cause the pace of life to change in a rainforest lizard?

Life history theory emphasizes that finite resources result in allocation trade-offs among the competing interests of self-maintenance, growth, reproduction, and survival. Environmental conditions, particularly during development, can influence these life history trade-offs, leading to the coupling of physiological and behavioural traits with life history strategies. Thus, populations may vary in the pattern of trait covariation, clustering along a fast-slow continuum, termed the extended pace-of-life syndrome (POLS) theory. We aimed to test how variation in ecological conditions influence life history trade-offs and their association with behaviour and physiology by comparing captive bred and wild-collected southern rainforest sunskink (Lampropholis similis). The captive bred skinks were the offspring of the wild-caught skinks, and all tests were conducted in the laboratory. We found that the groups differed, on average, in growth rate, body condition, thermal preferences, sprint performance, and activity. Counter to our expectation, wild-caught skinks exhibited a faster pace of life relative to captive-bred skinks despite experiencing more challenging environmental conditions. Furthermore, life history trade-offs were not detected, nor were traits correlated to form the syndrome. Studies are needed to identify the proximate mechanisms causing life history trade-offs and how they lead to the coupling, or decoupling, of physiological and behavioural traits. Such information will provide vital insight into how ecological forces drive the evolution of traits.

Wolbachia pipientis (Rickettsiales: Rickettsiaceae) mediated effects on the fitness and performance of Aedes aegypti (Diptera: Culicidae) under variable temperatures and initial larval densities.

Wolbachia pipientis (Hertig, 1936), also referred as Wolbachia, is a bacterium present across insect taxa, certain strains of which have been demonstrated to impact the fitness and capacity to transmit viruses in mosquitoes, particularly Aedes aegypti (Linnaeus, 1762). Most studies examine these impacts in limited sets of environmental regimes. Here we seek to understand the impacts of environmentally relevant conditions such as larval density, temperature, and their interaction on wAlbB-infected A. aegypti. Using a factorial design, we measured wAlbB stability (relative density, post-emergence in females, and in progeny), the ability for wAlbB to induce cytoplasmic incompatibility, and bacterial effects on mosquito fitness (fecundity, fertility, and body mass) and performance (adult survival and time to pupation) across 2 temperature regimes (fluctuating and constant) and 2 initial larval densities (low and high). Fluctuating daily regimes of temperature (27 to 40 °C) led to decreased post-emergence wAlbB density and increased wAlbB density in eggs compared to constant temperature (27 °C). An increased fecundity was found in wAlbB-carrying females reared at fluctuating temperatures compared to uninfected wild-type females. wAlbB-carrying adult females showed significantly increased survival than wild-type females. Contrarily, wAlbB-carrying adult males exhibited a significantly lower survival than wild-type males. We found differential effects of assessed treatments (Wolbachia infection status, temperature, and larval density) across mosquito sexes and life stages. Taken together, our results indicate that realistic conditions may not impact dramatically the stability of wAlbB infection in A. aegypti. Nonetheless, understanding the ecological consequence of A. aegypti-wAlbB interaction is complex due to life history tradeoffs under conditions faced by natural populations.

Phenotypically plastic responses to environmental variation are more complex than life history theory predicts.

For insects that exhibit wing polyphenic development, abiotic and biotic signals dictate the adult wing morphology of the insect in an adaptive manner such that in stressful environments the formation of a flight-capable morph is favored and in low-stress environments, a flightless morph is favored. While there is a relatively large amount known about the environmental cues that dictate morph formation in wing polyphenic hemipterans like planthoppers and aphids, whether those cues dictate the same morphs in non-hemipteran (i.e., cricket) wing polyphenic species has not been explicitly investigated. To experimentally test the generality of environmental cue determination of wing polyphenism across taxa with diverse life histories, in this study, we tested the importance of food quantity, parasitic infection, and tactile cues on wing morph determination in the wing polyphenic sand field cricket, Gryllus firmus. Our results also show that certain stress cues, such as severe diet quantity limitation and parasitic infection, actually led to an increase in the production of flightless morph. Based on these findings, our results suggest that physiological and genetic constraints are important to an organism's ability to respond to environmental variation in an adaptive manner beyond simple life history trade-offs.

Coping with stress: Salt type, concentration, and exposure history limit life history tradeoffs in response to road salt salinization

Substantial increases in the salinity of freshwater ecosystems has occurred around the globe from causes such as climate change, industrial operations, and the application of road deicing salts. We know very little about how plastic responses in life history traits or rapid evolution of new traits among freshwater organisms could promote stability in ecological communities affected by salinization. We performed a cohort life history analysis from birth to death with 180 individuals of a ubiquitous freshwater zooplankter to understand how life history traits are affected by exposure to two common salt types causing salinization—sodium chloride (NaCl) and calcium chloride (CaCl2)—across two environmentally relevant concentrations. We also tested if a multi-generational exposure history to high salinity altered life-history responses. We tracked and measured lifespan, time to maturation, brood size, brood interval, and body size. We found smaller brood sizes but slightly longer lifespans occurred at a low concentration of NaCl (230 mg Cl−/L). The longer lifespans led to more, albeit smaller broods, which generated a similar lifetime reproductive output compared to the no-salt control populations. At higher concentrations of NaCl and CaCl2, we found lifetime reproductive output was reduced by 23 % to 83 % relative to control populations because no tradeoff among life history traits occurred. In CaCl2, we observed shorter life spans, longer time intervals between smaller broods, and smaller body sizes leading to reduced lifetime reproductive output. We also found that a multi-generational exposure to the salt types did not convey any advantages for lifetime reproductive output. In some cases, the exposure history worsened the life history trait responses suggesting maladaptation. Our findings suggest that life history tradeoffs for freshwater species can occur in response to salinization, but these tradeoffs will largely depend on salt type and concentration, which will have implications for biodiversity and ecological stability.

A female-biased gene expression signature of dominance in cooperatively breeding meerkats.

Dominance is a primary determinant of social dynamics and resource access in social animals. Recent studies show that dominance is also reflected in the gene regulatory profiles of peripheral immune cells. However, the strength and direction of this relationship differs across the species and sex combinations investigated, potentially due to variation in the predictors and energetic consequences of dominance status. Here, we investigated the association between social status and gene expression in the blood of wild meerkats (Suricata suricatta; n = 113 individuals), including in response to lipopolysaccharide, Gardiquimod (an agonist of TLR7, which detects single-stranded RNA invivo) and glucocorticoid stimulation. Meerkats are cooperatively breeding social carnivores in which breeding females physically outcompete other females to suppress reproduction, resulting in high reproductive skew. They therefore present an opportunity to disentangle the effects of social dominance from those of sex per se. We identify a sex-specific signature of dominance, including 1045 differentially expressed genes in females but none in males. Dominant females exhibit elevated activity in innate immune pathways and a larger fold-change response to LPS challenge. Based on these results and a preliminary comparison to other mammals, we speculate that the gene regulatory signature of social status in the immune system depends on the determinants and energetic costs of social dominance, such that it is most pronounced in hierarchies where physical competition is important and reproductive skew is large. Such a pattern has the potential to mediate life history trade-offs between investment in reproduction versus somatic maintenance.

Comparative life-history responses of lacewings to changes in temperature.

Insects play a crucial role in all ecosystems, and are increasingly exposed to higher in temperature extremes under climate change, which can have substantial effects on their abundances. However, the effects of temperature on changes in abundances or population fitness are filtered through differential responses of life-history components, such as survival, reproduction, and development, to their environment. Such differential responses, or trade-offs, have been widely studied in birds and mammals, but comparative studies on insects are largely lacking, limiting our understanding of key mechanisms that may buffer or exacerbate climate-change effects across insect species. Here, we performed a systematic literature review of the ecological studies of lacewings (Neuroptera), predatory insects that play a crucial role in ecosystem pest regulation, to investigate the impact of temperature on life cycle dynamics across species. We found quantitative information, linking stage-specific survival, development, and reproduction to temperature variation, for 62 species from 39 locations. We then performed a metanalysis calculating sensitives to temperature across life-history processes for all publications. We found that developmental times consistently decreased with temperature for all species. Survival and reproduction however showed a weaker response to temperature, and temperature sensitivities varied substantially among species. After controlling for the effect of temperature on life-history processes, the latter covaried consistently across two main axes of variation related to instar and pupae development, suggesting the presence of life-history trade-offs. Our work provides new information that can help generalize life-history responses of insects to temperature, which can then expand comparative demographic and climate-change research. We also discuss important remaining knowledge gaps, such as a better assessment of adult survival and diapause.

Age estimation in tortoises: an evaluation of methods for the spur-thighed tortoise (Testudo graeca)

Abstract Age and growth-related parameters provide a better understanding of life-history adaptations and trade-offs and can be studied in the wild through capture-mark-recapture (CMR) or sclerochronology (i.e., skeletochronology and counting growth marks on hard structures). In chelonians, skeletochronology is limited to carcasses, CMR is limited by time and funding constraints, but counting shell growth annuli (SGA count) is a cheaper and faster alternative. A long-term CMR study in Testudo graeca from south-eastern Romania allowed us to compare the age estimated by the two sclerochronology methods using carcasses, and calibrate the results with data obtained from recaptured tortoises. We found that the accuracy of SGA counts significantly decreased with time (i.e., years between captures and older individuals). Skeletochronology showed the best results with long bones (i.e., ulna, radius, femur), but overall underestimated the age when compared to SGA counts; we obtained comparable results from these two methods in tortoises up to 17 years old. The oldest age estimated by skeletochronology alone was 28 years, 30 years by SGA counts, and 40 years by SGA counts when calibrated by CMR. The growth models using age estimations from both skeletochronology and SGA counts were similar, highlighting their usefulness in monitoring growth trajectories. Our study showed that while age estimation in tortoises is challenging, a combination of methods can improve its accuracy.

A role of epigenetic mechanisms in regulating female reproductive responses to temperature in a pest beetle.

Many species are threatened by climate change and must rapidly respond to survive in changing environments. Epigenetic modifications, such as DNA methylation, can facilitate plastic responses by regulating gene expression in response to environmental cues. Understanding epigenetic responses is therefore essential for predicting species' ability to rapidly adapt in the context of global environmental change. Here, we investigated the functional significance of different methylation-associated cellular processes on temperature-dependent life history in seed beetles, Callosobruchus maculatus Fabricius 1775 (Coleoptera: Bruchidae). We assessed changes under thermal stress in (1) DNA methyltransferase (Dnmt1 and Dnmt2) expression levels, (2) genome-wide methylation and (3) reproductive performance, with (2) and (3) following treatment with 3-aminobenzamide (3AB) and zebularine (Zeb) over two generations. These drugs are well-documented to alter DNA methylation across the tree of life. We found that Dnmt1 and Dnmt2 were expressed throughout the body in males and females, but were highly expressed in females compared with males and exhibited temperature dependence. However, whole-genome methylation did not significantly vary with temperature, and only marginally or inconclusively with drug treatment. Both 3AB and Zeb led to profound temperature-dependent shifts in female reproductive life history trade-off allocation, often increasing fitness compared with control beetles. Mismatch between magnitude of treatment effects on DNA methylation versus life history effects suggest potential of 3AB and Zeb to alter reproductive trade-offs via changes in DNA repair and recycling processes, rather than or in addition to (subtle) changes in DNA methylation. Together, our results suggest that epigenetic mechanisms relating to Dnmt expression, DNA repair and recycling pathways, and possibly DNA methylation, are strongly implicated in modulating insect life history trade-offs in response to temperature change.

Pleiotropy alleviates the fitness costs associated with resource allocation trade-offs in immune signalling networks.

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.