Macronutrient composition and glyphosate-based herbicide interact to influence resource allocation

Fitness depends on both the resources that individuals acquire and the allocation of those resources to traits that influence survival and reproduction. Optimal resource allocation differs between females and males as a consequence of their fundamentally different reproductive strategies. However, because most traits have a common genetic basis between the sexes, conflicting selection between the sexes over resource allocation can constrain the evolution of optimal allocation within each sex, and generate trade-offs for fitness between them (i.e. 'sexual antagonism' or 'intralocus sexual conflict'). The theory of resource acquisition and allocation provides an influential framework for linking genetic variation in acquisition and allocation to empirical evidence of trade-offs between distinct life-history traits. However, these models have not considered the emergence of trade-offs within the context of sexual dimorphism, where they are expected to be particularly common. Here, we extend acquisition-allocation theory and develop a quantitative genetic framework for predicting genetically based trade-offs between life-history traits within sexes and between female and male fitness. Our models demonstrate that empirically measurable evidence of sexually antagonistic fitness variation should depend upon three interacting factors that may vary between populations: (1) the genetic variances and between-sex covariances for resource acquisition and allocation traits, (2) condition-dependent expression of resource allocation traits and (3) sex differences in selection on the allocation of resource to different fitness components.

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Heatwaves are increasingly prevalent and can constrain investment into important life-history traits. In addition to heatwaves, animals regularly encounter threats from other organisms in their environments, such as predators. The combination of these two environmental factors introduces a decision-making conflict—heat exposure requires more food intake to fuel investment into fitness-related traits, but foraging in the presence of predators increases the threat of mortality. Thus, we used female variable field crickets (Gryllus lineaticeps) to investigate the effects of heatwaves in conjunction with predation risk (exposed food and water sources, and exposure to scent from black widow spiders, Latrodectus hesperus) on resource acquisition (food intake) and allocation (investment into ovarian and somatic tissues). A simulated heatwave increased food intake and the allocation of resources to reproductive investment. Crickets exposed to high predation risk reduced food intake, but they were able to maintain reproductive investment at an expense to investment into somatic tissue. Thus, heatwaves and predation risk deprioritized investment into self-maintenance, which may impair key physiological processes. This study is an important step towards understanding the ecology of fear in a warming world.

The constancy of the genetic variance-covariance matrix (G matrix) across environments and populations has been discussed and tested empirically over the years but no consensus has so far been reached. In this paper, I present a model in which morphological traits develop hierarchically, and individuals differ in their resource allocation and acquisition patterns. If the variance in resource acquisition is many times larger than the variance in resource allocation then strong genetic correlations are expected, and with almost isometric relations among traits. As the variation in resource acquisition decreases below a certain threshold, the correlations decrease overall and the relations among traits become a function of the allocation patterns, and in particular reflecting the basal division of allocation. A strong bottleneck can break a pattern of strong genetic correlation, but this effect diminishes rapidly with increasing bottleneck size. This model helps to understand why some populations change their genetic correlations in different environments, whereas others do not, since the key factor is the relation between the variances in resource acquisition and allocation. If a change in environment does not lead to a change in this ratio, no change can be expected, whereas if the ratio is changed substantially then major changes can be expected. This model can also help to understand the constancy of morphological patterns within larger taxa as a function of constancy in resource acquisition patterns over time and environments. When this pattern breaks, for example on islands, larger changes can be expected.

The constancy of the genetic variance-covariance matrix (G matrix) across environments and populations has been discussed and tested empirically over the years but no consensus has so far been reached. In this paper, I present a model in which morphological traits develop hierarchically, and individuals differ in their resource allocation and acquisition patterns. If the variance in resource acquisition is many times larger than the variance in resource allocation then strong genetic correlations are expected, and with almost isometric relations among traits. As the variation in resource acquisition decreases below a certain threshold, the correlations decrease overall and the relations among traits become a function of the allocation patterns, and in particular reflecting the basal division of allocation. A strong bottleneck can break a pattern of strong genetic correlation, but this effect diminishes rapidly with increasing bottleneck size. This model helps to understand why some populations change their genetic correlations in different environments, whereas others do not, since the key factor is the relation between the variances in resource acquisition and allocation. If a change in environment does not lead to a change in this ratio, no change can be expected, whereas if the ratio is changed substantially then major changes can be expected. This model can also help to understand the constancy of morphological patterns within larger taxa as a function of constancy in resource acquisition patterns over time and environments. When this pattern breaks, for example on islands, larger changes can be expected.

Microplastics (MPs) are small-sized (< 5 mm) bits of plastic present in all types of environments, including terrestrial ecosystems that are rapidly warming. Yet, the biological interplay between MPs and temperature is poorly understood in terrestrial animals. Here, we addressed three hypotheses to determine how: (1) temperature influences biological responses to MPs, (2) MPs influence thermal biology, and (3) temperature and MPs combine to influence the acquisition and allocation of resources. Specifically, we fed field crickets (Gryllus lineaticeps) different concentrations of nylon (polyamide) microfilaments while they were maintained at 23 °C, 28 °C, or 33 °C. Despite ingesting 2.5-fold more MPs, warmer individuals did not absorb more MPs into their bodies. Exposure to MPs increased investment into somatic tissue and self-maintenance, but individuals consuming MPs still had lower desiccation tolerance. Warming and MPs both promoted food consumption, but they differentially affected the life-history tradeoff between investment into self-maintenance vs. reproduction. In sum, appetite, life-history strategy, and dynamics in the digestive tract may be critical to animals simultaneously exposed to warming and MPs.

Kairomone‐induced anti‐predation defences in zooplankton mediate trophic interactions in aquatic ecosystems. Changes in food quality greatly affect induced defences because of the potential influence on resource allocation. Understanding how zooplankton respond to predation risk under poor nutrition conditions is critical for predicting ecosystem function. The present study focused on the fish kairomone‐induced defences in Daphnia pulex fed unicellular non‐toxic Microcystis aeruginosa. Transcriptions of key genes were detected to interpret changes in morphological and life history traits. Additionally, the degree of responsiveness of traits to increasing proportions of M. aeruginosa in the diet was compared at different endpoints with varied exposure duration. Daphnia pulex decreased body size but showed an elongated tail spine as morphological adaptations to the presence of fish kairomones, supported by enhanced transcriptions of chitin deacetylase and cuticle protein genes. However, with suppressed expression of the related genes, tail spine length was linearly reduced by increasing proportions of M. aeruginosa in the diet, accompanied by decreased somatic growth and reproduction. Presence of fish kairomones interactively affected the inhibitive effects of increasing proportions of M. aeruginosa in the diet on Daphnia growth, reproduction, and tail spine defence but not body size. In addition, the magnitude of effects of M. aeruginosa on Daphnia growth and morphological responses under fish kairomone exposure was increased with the increasing length of exposure time from 3–7 days (reaching maturity) to 14 days (by the end of tests), indicating an aggravated inhibitive effect of M. aeruginosa on induced defences over time. The present study provides references for evaluating zooplankton‐fish interactions under poor nutrition conditions. Since a cyanobacterial bloom may last from a few weeks to several months, experiments involving the whole life span of zooplankton are thought to fully reveal the actual impact of cyanobacteria on interspecific interactions related to zooplankton. In addition, unifying the exposure time to cyanobacteria for comparative studies is recommended in future research.

The life-history of an organism can be studied and understood in terms of acquisition and expenditure of resources. In butterflies, the use of resources for reproduction has been the focus of much research due to the possibility to easily quantify both the input of resources from different sources over the life-cycle as well as the partitioning of these resources to reproduction. In the first part of my thesis we studied how the pattern of partitioning of resources between somatic tissue, such as muscles, wings and exoskeleton, and storage of resources for reproductive purposes during metamorphosis affects reproduction. Theory predicts that reproduction should be strongly dependent on the relative investments in soma and reproductive reserves, but this has generally proven difficult to show empirically. Butterflies are eminently suited for testing this prediction, and our results show that fecundity of female comma butterflies (Polygonia c-album) is strongly influenced by allocation priorities. One aspect of resource use that has not attracted attention until recently is the possibility that butterflies during the reproductive stage can break down flight muscles in the thorax and use muscle nutrients for reproduction. Since butterflies are generally resource limited this could alleviate the costs resulting from somatic investment found in paper I. Through a series of studies we show that thorax mass and nitrogen content decreases over the adult lifespan in a manner consistent with the hypothesis that thorax resources are used for reproduction. In order to determine if these resources could actually come from the flight muscles, something that is known to occur in other insects, the reduction in flight muscle size over the lifespan was studied in the green-veined white butterfly (Pieris napi). The results showed that flight muscle size decreased with on average 75% in long-lived females, suggesting that breakdown of flight muscles could indeed influence reproduction. Taken together, the work in this thesis shows that resource allocation during metamorphosis strongly influences the reproductive potential, but that butterflies can overcome some of the costs of somatic investment by reallocating resources from thoracic tissue to reproduction.

The frequency, duration and co-occurrence of several environmental stressors, such as heat waves and droughts, are increasing globally. Such multiple stressors may have compounding or interactive effects on animals, resulting in either additive or non-additive costs, but animals may mitigate these costs through various strategies of resource conservation or shifts in resource allocation. Through a factorial experiment, we investigated the independent and interactive effects of a simulated heat wave and water limitation on life-history, physiological and behavioral traits. We used the variable field cricket, Gryllus lineaticeps, which exhibits a wing dimorphism that mediates two distinct life-history strategies during early adulthood. Long-winged individuals invest in flight musculature and are typically flight capable, whereas short-winged individuals lack flight musculature and capacity. A comprehensive and integrative approach with G. lineaticeps allowed us to examine whether life-history strategy influenced the costs of multiple stressors as well as the resulting cost-limiting strategies. Concurrent heat wave and water limitation resulted in largely non-additive and single-stressor costs to important traits (e.g. survival and water balance), extensive shifts in resource allocation priorities (e.g. reduced prioritization of body mass) and a limited capacity to conserve resources (e.g. heat wave reduced energy use only when water was available). Life-history strategy influenced the emergency life-history stage because wing morphology and stressor(s) interacted to influence body mass, boldness behavior and immunocompetence. Our results demonstrate that water availability and life-history strategy should be incorporated into future studies integrating important conceptual frameworks of stress across a suite of traits - from survival and life history to behavior and physiology.

Life-history theory predicts a negative correlation between reproduction and survival because individuals differ in their investment in early reproduction at the expense of survival. However, life-history trade-offs can be masked when individual differences in resource allocation are smaller than those in resource acquisition. In polymorphic species, as distinct morphs exhibit differences in intrinsic physiology, the relative effects of resource acquisition and allocation on life-history traits will differ between morphs, contributing to morph-specific life-history correlations. Here, in the wing-dimorphic water strider Aquarius paludum, we found that wing morphs differed in within-morph individual-level life-history correlations. Longer-lived flight-capable long-winged females produced fewer eggs per day and matured later, whereas life-history trade-offs were not observed in short-winged flightless females. The survival-reproduction trade-off observed in long-winged females may be a result of individual differences in the timing of wing muscle histolysis. Individuals that underwent wing histolysis early would have increased reproduction at the expense of a shorter life, whereas individuals with late wing histolysis would have reduced reproduction but a longer life. Short-winged females, who never develop wings, effectively have more resources to allocate to both survival and reproduction, masking any life-history trade-offs. Thus, we suggest that morph-specific effects of resource allocation trade-offs can shape the morph-specific extent of individual variation in life-history strategies, which may contribute to the evolution and maintenance of within-species polymorphism.

Size and growth early in life are associated with physiological development, and these traits influence fitness. Life history theory predicts that the relationship between traits reflect constraints involving allocation and acquisition of resources. Using longitudinal data from 113 wild nestling barn swallows (Hirundo rustica erythrogaster), we first characterized developmental changes in glucose metabolism, a physiological trait involved in energy mobilization and response to stress. Next, we tested hypotheses from life history theory about allocation and acquisition of resources based on associations of nestling size and growth with glucose physiology and assessed whether these relationships are modified by parental care. Larger nestlings had higher baseline blood glucose and larger magnitude of change in glucose in response to a stressor than smaller nestlings. Furthermore, the relationship in which greater growth was associated with a stronger stress response, as indicated by a larger magnitude of increase in glucose levels, was most pronounced among birds in nests that received the lowest amount of parental care. These results suggest that physiological constraints may contribute to the early-life disadvantage of slow growth, especially in the context of lower parental care. While these findings are inconsistent with a trade-off involving differential allocation of resources between life history traits, they align with the differential acquisition hypothesis.

Summary 1Resource acquisition and allocation are the physiological mechanisms integrating foraging and life-history traits. An understanding of the patterns of acquisition and allocation in different environments and organisms is critical to a predictive theory of life history. 2Here I develop an allocation framework, which provides a template for conceptualizing the interactions among resource acquisition, allocation and life-history traits. The framework describes the process through which food is taken in by an organism at specific life stages, then allocated to growth, survival (including maintenance, defence, dispersal, etc), reproduction and further foraging. 3I use the allocation framework to examine allocation to life-history traits in insects under both benign and stressful environments. Stressful environments result from resource scarcity or harsh environmental conditions. I consider effects of consistent stress or variable stress across time. 4Several broad generalizations emerge from empirical studies, viewed in the allocation framework. First, resource congruence, or the requirement for specific nutrient ratios in, for example, eggs, results in different limiting nutrients for each life-history trait. Second, the timing of resource acquisition affects both allocation patterns and the identity of limiting nutrients for a given life-history trait. Third, physiological trade-offs may occur across, not just within, life stages. Fourth, apparent trade-offs may be driven by differences among traits in resource congruence constraints and deleterious effects of excess nutrients on a particular trait. Fifth, allocation response to environmental stress shows age-specific and sex-specific patterns. Sixth, physiological trade-offs are often more pronounced under environmental stress. Finally, even within insects, there is considerable variability in allocation response to environmental stress. We do not yet have sufficiently diverse and thorough case studies to understand why this is so. Studies in the wild, or relating laboratory conditions to wild environments, are also needed. 5Senescence can also be understood in an allocation framework. The present approach provides a necessary functional basis for understanding patterns of senescence in diverse organisms and environments. 6The allocation framework fosters a mechanistic understanding of life-history patterns, and the beginning of an understanding of the processes underlying those patterns.

It is increasingly clear that parental environment can play an important role in determining offspring phenotype. These “transgenerational effects” have been linked to many different components of the environment, including toxin exposure, infection with pathogens and parasites, temperature and food quality. In this study, we focus on the latter, asking how variation in the quantity and quality of nutrition affects future generations. Previous studies have shown that artificial diets are a useful tool to examine the within-generation effects of variation in macronutrient content on life history traits, and could therefore be applied to investigations of the transgenerational effects of parental diet. Synthetic diets varying in total macronutrient content and protein: carbohydrate ratios were used to examine both within- and trans-generational effects on life history traits in a generalist stored product pest, the Indian meal moth Plodia interpunctella. The macronutrient composition of the diet was important for shaping within-generation life history traits, including pupal weight, adult weight, and phenoloxidase activity, and had indirect effects via maternal weight on fecundity. Despite these clear within-generation effects on the biology of P. interpunctella, diet composition had no transgenerational effects on the life history traits of offspring. P. interpunctella mothers were able to maintain their offspring quality, possibly at the expense of their own somatic condition, despite high variation in dietary macronutrient composition. This has important implications for the plastic biology of this successful generalist pest.

Species' life history traits, such as fecundity, and how they co‐vary with other traits are central to models in population and community ecology. Within species, increasing fecundity with body size is often driven by nutritional quality of the diet. How and why fecundity varies among species is poorly understood but likely to be related, at least in part, to patterns of resource acquisition and allocation. This study tested for an interspecific, fecundity–size relationship among caddisfly species and tested whether fecundity covaried with larval diet. Data on fecundity and body size were collated for 102 species in 75 genera and 28 families from around the world. Species were assigned to one of four categories of larval diet (algivores, detritivores, filter‐feeders, predators) and also two combined diet groups, differentiated by the prevalence of animal versus plant material. A limiting relationship best described the positive association between fecundity and body size of all caddisflies, where size set an upper limit to fecundity. Diet explained variation below the upper limit. Compared to species with plant‐based diets, consumers of animal material had higher fecundity and diet‐specific fecundity–size relationships with steeper slopes. All relationships were hypoallometric (slopes less than 1), indicating a disproportionate effect of size on fecundity: in each diet group, large‐bodied species produced absolutely more, but proportionately fewer eggs than smaller‐bodied species, suggesting size‐related shifts in resource allocation. The largest species were detritivores, which is consistent with the Jarman–Bell principle that large animals are likely to have nutritionally poor diets. These diet‐related patterns in fecundity may lead to diet‐related patterns in population dynamics among species within freshwater communities that have not been considered previously.

Allocation of resources to current reproduction may reduce future reproduction, growth, and survival, but individual heterogeneity in resource acquisition may obscure this fitness cost. In capital breeders, heterogeneity in reproductive success is often related to body mass or condition, underlining the importance of stored reserves for reproduction. Heterogeneity in the rate of resource acquisition could also affect reproduction. Resource acquisition depends on food intake, but the effects of individual foraging rate on mass gain and reproductive success in wild herbivorous mammals are unknown. We measured how individual bite rate affected mass change and reproductive success of 55 female eastern gray kangaroos (Macropus giganteus) over 2 years. Females with faster bite rate had greater subsequent mass gain, leading to greater offspring survival. In one of 2 years, bite rate directly increased juvenile survival to 8 months. Bite rate appeared to have a direct effect on survival to weaning for young born to females with above-average mass gain, particularly for females in better body condition. Independent of bite rate, individual mass change explained most of the variation in offspring survival. We found a weak positive effect of body condition on reproductive success, suggesting that condition affected reproductive success through its effect on mass change and bite rate. Kangaroos appeared to combine income and capital breeding strategies to deal with internal and external constraints on resource allocation. Our study underlines the importance of accounting for different sources of individual heterogeneity that may affect trade-offs among life-history traits, with important consequences for population dynamics and the evolution of reproductive strategies.