Herbivore-mediated ecological costs of reproduction shape the life history of an iteroparous plant

Plant reproduction yields immediate fitness benefits but can be costly in terms of survival, growth, and future fecundity. Life-history theory posits that reproductive strategies are shaped by trade-offs between current and future fitness that result from these direct costs of reproduction. Plant reproduction may also incur indirect ecological costs if it increases susceptibility to herbivores. Yet ecological costs of reproduction have received little empirical attention and remain poorly integrated into life-history theory. Here, we provide evidence for herbivore-mediated ecological costs of reproduction, and we develop theory to examine how these costs influence plant life-history strategies. Field experiments with an iteroparous cactus (Opuntia imbricata) indicated that greater reproductive effort (proportion of meristems allocated to reproduction) led to greater attack by a cactus-feeding insect (Narnia pallidicornis) and that damage by this herbivore reduced reproductive success. A dynamic programming model predicted strongly divergent optimal reproductive strategies when ecological costs were included, compared with when these costs were ignored. Meristem allocation by cacti in the field matched the optimal strategy expected under ecological costs of reproduction. The results indicate that plant reproductive allocation can strongly influence the intensity of interactions with herbivores and that associated ecological costs can play an important selective role in the evolution of plant life histories.     

Multiple mating in the traumatically inseminating Warehouse pirate bug, Xylocoris flavipes: effects on fecundity and longevity

Optimal mating frequencies differ between sexes as a consequence of the sexual differentiation of reproductive costs per mating, where mating is normally more costly to females than males. In mating systems where sexual reproduction is costly to females, sexual conflict may cause both direct (i.e. by reducing female fecundity or causing mortality) and indirect (i.e. increased risk of mortality, reduced offspring viability) reductions in lifetime reproductive success of females, which have individual and population consequences. We investigated the direct and indirect costs of multiple mating in a traumatically inseminating (TI) predatory Warehouse pirate bug, Xylocoris flavipes (Reuter) (Hemiptera: Anthocoridae), where the male penetrates the female's abdomen during copulation. This study aimed to quantify the effects of TI on female fecundity, egg viability, the lifetime fecundity schedule, longevity and prey consumption in this cosmopolitan biocontrol agent. We found no difference in the total reproductive output between mating treatments in terms of total eggs laid or offspring viability, but there were significant differences found in daily fecundity schedules and adult longevity. In terms of lifetime reproduction, female Warehouse pirate bugs appear to be adapted to compensate for the costs of TI mating to their longevity.     

THE EVOLUTION OF REPRODUCTIVE EFFORT IN LIZARDS AND SNAKES

Life history theory suggests that the optimal evolved level of reproductive effort (RE) for an organism depends upon the degree to which additional current reproductive investment reduces future reproductive output. Future reproduction can be decreased in two ways, through (i) decreases in the organism's survival rate, and/or (ii) decreases in the organism's growth (and hence subsequent fecundity). The latter tradeoff–that is, the “potential fecundity cost”—should affect the evolution of RE only in species with relatively high survival rate, a relatively high rate of fecundity increase with body size, or a relatively high reproductive frequency per annum. Unless these conditions are met, the probable benefit in future fecundity obtained from decreasing present reproductive output is too low for natural selection to favor any reduction in RE below the maximum physiologically possible. Published data on survival rate, reproductive frequency and relative clutch mass (RCM) suggest that many lizard species fall well below the level at which natural selection can be expected to influence RE through such “potential fecundity” tradeoffs. Hence, the relative allocation of resources between growth and reproduction is unlikely to be directly optimized by natural selection in these animals. Instead, energy allocation should influence the evolution of RE only indirectly, via effects on an organism's probability of survival during reproduction. Survival costs of reproduction may be the most important evolutionary determinants of RE in many reptiles, and information on the nature and extent of such costs is needed before valid measures of reptilian RE can be constructed.     

Costs of reproduction and terminal investment by females in a semelparous marsupial

Evolutionary explanations for life history diversity are based on the idea of costs of reproduction, particularly on the concept of a trade-off between age-specific reproduction and parental survival, and between expenditure on current and future offspring. Such trade-offs are often difficult to detect in population studies of wild mammals. Terminal investment theory predicts that reproductive effort by older parents should increase, because individual offspring become more valuable to parents as the conflict between current versus potential future offspring declines with age. In order to demonstrate this phenomenon in females, there must be an increase in maternal expenditure on offspring with age, imposing a fitness cost on the mother. Clear evidence of both the expenditure and fitness cost components has rarely been found. In this study, we quantify costs of reproduction throughout the lifespan of female antechinuses. Antechinuses are nocturnal, insectivorous, forest-dwelling small (20-40 g) marsupials, which nest in tree hollows. They have a single synchronized mating season of around three weeks, which occurs on predictable dates each year in a population. Females produce only one litter per year. Unlike almost all other mammals, all males, and in the smaller species, most females are semelparous. We show that increased allocation to current reproduction reduces maternal survival, and that offspring growth and survival in the first breeding season is traded-off with performance of the second litter in iteroparous females. In iteroparous females, increased allocation to second litters is associated with severe weight loss in late lactation and post-lactation death of mothers, but increased offspring growth in late lactation and survival to weaning. These findings are consistent with terminal investment. Iteroparity did not increase lifetime reproductive success, indicating that terminal investment in the first breeding season at the expense of maternal survival (i.e. semelparity) is likely to be advantageous for females.     

Early-life reproduction is associated with increased mortality risk but enhanced lifetime fitness in pre-industrial humans

The physiology of reproductive senescence in women is well understood, but the drivers of variation in senescence rates are less so. Evolutionary theory predicts that early-life investment in reproduction should be favoured by selection at the cost of reduced survival and faster reproductive senescence. We tested this hypothesis using data collected from preindustrial Finnish church records. Reproductive success increased up to age 25 and was relatively stable until a decline from age 41. Women with higher early-life fecundity (ELF; producing more children before age 25) subsequently had higher mortality risk, but high ELF was not associated with accelerated senescence in annual breeding success. However, women with higher ELF experienced faster senescence in offspring survival. Despite these apparent costs, ELF was under positive selection: individuals with higher ELF had higher lifetime reproductive success. These results are consistent with previous observations in both humans and wild vertebrates that more births and earlier onset of reproduction are associated with reduced survival, and with evolutionary theory predicting trade-offs between early reproduction and later-life survival. The results are particularly significant given recent increases in maternal ages in many societies and the potential consequences for offspring health and fitness.     

Evaluation of reproductive costs for Weddell seals in Erebus Bay, Antarctica

1. Organisms balance current reproduction against future survival and reproduction, which results in life-history trade-offs. These trade-offs are also known as reproductive costs and may represent significant factors shaping life-history strategy for many species. 2. Using multistate mark-resight models and 26 years of mark-resight data (1979-2004), we estimated the costs of reproduction to survival and reproductive probabilities for Weddell seals in Erebus Bay, Antarctica and evaluated whether this species either conformed to the 'prudent parent' reproductive strategy predicted by life-history theory for long-lived mammals or alternatively, incurred costs to survival in order to reproduce in a variable environment (flexible-strategy hypothesis). 3. Results strongly supported the presence of reproductive costs to survival (mean annual survival probability was 0.91 for breeders vs. 0.94 for nonbreeders), a notable difference for a long-lived mammal, demonstrating that investment in reproduction does result in a cost to survival for Weddell seals, contrary to the prudent parent hypothesis. 4. Reproductive costs to subsequent reproductive probabilities were also present for first-time breeders (mean probability of breeding the next year was 31.3% lower for first-time breeders than for experienced breeders), thus supporting our prediction of the influence of breeding experience. 5. We detected substantial annual variation in survival and breeding probabilities. Breeding probabilities were negatively influenced by summer sea-ice extent, whereas weak evidence suggested that survival probabilities were affected more by winter sea-ice extent, and the direction of this effect was negative. However, a model with annual variation unrelated to any of our climate or sea-ice covariates performed best, indicating that further study will be needed to determine the appropriate mechanism or combination of mechanisms underlying this annual variation.     

Changing costs of reproduction: age-based differences in reproductive allocation and escape performance in a livebearing fish

The reproductive value hypothesis predicts that if residual reproductive value declines as a female ages, then young females should allocate less of available energy to current fecundity and more to future reproduction; whereas, older females should allocate more of available energy to current fecundity and less to future reproduction (i.e. survival). We test the prediction that older female Gambusia affinis exhibit higher levels of allocation to reproduction (i.e. fecundity) and consequently experience greater decline in escape performance (survival cost) during pregnancy compared to young females. Old females had relatively larger clutch wet masses and clutch wet mass increased more during pregnancy compared to young females. Correspondingly, old females exhibit a significant decline in escape velocity over the course of pregnancy; whereas young females show no change in escape velocity throughout pregnancy. Old females have higher escape velocities early in pregnancy and their performance only declines to about the level of performance of young females by the end of pregnancy. Thus, although old females exhibit a greater decline in performance they are better able to ameliorate the cost of decreased performance.     

Reproductive versus ecological advantages to larger body size in female snakes, Vipera aspis

Body size can influence an organism's microevolutionary fitness either via ecological factors (ecological selection) or changes in reproductive output (sexual or fecundity selection). Published studies on sexual dimorphism in reptiles have generally focussed on sexual-selective forces on males, under the implicit assumption that the intensity of fecundity selection in females (and hence, overall selection on female body size) is likely to be relatively consistent among lineages. In this paper, we explore the degree to which larger body size enhances ecological attributes (e.g., food intake, growth, survival) and reproductive output (reproductive frequency, litter size, offspring size, offspring viability) in free-ranging female aspic vipers, Vipera aspis . The less-than-annual reproductive frequency of these animals allows us to make a direct comparison between females in years during which they concentrate on "ecological" challenges (especially building energy reserves) versus reproductive challenges (producing a litter). Because female snakes have limited abdominal space to hold the clutch (litter), we expect that fecundity should depend on body size. However, our data show that larger body size had a more consistent effect on ecological attributes (such as feeding rates and "costs of reproduction") than on reproductive output per se. Indeed, total reproductive output was maximised at intermediate body sizes. These results suggest that variation in female body size among and within species (and hence, in the degree of sexual dimorphism) may be driven by the ecological as well as reproductive consequences of body size variation in both sexes.     

Differences in Patterns of Reproductive Allocation between the Sexes in Nicrophorus orbicollis

Organisms are selected to maximize lifetime reproductive success by balancing the costs of current reproduction with costs to future survival and fecundity. Males and females typically face different reproductive costs, which makes comparisons of their reproductive strategies difficult. Burying beetles provide a unique system that allows us to compare the costs of reproduction between the sexes because males and females are capable of raising offspring together or alone and carcass preparation and offspring care represent the majority of reproductive costs for both sexes. Because both sexes perform the same functions of carcass preparation and offspring care, we predict that they would experience similar costs and have similar life history patterns. In this study we assess the cost of reproduction in male Nicrophorus orbicollis and compare to patterns observed in females. We compare the reproductive strategies of single males and females that provided pre- and post-hatching parental care. There is a cost to reproduction for both males and females, but the sexes respond to these costs differently. Females match brood size with carcass size, and thus maximize the lifetime number of offspring on a given size carcass. Males cull proportionately more offspring on all carcass sizes, and thus have a lower lifetime number of offspring compared to females. Females exhibit an adaptive reproductive strategy based on resource availability, but male reproductive strategies are not adaptive in relation to resource availability.     

Modulation of the adrenocortical response to acute stress with respect to brood value, reproductive success and survival in the Eurasian hoopoe

Reproducing parents face the difficult challenge of trading-off investment in current reproduction against presumed future survival and reproduction. Glucocorticoids are supposed to mediate this trade-off because the adrenocortical response to stress disrupts normal reproductive behaviour in favour of self-maintenance and own survival. According to the brood-value hypothesis, individuals with a low survival probability until the next reproductive season have to invest in current reproduction, a process driven by a down-regulation of their adrenocortical response. If the adrenocortical response to stress effectively mediates the trade-off between current reproduction versus future survival and reproduction, we expect a negative relationship with reproductive success and a positive correlation of the adrenocortical stress response with survival. We studied the relationship between corticosterone secretion in parents and their current brood value, reproductive success and survival in a short-lived multi-brooded bird, the Eurasian hoopoe Upupa epops. The adrenocortical response to acute handling stress was correlated with the brood value within the individual (first and second broods of the year) and between individuals. Birds breeding late in the season mounted a lower total corticosterone response to acute stress than birds breeding earlier, while females showed lower levels than males. We observed a negative relationship between the adrenocortical stress response and rearing success or fledging success in females, as predicted by the brood-value hypothesis. However, we could not evidence a clear link between the adrenocortical stress response and survival. Future research testing the brood-value hypothesis and trade-offs between current reproduction and future survival should also measure free corticosterone and carefully differentiate between cross-sectional (i.e. between-individual) and individual-based experimental studies.     

Differential costs of reproduction in females and hermaphrodites in a gynodioecious plant

Background and Aims

Plants exhibit a variety of reproductive systems where unisexual (females or males) morphs coexist with hermaphrodites. The maintenance of dimorphic and polymorphic reproductive systems may be problematic. For example, to coexist with hermaphrodites the females of gynodioecious species have to compensate for the lack of male function. In our study species, Geranium sylvaticum, a perennial gynodioecious herb, the relative seed fitness advantage of females varies significantly between years within populations as well as among populations. Differences in reproductive investment between females and hermaphrodites may lead to differences in future survival, growth and reproductive success, i.e. to differential costs of reproduction. Since females of this species produce more seeds, higher costs of reproduction in females than in hermaphrodites were expected. Due to the higher costs of reproduction, the yearly variation in reproductive output of females might be more pronounced than that of hermaphrodites.

Methods

Using supplemental hand-pollination of females and hermaphrodites of G. sylvaticum we examined if increased reproductive output leads to differential costs of reproduction in terms of survival, probability of flowering, and seed production in the following year.

Key Results

Experimentally increased reproductive output had differential effects on the reproduction of females and hermaphrodites. In hermaphrodites, the probability of flowering decreased significantly in the following year, whereas in females the costs were expressed in terms of decreased future seed production.

Conclusions

When combining the probability of flowering and seed production per plant to estimate the multiplicative change in fitness, female plants showed a 56 % and hermaphrodites showed a 39 % decrease in fitness due to experimentally increased reproduction. Therefore, in total, female plants seem to be more sensitive to the cost of reproduction in terms of seed fitness than hermaphrodites.     

Trade‐offs in evolutionary immunology: just what is the cost of immunity?

It has become increasingly clear that life-history patterns among the vertebrates have been shaped by the plethora and variety of immunological risks associated with parasitic faunas in their environments. Immunological competence could very well be the most important determinant of life-time reproductive success and fitness for many species. It is generally assumed by evolutionary ecologists that providing immunological defences to minimise such risks to the host is costly in terms of necessitating trade-offs with other nutrient-demanding processes such as growth, reproduction, and thermoregulation. Studies devoted to providing assessments of such costs and how they may force evolutionary trade-offs among life-history characters are few, especially for wild vertebrate species, and their results are widely scattered throughout the literature. In this paper we attempt to review this literature to obtain a better understanding of energetic and nutritional costs for maintaining a normal immune system and examine how costly it might be for a host who is forced to up-regulate its immunological defence mechanisms. The significance of these various costs to ecology and life history trade-offs among the vertebrates is explored. It is concluded that sufficient evidence exists to support the primary assumption that immunological defences are costly to the vertebrate host.     

Reproductive Competition Among Males in Multimale Groups of Primates: Modeling the Costs and Effectiveness of Conflict

Multimale groups of primates are characterized by strong reproductive competition among males, generally resulting in an uneven division of male reproductive success (reproductive skew). The observed patterns of conflict and reproductive skew have often been attributed to the so-called tug-of-war model. We show, however, that two important assumptions of this model are not met in male primates. First, the tug-of-war model assumes that reproductive conflict reduces overall group productivity, but in male primates (and most other vertebrates) conflict likely involves mortality rather than fecundity costs. Second, the tug-of-war model does not account for the possibility that male primates can achieve some reproductive success without engagement in open conflict, such as when a single male cannot guard several receptive females at the same time. We therefore develop a dynamic version of the tug-of-war model, in which reproductive competition causes mortality costs, and in which individuals can gain uncontested shares of reproduction dependent on the degree of female receptive overlap. This model differs substantially from the original tug-of-war model, and derives a new and rich set of comparative predictions. For instance, it predicts that the level of conflict among males declines as the queuing success of subordinate males increases (as survival increases), and also, as their uncontested share of reproduction increases, e.g., as female receptive overlap increases. Our model shows how male–male conflict and female receptive overlap collectively determine the level of reproductive skew among male primates, and illustrates that this relationship is more complex than previously thought.     

Heterogeneity in individual quality overrides costs of reproduction in female reindeer

Reproductive allocation at one age is predicted to reduce the probability of surviving to the next year or to lead to a decrease in future reproduction. This prediction assumes that reproduction involves fitness costs. However, few empirical studies have assessed whether such costs may vary with the age at primiparity or might be overridden by heterogeneities in individual quality. We used data from 35 years’ monitoring of individually marked semi-domestic reindeer females to investigate fitness costs of reproduction. Using multi-state statistical models, we compared age-specific survival and reproduction among four reproductive states (never reproduced, experienced non-breeders, reproduced but did not wean offspring, and reproduced and weaned offspring) and among contrasted age at primiparity. We assessed whether reproductive costs occurred, resulting in a trade-off between current reproduction and future reproduction or survival, and whether early maturation was costly or rather reflected differences in individual quality of survival and reproduction capabilities. We did not find any evidence for fitness costs of reproduction in female reindeer. We found no cost of gestation and lactation in terms of future reproduction and survival. Conversely, successful breeders had higher survival and subsequent reproductive success than experienced non-breeders and unsuccessful breeders, independently of the age at primiparity. Moreover, it was beneficial to mature earlier, especially for females that successfully weaned their first offspring. Successful females at early primiparity remained successful throughout their life, clearly supporting the existence of marked among-female differences in quality. The weaning success peaked for multiparous females and was lower for first-time breeders, indicating a positive effect of experience on reproductive performance. Our findings emphasize an overwhelming importance of individual quality and experience to account for observed variation in survival and reproductive patterns of female reindeer that override trade-offs between current reproduction and future performance, at least in the absence of harsh winters.     

Sexual dimorphism and cost of reproduction in the dioecious shrub Lindera benzoin (Lauraceae)>

We examined sexual dimorphism in reproductive allocation and its effects on growth and subsequent reproduction in a natural population of the dioecious woody shrub Lindera benzoin (L.) Blume. In addition to comparing natural patterns of growth and reproduction in a marked population of 251 females and 87 males, we experimentally examined the effect of reduced reproduction on future growth and reproduction in female plants and examined sexual dimorphism in carbon/nutrient balance. Our results suggest that females of L. benzoin bear greater reproductive costs in terms of both biomass and minerals. These costs were measurable in terms of current biomass and allocation of nitrogen to reproduction, as well as subsequent growth, reproduction, and tissue carbon/nutrient balance. Based upon the results of a fruit-thinning experiment and path analysis, fruit production in 1991 appeared to have direct negative effects on fruit production in 1992, an effect that was not necessarily mediated through effects on plant growth. We discuss our results in the context of other intrinsic and extrinsic factors that can influence growth, reproductive costs, and mortality in this species.     

Direct and ecological costs of resistance and tolerance in the stinging nettle

Plant resistance and tolerance to herbivores, parasites, pathogens, and abiotic factors may involve two types of costs. First, resistance and tolerance may be costly in terms of plant fitness. Second, resistance and tolerance to multiple enemies may involve ecological trade-offs. Our study species, the stinging nettle ( Urtica dioica L.) has significant variation among seed families in resistance and tolerance as well as costs of resistance and tolerance to the holoparasitic plant Cuscuta europaea L. Here we report on variation among seed families (i.e. genetic) in tolerance to nutrient limitation and in resistance to both mammalian herbivores (i.e. number of stinging trichomes) and an invertebrate herbivore (i.e. inverse of the performance of a generalist snail, Arianta arbustorum). Our results indicate direct fitness costs of snail resistance in terms of host reproduction whereas we did not detect fitness costs of mammalian resistance or tolerance to nutrient limitation. We further tested for ecological trade-offs among tolerance or resistance to the parasitic plant, herbivore resistance, and tolerance to nutrient limitation in the stinging nettle. Tolerance of nettles to nutrient limitation and resistance to mammalian herbivores tended to correlate negatively. However, there were no significant correlations among resistance and tolerance to the different natural enemies (i.e. parasitic plants, snails, and mammals). The results of this greenhouse study thus suggest that resistance and tolerance of nettles to diverse enemies are free to evolve independently of each other but not completely without direct costs in terms of plant fitness.     

Mating frequency and inclusive fitness in Drosophila melanogaster

In many species, increased mating frequency reduces maternal survival and reproduction. In order to understand the evolution of mating frequency, we need to determine the consequences of increased mating frequency for offspring. We conducted an experiment in Drosophila melanogaster in which we manipulated the mating frequency of mothers and examined the survival and fecundity of the mothers and their daughters. We found that mothers with the highest mating frequency had accelerated mortality and more rapid reproductive senescence. On average, they had 50% shorter lives and 30% lower lifetime reproductive success (LRS) than did mothers with the lowest mating frequency. However, mothers with the highest mating frequency produced daughters with 28% greater LRS. This finding implies that frequent mating stimulates cross-generational fitness trade-offs such that maternal fitness is reduced while offspring fitness is enhanced. We evaluate these results using a demographic metric of inclusive fitness. We show that the costs and benefits of mating frequency depend on the growth rate of the population. In an inclusive fitness context, there was no evidence that increased mating frequency results in fitness costs for mothers. These results indicate that cross-generational fitness trade-offs have an important role in sexual selection and life-history evolution.     

“Costs” of reproduction in reptiles

Summary Many theoretical models of life-history evolution rely on the existence of trade-offs between current fecundity and probable future fecundity and survival. Such costs of reproduction have been demonstrated only rarely. Field and laboratory studies on six species of Australian scincid lizards show that gravid females are more vulnerable to predation than are non-gravid females, primarily because (i) they are physically burdened (running speeds are reduced by 20 to 30%), and (ii) they bask more often (in some species). However, food intake is not reduced in gravid animals. A review of published literature suggests that reproductive trade-offs are widespread among reptiles, but the nature of the reproductive costs may vary widely among related species. Within the range of annual survivorship rates of most lizard species, trade-offs between fecundity and survival are likely to be the main evolutionary determinants of optimal levels of reproductive effort. Trade-offs between fecundity and bodily growth are less likely to be significant.     

Resource availability modulates the effect of body size on reproductive development

Within-species variation in animal body size predicts major differences in life history, for example, in reproductive development, fecundity, and even longevity. Purely from an energetic perspective, large size could entail larger energy reserves, fuelling different life functions, such as reproduction and survival (the “energy reserve” hypothesis). Conversely, larger body size could demand more energy for maintenance, and larger individuals might do worse in reproduction and survival under resource shortage (the “energy demand” hypothesis). Disentangling these alternative hypotheses is difficult because large size often correlates with better resource availability during growth, which could mask direct effects of body size on fitness traits. Here, we used experimental body size manipulation in the freshwater cnidarian Hydra oligactis, coupled with manipulation of resource (food) availability to separate direct effects of body size from resource availability on fitness traits (sexual development time, fecundity, and survival). We found significant interaction between body size and food availability in sexual development time in both males and females, such that large individuals responded less strongly to variation in resource availability. These results are consistent with an energy reserve effect of large size in Hydra. Surprisingly, the response was different in males and females: small and starved females delayed their reproduction, while small and starved males developed reproductive organs faster. In case of fecundity and survival, both size and food availability had significant effects, but we detected no interaction between them. Our observations suggest that in Hydra, small individuals are sensitive to fluctuations in resource availability, but these small individuals are able to adjust their reproductive development to maintain fitness.     

Effect of food restriction on survival and reproduction of a termite

Food availability affects the trade-off between maintenance and reproduction in a wide range of organisms, but its effects on social insects remain poorly understood. In social insects, the maintenance-reproduction trade-off seems to be absent in individuals but may appear at the colony level, although this is rarely investigated. In this study, we restricted food availability in a termite species to test how it affects survival and reproduction, both at the individual and colony level. Using Bayesian multivariate response models, we found very minor effects of food restriction on the survival of queens, individual workers or on the colonies. In contrast, queen fecundity was significantly reduced, whereas colony-level fecundity (i.e., the number of dispersing alates, future reproductives) increased under food restriction as workers gave up cooperation within the colony and became alates that dispersed. Our study shows that life-history trade-offs can be mitigated by individuals' social behaviours in social organisms.