Age-specific resource investment strategies: evidence from female Richardson's ground squirrels (Spermophilus richardsonii)

To avoid a possible cost to their future survival and/or reproduction, individuals must balance their somatic and reproductive investments. The van Noordwijk and De Jong model of resource investment predicts that investments into reproduction and soma can vary among individuals of a population based on the variation in the total amount of energy that individuals acquire. With principal components analysis (PCA), we created two axes of life history for female Richardson's ground squirrels Spermophilus richardsonii : an index of total energy investment (PC1) and an index of investment tactic (PC2). Using these indices, we examined patterns of resource allocation to reproductive and somatic investments. Because yearling female Richardson's ground squirrels complete growth to adult size during pregnancy and early lactation, their somatic needs exceed those of older, fully grown females. Therefore, we predicted that yearlings would show more evidence of a tradeoff between reproductive and somatic investments compared with older females. Both yearling and older females invested four to five times more mass into their litters than into their own body mass. With increasing total investment, yearling females increased investment in both reproduction and themselves, whereas older females invested relatively more in reproduction than themselves. Regardless of age, females that emerged heavier from hibernation invested fewer resources into themselves and more into their litters. Variation in total energy investment and investment tactic indices was similar for yearling and older females. Contrary to our prediction, however, yearling females showed positive associations between reproductive and somatic investments, whereas older females exhibited showed no significant association between reproductive and somatic investments.     

Sexual and vegetative reproduction in the aboveground part of a dioecious clonal plant, <Emphasis Type="Italic">Dioscorea japonica</Emphasis> (Dioscoreaceae)

In dioecious clonal plants, the reproductive effort required to set seeds will be responsible for the larger investment in sexual reproduction by females. If there will be a trade-off in resource allocation between sexual and clonal reproduction, this differential sexual reproduction will lead to sexual differentiation in the relative amount of clonal reproduction. To test this prediction, we studied differences between the sexes in their phenologies and investments in sexual and vegetative reproduction (clonal reproduction by means of bulbils) with respect to ramet size in a dioecious clonal plant, Dioscorea japonica Thunb. The period of bulbil production overlapped the period during which infructescences developed. Females flowered later, produced heavier inflorescences, and fewer flowers per inflorescence than did males. Regression analysis using the size of the individual plants demonstrated that large females made smaller investments in inflorescences and larger investments in sexual reproduction than did large males. In contrast, females invested fewer resources in vegetative reproduction than did males. However, the total investments in sexual and vegetative reproduction did not differ between the sexes. These results supported our hypothesis on the sexual differentiation in sexual and clonal reproduction.     

A test of the reproductive cost hypothesis for sexual size dimorphism in Yarrow's spiny lizard Sceloporus jarrovii

1. Trade-offs between reproduction and growth are central assumptions of life-history theory, but their implications for sexual size dimorphism (SSD) are poorly understood. 2. Adult male Yarrow's spiny lizards Sceloporus jarrovii average 10% larger than adult females. In a low-altitude (1700 m) population, this SSD develops because males grow more quickly than females during the first year of life, particularly during the first female reproductive season. This study tests the hypothesis that SSD develops because female growth is constrained by energetic costs of reproduction. 3. To test for a growth cost of reproduction, I compared growth rates of free-living females that differed, either naturally or experimentally, in reproductive status. Females that naturally delayed reproduction until their second year grew more quickly than females that reproduced as yearlings, and ovariectomized yearlings grew more quickly and to larger sizes than reproductive controls. 4. To determine whether SSD develops in the absence of this inferred reproductive cost, I also studied a high-altitude (2500 m) population in which all females delay reproduction until their second year. Sex differences in growth trajectories were similar to those observed at low altitude, such that males averaged 10% larger than females even prior to female reproduction. 5. Although female growth may be constrained by reproduction, multiple lines of evidence indicate that this cost is insufficient to explain the full magnitude of SSD in S. jarrovii. First, differences in growth of reproductive and nonreproductive females are not observed until the final month of gestation, by which time SSD is already well developed. Second, the growth benefit accruing from experimental inhibition of reproduction accounts for only 32% of the natural sex difference in body size. Finally, SSD develops well in advance of female reproduction in a high-altitude population with delayed maturation.     

Reproductive burden, locomotor performance, and the cost of reproduction in free ranging lizards

Abstract. A reduction in the locomotor capacity of gravid females is considered to be a cost of reproduction if it leads to an increased risk of mortality. In this study, we measured the change in endurance between gravid and postgravid female side-blotched lizards ( Uta stansburiana ) as a test of the cost of reproduction. We also altered reproductive investment in some females by direct ovarian manipulation (yolkectomy), which decreased reproductive burden by 30%. Regardless of experimental treatment, all females had lower endurance when gravid. Endurance was 28% lower in gravid females from the yolkectomy treatment and 31% lower in the unmanipulated females relative to postoviposition females. The experimental reduction in clutch mass resulted in a 21% increase in endurance of gravid yolkectomy females relative to control females. Postovipositional endurance was significantly higher in the yolkectomized females than unmanipulated females, which suggests that the cost of reproduction carries over to postoviposition performance. Unmanipulated females exhibited a significant negative association between endurance and size-specific burden. Endurance was not correlated with clutch size or size-specific burden in the yolkectomy females. Survivorship to the second clutch was higher in the yolkectomy females. The results from a logistic regression showed the probability of survival to the second clutch was significantly and positively associated with endurance after controlling for the effects of treatment. Our analyses demonstrated that the decrement in performance associated with current reproductive investment represents a cost of reproduction expressed as diminished locomotor performance and lowered survivorship to the next clutch.     

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.     

Assessment of costs of reproduction in a pelagic seabird using multistate mark-recapture models

We used a long‐term population band‐resight survey database, a parallel reproduction database, and multistate mark–recapture analysis to assess the costs of reproduction, a keystone concept of life‐history evolution, in Nazca boobies (Sula granti) from Punta Cevallos, Isla Española, Galápagos, Ecuador. We used eight years of resight and breeding data to compare models that included sex‐ and state‐specific survival probabilities and probabilities of transition between reproductive states using multistate mark–recapture models. Models that included state‐specific effects were compared with models lacking such effects to evaluate costs of reproduction. The top model, optimizing the trade‐off of model simplicity and fit to the data using the Akaike Information Criterion (AIC), showed evidence of a temporally varying survival cost of reproduction: nonbreeders showed higher annual survival than breeders did in some years. Because increasing investment among breeders showed no negative association with survival and subsequent breeding success, this evidence indicates a cost to both males and females of initiating, but not of continuing, a reproductive attempt. In some cases, breeders reaching the highest reproductive state (fledging an offspring) showed higher survival or subsequent breeding success than did failed breeders, consistent with differences in overall quality that promote both survival and reproduction. Although a male‐biased adult sex ratio was observed in this population of Nazca boobies, models of state‐ and sex‐specific survival and transition probabilities were not supported, indicating that males and females do not incur different costs of reproduction, and that the observed sex ratio bias is not due to sex‐specific adult mortality.     

Survival costs of reproduction are mediated by parasite infection in wild Soay sheep

A trade‐off between current and future fitness potentially explains variation in life‐history strategies. A proposed mechanism behind this is parasite‐mediated reproductive costs: individuals that allocate more resources to reproduction have fewer to allocate to defence against parasites, reducing future fitness. We examined how reproduction influenced faecal egg counts (FEC) of strongyle nematodes using data collected between 1989 and 2008 from a wild population of Soay sheep in the St. Kilda archipelago, Scotland (741 individuals). Increased reproduction was associated with increased FEC during the lambing season: females that gave birth, and particularly those that weaned a lamb, had higher FEC than females that failed to reproduce. Structural equation modelling revealed future reproductive costs: a positive effect of reproduction on spring FEC and a negative effect on summer body weight were negatively associated with overwinter survival. Overall, we provide evidence that parasite resistance and body weight are important mediators of survival costs of reproduction.     

Costs of reproduction in a tropical invariant-clutch producing lizard (Carlia rubrigularis)

Reproduction involves costs and benefits, whereby increased expenditure into current reproduction can reduce future reproductive success. Costs of reproduction, often assessed using the reduction in locomotor speed, have become well established in temperate-zone lizard species. However, substantial differences in biotic conditions and life-history traits between temperate- and tropical-zone lizards suggest that such costs may be different or of less importance for tropical species. This study examined the effects of reproduction on locomotor speed in the tropical invariant-clutch producing lizard Carlia rubrigularis . Counter to predictions and despite a low relative clutch mass (RCM), gravid and post-oviposition females experienced a reduction in locomotor speed with a physiological basis that was unrelated to the level of reproductive investment. In addition, gravid and postoviposition females exhibited locomotor speeds that were inversely related to the timing of oviposition and approached the speed of non-reproductive females after 3 weeks of oviposition. These results suggest that in addition to RCM, selection may act to reduce the period of recovery in species with extended reproductive seasons and which make numerous bouts of reproduction, such as C. rubrigularis .     

Sexual abstinence and the cost of reproduction in adult male water snakes, Nerodia sipedon

Low frequency of reproduction among iteroparous organisms is most often observed among female ectothermic vertebrates and is thought to be a strategy used to defer reproductive costs. We assessed reproductive costs of male water snakes ( Nerodia sipedon ) to determine why half of adult males abstain from reproduction each year. There was no evidence of a short-term energetic cost of reproduction. Change in mass did not differ between reproductive and non-reproductive males during the one-month mating season or during the entire four-month activity season. Changes in mass of reproductive males were similar at two sites in which the spatial distribution of females differed. However, there were size-specific differences in growth and survival between reproductive and non-reproductive males. Among reproductive males growth rate decreased with body size at a lower rate than among non-reproductive males. Survival increased with body size for reproductive males, but decreased with body size among non-reproductive males. Most of the differential survival between reproductive and non-reproductive males did not occur during the mating season but rather during hibernation. Size-related differences between reproductive and non-reproductive males may reflect selection having eliminated low quality males from the larger size classes. Overall our results appear most consistent with there being high variance in male quality, such that the best males can bear the cost of reproducing and still grow and survive as well or better than low quality males that abstain from reproduction.     

Both sexes pay a cost of reproduction in a frog with biparental care

The assumption that reproduction is costly is central to life‐history theory. Good evidence supporting this premise comes from studies, mostly in short‐lived invertebrates, demonstrating a negative relationship between reproduction and longevity. Whether this trade‐off operates broadly, for example in males and females and in short‐ and long‐lived organisms, remains unresolved. We found a negative relationship between reproduction and days survived in captive, wild‐caught, individuals of a long‐lived poison frog with biparental care (Oophaga pumilio). The proportion of time that individuals spent paired and tadpole production rate were negatively associated with days survived in both sexes, and clutch production was negatively associated with days survived in females. These results broaden the taxonomic base upon which this tenet of life‐history theory is built, empirically confirm that females of this species should be choosy when selecting mates and caring for offspring, and suggest that the costs of ‘limited’ male care in this species deserve re‐evaluation. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 211–218.     

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.     

Significance of spring migration and flexibility in flight-muscle histolysis in waterstriders (Heteroptera, Gerridae)

Abstract. 1. Individuals of long-winged waterstrider (Gerridae) species were found in spring far from their breeding habitats, which indicates that they fly before reproduction.
2. Field samples and laboratory studies show that once they return to their breeding sites, many individuals of three waterstrider species ( Gerris odontogaster (Zett.), Gerris lacustris (L.) and Limnoporus rufoscutellatus (Lat.)) histolyse wing muscles and lose flight ability during their reproductive period.
3. The extent of flight-muscle histolysis varies with environmental factors. Food scarcity affects flight-muscle histolysis in G.odontogaster females. In G.Lacustris , flight-muscle histolysis was more common in the laboratory than in the field samples. Proportionately more females than males lost their flight ability by the end of the reproductive period.
4. Flight ability had direct costs in reproductive potential with (non-flyer) females, which histolysed their flight muscles, laying more eggs than (flyer) females, which maintained flight ability. This was also the case during food scarcity. Non-flyer males of G.odontogaster survived longer than flyer males.
5. Spring migration was distinguished from dispersal during the reproductive period, because these flights serve different functions. Flight-muscle histolysis of females during reproduction is a qualitative reproductive option, with a trade-off between dispersal ability and reproductive potential. Ability to change reproductive behaviour depending on environmental conditions increases an individual's ability to cope with a large variety of habitats.     

The cost of dominance: suppressing subordinate reproduction affects the reproductive success of dominant female banded mongooses

Social species show considerable variation in the extent to which dominant females suppress subordinate reproduction. Much of this variation may be influenced by the cost of active suppression to dominants, who may be selected to balance the need to maximize the resources available for their own offspring against the costs of interfering with subordinate reproduction. To date, the cost of reproductive suppression has received little attention, despite its potential to influence the outcome of conflict over the distribution of reproduction in social species. Here, we investigate possible costs of reproductive suppression in banded mongooses, where dominant females evict subordinates from their groups, thereby inducing subordinate abortion. We show that evicting subordinate females is associated with substantial costs to dominant females: pups born to females who evicted subordinates while pregnant were lighter than those born after undisturbed gestations; pups whose dependent period was disrupted by an eviction attained a lower weight at independence; and the proportion of a litter that survived to independence was reduced if there was an eviction during the dependent period. To our knowledge, this is the first empirical study indicating a possible cost to dominants in attempting to suppress subordinate breeding, and we argue that much of the variation in reproductive skew both within and between social species may be influenced by adaptive variation in the effort invested in suppression by dominants.     

The effect of elevated reproductive effort onhumoral immune function in collared flycatcher females

In order to test whether high reproductive investments impair immune function in naturally breeding collared flycatchers, we performed a brood manipulation experiment and simultaneously induced an immune response by challenging birds with a non-pathogenic antigen – sheep red blood cells (SRBC). Females rearing experimentally enlarged number of nestlings showed significantly lower level of specific anti-SRBC antibodies than control females attending unaltered broods, but only in one of the two study years. The haemoconcentration of leukocytes did not differ between the two groups in both study years. The significant difference in immunological responsiveness between control and enlarged group coincided with differences in survival probability to the next breeding season: females attending enlarged broods showed lower probability of survival than control females, but there was no relationship between the level of immune response and survival probability. Our results indicate that reproduction may indeed trade for resources with immune functions at least in terms of specific antibody production. However, as in the other studies on reproductive costs, these costs seem not always to be pronounced.     

Senescence and costs of reproduction in the life history of a small precocial species

Species following a fast life history are expected to express fitness costs mainly as increased mortality, while slow‐lived species should suffer fertility costs. Because observational studies have limited power to disentangle intrinsic and extrinsic factors influencing senescence, we manipulated reproductive effort experimentally in the cavy (Cavia aperea) which produces extremely precocial young. We created two experimental groups: One was allowed continuous reproduction (CR) and the other intermittent reproduction (IR) by removing males at regular intervals. We predicted that the CR females should senesce (and die) earlier and produce either fewer and/or smaller, slower growing offspring per litter than those of the IR group. CR females had 16% more litters during three years than IR females. CR females increased mass and body condition more steeply and both remained higher until the experiment ended. Female survival showed no group difference. Reproductive senescence in litter size, litter mass, and reproductive effort (litter mass/maternal mass) began after about 600 days and was slightly stronger in CR than IR females. Litter size, litter mass, and offspring survival declined with maternal age and were influenced by seasonality. IR females decreased reproductive effort less during cold seasons and only at higher age than CR females. Nevertheless, offspring winter mortality was higher in IR females. Our results show small costs of reproduction despite high reproductive effort, suggesting that under ad libitum food conditions costs depend largely on internal regulation of allocation decisions.     

Food supply modifies the trade-off between past and future reproduction in a sexual parasite–host system (<Emphasis Type="Italic">Rana esculenta,Rana lessonae</Emphasis>)

Life history theory is concerned with the costs of survival, growth and reproduction under different ecological conditions and the allocation of resources to meet these costs. Typical approaches used to address these topics include manipulation of food resources, followed by measures of subsequent reproductive traits, and measures of the relationship between current and future reproductive investment. Rarely, however, do studies test for the interaction of past investment, present resource availability and future investment simultaneously. Here, we investigate this interaction in females of a sexual parasite–host system consisting of the hybridogenetic frog Rana esculenta (E) and one of its parental species Rana lessonae (L). We kept females from each of two groups (with or without previous reproduction) under two food treatments (low or high) and regularly recorded their growth as well as their body condition and hormone titres as measures of future reproductive condition. After keeping them in hibernation until the following spring, we exposed the females to males, recorded whether they spawned or not and related this response to their condition in the previous autumn. Past reproduction negatively affected growth during summer and condition during autumn which, in turn, reduced the following year’s reproductive output. These costs of previous reproduction were less pronounced under the high than under the low food treatment and lower in R. lessonae than in R. esculenta. Increasing food supply improved reproductive condition more in L than in E females. These species differences in reproductive costs and food requirements provide a mechanistic explanation for why E females skip annual reproduction almost twice as often as L females. Since R. esculenta is a sexual parasite that depends on R. lessonae for successful reproduction, these species-specific life history patterns not only affect individual fitness but also the spatial structure and temporal dynamics of mixed LE populations.     

Reproductive allocation and the long-term costs of reproduction in Siparuna grandiflora, a dioecious neo-tropical shrub

1 Using a combination of observational and experimental approaches, both allocation of resources to reproduction (often called the direct cost of reproduction) and the subsequent long-term costs (the indirect, delayed or demographic cost) associated with reproductive allocation to male and female function in Siparuna grandiflora (Siparunaceae), a tropical dioecious shrub, were examined.
2 The objectives were to determine whether females allocate more biomass or nitrogen per reproductive episode than males, and whether there is a long-term cost of reproduction in terms of subsequent growth or reproduction for either sex. If there is no long-term cost of reproduction, then reproduction may be viewed as free in an evolutionary sense.
3 As is generally the case in dioecious species, females allocated more biomass and nitrogen to reproduction than males. Females also showed delayed costs of reproduction in terms of decreased growth and subsequent reproduction, whereas males did not.
4 The lack of measurable delayed costs in males suggests that with the evolution of dioecy, selection has reduced delayed costs of reproduction in S. grandiflora males. In contrast, females that were prevented from reproducing were able to re-allocate resources to growth, and produced more stem length on average than males. This re-allocation response may have evolved to reduce delayed costs of reproduction in females over time frames longer than that considered in the present study.     

Masting uncoupling: mast seeding does not follow all mast flowering episodes in a dioecious juniper tree

Evolutionary selective forces, like predator satiation and pollination efficiency, are acknowledged to be major causes of masting (the variable, periodic and synchronic production of seeds in a population). However, a number of recent studies indicate that resources might also play an important role on shaping masting patterns. Dioecious masting species offer a privileged framework to study the role of resources on masting variation, since male and female plants often experience different reproductive costs and selective pressures. We followed masting and reproductive investment (RI) of the dioecious tree Juniperus thurifera in two populations along 10 years and studied the different response of males and females to experimentally increased water and nutrient availability in a third population. Juniperus thurifera females invested in reproduction three times more resources than males. Such disparity generated different resource‐use strategies in male and female trees. Tree‐ring growth and water use efficiency (WUE) confirmed that sexes differed in their resource investment temporal pattern, with males using current resources for reproduction and females using resources accumulated during longer periods. Watered and fertilized female trees presented significantly higher flowering reproductive investments than males and experienced an extraordinary mast‐flowering event. However, seeding RI and mast seeding were not affected by the treatment. This suggests that although resource availability affects the reproductive output of this species, there are other major forces regulating masting on J. thurifera. During 10 years, J. thurifera male and female trees presented high and low flowering years more or less synchronously. However, not all mast flowering episodes resulted in mast seeding, leading to masting uncoupling between flowering and seeding. Since flowering costs represent only 1% of females’ total reproductive investments, masting uncoupling could be a beneficial bet‐hedging strategy to maximize reproductive output in spite of unpredictable catastrophic events.     

Reproductive allocation and costs in gynodioecious Leucopogon melaleucoides (Ericaceae): implications for the evolution of gender dimorphism

In dioecious species, females typically allocate more resources to reproduction and incur greater costs of reproduction than males. In gynodioecious species, sex-based differences in reproductive allocation (RA) and costs have been less studied. Such knowledge, however, is relevant to address how females establish and increase in frequency in populations. We examine RA and reproductive costs by comparing fruit set, the proportion of biomass allocated to reproduction, and the responses of fruit set and vegetative growth to shoot defoliation in females and hermaphrodites in gynodioecious Leucopogon melaleucoides. Relative to hermaphrodites, females exhibited a two-fold fruit set advantage. Female fruit set increased proportionately with flower number, but hermaphrodite fruit set was reduced on plants with more flowers. Sex-based differences in allocation to other traits were small. Thus, female RA at flowering was similar to hermaphrodite RA, but was 1.4-fold greater at fruiting. Relative to controls, defoliation reduced fruit set and the percentage of shoots that produced new vegetative growth similarly in both sexes. However, females had a lower proportion of shoots with new growth overall. Further, defoliation on females reduced the dry mass of new growth by 44% compared with controls, whereas hermaphrodites were not affected. These results indicate a trade-off between reproduction and vegetative growth, and greater female costs of reproduction, particularly under resource-limiting conditions. In the absence of compensatory traits to offset higher female reproductive costs, such trade-offs have the potential to retard the spread of females in gynodioecious populations.