A dynamic model of size-dependent reproductive effort in a sequential hermaphrodite: a counterexample to Williams's conjecture

In 1966, G. C. Williams showed that for iteroparous organisms, the level of reproductive effort that maximizes fitness is that which balances the marginal gains through current reproduction against the marginal losses to expected future reproduction. When, over an organism's lifetime, the value of future reproduction declines relative to the value of current reproduction, the level of effort allocated to current reproduction should always increase with increasing age. Conversely, when the value of future reproduction increases relative to the value of current reproduction, the level of effort allocated to current reproduction should decrease or remain at zero. While this latter pattern occurs commonly in species that exhibit a delayed age at first reproduction, it may also occur following an initial period of reproduction in some sex-changing organisms that experience a dramatic increase in reproductive potential as they grow larger. Indeed, this schedule of reproductive effort is predicted by models of "early" sex change; however, these models may arrive at this result incidentally because they consider only two reproductive states: on and off. In order to examine the schedule of reproductive effort in greater detail in a system where the potential reproductive rate increases sharply, we adapt the logic and methods of time-dependent dynamic-programming models to develop a size-dependent model of reproductive effort for an example species that experiences a dramatic increase in reproductive potential at large sizes: the bluehead wrasse, Thalassoma bifasciatum. Our model shows that the optimal level of reproductive effort will decline with increasing size or age when increases to the residual reproductive value outpace the increases to current reproductive potential. This result confirms the logic of Williams's analysis of optimal life histories, while offering a realistic counterexample to his conjecture of ever-increasing allocation to current reproduction.     

Female red squirrels fit Williams' hypothesis of increasing reproductive effort with increasing age

Williams predicted that reproductive effort should increase as individuals age and their reproductive value declines. This simple prediction has proven difficult to test because conventional measures of energy expenditure on reproduction may not be a true reflection of reproductive effort. We investigated age-specific variation in female reproductive effort in a stable population of North American red squirrels where energy expenditure on reproduction is likely to reflect actual reproductive effort. We used seven measures of reproductive effort spanning conception to offspring weaning. We found that females completed growth by age 3 and that reproductive value decreased after this age likely because of reproductive and survival senescence. We therefore, predicted that reproductive effort would increase from age 3 onwards. The probability of breeding, litter mass at weaning, and likelihood of territory bequeathal were all lower for 1- and 2-year-old females than for females older than 3 years, the age at which growth is completed. That growing females are faced with additional energetic requirements might account for their lower allocation to reproduction as compared with older females. The probability of attempting a second reproduction within the same breeding season and the propensity to bequeath the territory to juveniles increased from 3 years of age onwards, indicating an increase in reproductive effort with age. We think this increase in reproductive effort is an adaptive response of females to declining reproductive values when ageing, thereby supporting Williams' prediction.     

Divergent life history traits in two closely related species of Simocephalus (Cladocera: Daphnidae) inhabiting lentic environments in Venezuela

We describe life history tactics under laboratory conditions of two species of cladocerans of the genus Simocephalus. The populations live in two habitats with different characteristics. S. acutirostratus was isolated from a small temporary pool without fish. S. latirostris was found in the marginal vegetation of a reservoir with fish. Their life history was monitored for differences in traits such as clutch size, neonate size, age distribution, reproductive effort and adult survival. Our results show that S. acutirostratus (the larger-sized species) grows until it reaches the optimal foraging size and then begins to reproduce, while S. latirostris (the smaller-sized species) starts breeding before reaching the optimal foraging size, allocating energy mainly to reproduction. We explore the possibility that divergences in life history may arise as a response to environmental stress such as that produced by fishes.     

Primates and the evolution of long, slow life histories

Primates are characterized by relatively late ages at first reproduction, long lives and low fertility. Together, these traits define a life-history of reduced reproductive effort. Understanding the optimal allocation of reproductive effort, and specifically reduced reproductive effort, has been one of the key problems motivating the development of life-history theory. Because of their unusual constellation of life-history traits, primates play an important role in the continued development of life-history theory. In this review, I present the evidence for the reduced reproductive effort life histories of primates and discuss the ways that such life-history tactics are understood in contemporary theory. Such tactics are particularly consistent with the predictions of stochastic demographic models, suggesting a key role for environmental variability in the evolution of primate life histories. The tendency for?primates to specialize in high-quality, high-variability food items may make them particularly susceptible to environmental variability and explains their?low reproductive-effort tactics. I discuss recent applications of life-history theory to human evolution and emphasize the continuity between models used to explain peculiarities of human reproduction and senescence with the long, slow life histories of primates more generally.     

Energetics of age-specific reproductive effort in female Harp seals, Phoca groenlandica

The theory of reproductive effort is commonly viewed in the perspective of the cost of offspring to the parent. This interpretation predicts that older females make a greater reproductive effort than younger females, for whom the cost of lost future offspring is less. The benefit early-born offspring represent in future generations is greater than that of late-born offspring in most natural populations, so, alternatively, young females should make a greater reproductive effort. These hypotheses were investigated in nursing Harp seals by examining age-specific reproductive effort in terms of energetic maternal investment.
Younger Harp seal females lost weight at the same rate as did older females. Moreover. since younger, growing females tended to start lactation with less blubber than older females. weight loss during 10 days (d) of lactation represented a greater proportion of stored energy for young females. A successfully weaned pup, therefore, constituted a greater reproductive effort for them than for older females, consistent with benefit–oriented predictions from theory.
A model is presented to outline the components of an annual energy budget for female Harp seals in the context of reproductive effort. This model indicates that young females may devote a greater proportion of their annual net energy to reproduction and take a greater risk of lost future reproduction. It also identifies areas of inadequacy of existing data on pinniped energy budgets.     

Hormonal manipulation of offspring number: maternal effort and reproductive costs

We used exogenous gonadotropin hormones to physiologically enlarge litter size in the bank vole (Clethrionomys glareolus). This method allowed the study design to include possible production costs of reproduction and a trade-off between offspring number and body size at birth. Furthermore, progeny rearing and survival and postpartum survival of the females took place in outdoor enclosures to capture salient naturalistic effects that might be present during the fall and early winter. The aim of the study was to assess the effects of the manipulation on the growth and survival of the offspring and on the reproductive effort, survival, and future fecundity of the mothers. Mean offspring body size was smaller in enlarged litters compared to control litters at weaning, but the differences disappeared by the winter. Differences in litter sizes disappeared before weaning age due to higher mortality in enlarged litters. In addition to the effects of the litter size, offspring performance was probably also influenced by the ability of the mother to support the litter. Experimental females had higher reproductive effort at birth, and they also tended to have higher mortality during nursing. Combined effects of high reproductive effort at birth and high investment in nursing the litter entailed costs for the experimental females in terms of decreased probability of producing a second litter and a decreased body mass gain. Thus, enlarged litter size had both survival and fecundity costs for the mothers. Our results suggest that the evolution of litter size and reproductive effort is determined by reproductive costs for the mothers as well as by a trade-off between offspring number and quality.     

Dynamic influence of maternal and pup traits on maternal care during lactation in an income breeder, the antarctic fur seal

Life-history theory predicts that selection will favor optimal levels of parental effort that balance benefits of current reproduction with costs to survival and future reproduction. The optimal level of effort depends on parental traits, offspring traits, and provisioning strategy. Additionally, how these factors influence effort may differ depending on the stage of reproduction. The relative importance of maternal and offspring traits on energy allocation to offspring was investigated in known-age Antarctic fur seals Arctocephalus gazella across four stages of reproduction, using birth mass and milk-consumption measurements. Maternal traits were important during three of the four stages investigated, with larger females giving birth to larger pups and investing more in pups during perinatal and molt stages. Pup mass influenced maternal effort during the premolt stage, and provisioning strategy influenced postnatal maternal effort at all stages. Energy provided to the offspring during an attendance visit was positively related to the duration of the foraging-trip/visit cycle; however, when investment was controlled for trip/visit cycle duration, the overall rate of energy transfer was similar across trip durations. In addition to strong effects of maternal mass, pup traits affected energy allocation, suggesting that pup demand is important in determining maternal care. These findings emphasize the importance of considering state variables in life-history studies and suggest that timing of measurements of effort in species with long provisioning periods may influence conclusions and our ability to make comparisons of reproductive effort among species.     

Reproductive effort and associated costs in bison (Bison bison): do older mothers try harder?

To examine the prediction that reproductive effort should increasewith age, I compared female bison (Bison bison) of varying agesin terms of maternal behavior, reproductive costs, and the qualityand quantity of offspring. In support of predictions, oldermothers showed more tolerance toward and spent more time nursingtheir calves in months 1–5 than expected based on agedifferences in size and presumed milk production. The two oldestmothers, who died before calving again, appeared to make thegreatest effort. When mothers were barren between calves, whichoccurred more often in older females, their increased investmentenhanced the weight, dominance, maturation rate, and/or fecundityof previous and subsequent offspring. In contrast to predictions,however, offspring quality did not generally increase with maternalage; in fact, primiparae tended to produce larger daughters.Nursing behavior varied little in month 1, when offspring conditionwas apparendy most affected. Young mothers contacted their calvesmore often and tended to graze more during the first month.Reproductive costs appeared greater for young mothers; theirfecundity in years after calving was relatively low. Proportionalweight loss following reproduction decreased with age, althoughchanging growth rates complicate interpretation. The resultssuggest a general decrease in reproductive effort, or at leastin associated costs, during the reproductive life span. Thispattern may be due in part to the increased experience and dominancestatus of older mothers, through which they may avoid some ofthe reproductive costs incurred by primiparae.     

Tradeoff between offspring mass and subsequent reproduction in a highly iteroparous mammal

When resources are limited, current maternal investment should reduce subsequent reproductive success or survival. We used longitudinal data on marked mountain goats Oreamnos americanus to assess if offspring mass at weaning affected maternal survival and future reproduction. Offspring mass was positively correlated with survival of old mothers, suggesting that mothers produced lighter kids, and hence reduced reproductive effort, in their last reproduction. Offspring mass at weaning did not affect survival of young and prime‐aged mothers, but females that had weaned heavy offspring had a reduced probability of subsequent reproduction in years of low population density. Because offspring survival is correlated with weaning mass, mothers’ allocation to reproduction involves a tradeoff between current and future fitness returns. We demonstrate for the first time that allocation to current offspring mass in an iteroparous mammal reduces the probability of subsequent reproduction.     

A dynamic model of food allocation to starling (Sturnus vulgaris) nestlings

We present a dynamic model of food allocation to starling nestlings.Based on the premise that current reproductive activities mayhave detrimental effects on future breeding episodes, the modelis elaborated around the concept of a state variable. In thisimplementation, the state variable represents body mass. A numberof activities can be followed during the breeding season, andwe measured the value of these actions in terms of the contributionof the action to the fitness of the animal at the end of thenestling period. Using the final states reached by parents andyoung, we determined fitness by summing current breeding productionand future reproductive potential. We used backward inductionto find for each combination of states and nestling age thebehavioral options that maximize fitness. Subsequently, forwardsimulations were used to find average trajectories across timeof the following variables: parental and offspring states, foragingtime, and allocation of energy. We also investigated the effectsof brood size and harvest. Physiological parameters, necessaryto translate foraging decisions into body mass changes, aretaken from studies on starlings (Sturnus vulgaris). The resultsappear to closely fit available evidence for this species. Thediscussion relates basic findings of the model to previous resultsof static and deterministic approaches. Limits to the usefulnessof the model are discussed. [Behav Ecol 1991; 2: 21-37]     

Different reproductive tactics in male collared flycatchers signalled by size of secondary sexual character

Most studies of variation in male reproductive tactics have focused on conspicuous categorical differences in mating behaviour (i.e. variation in mating strategies). However, in the presence of trade-offs between investment in competition over matings, parental care and survival, a male''s optimal allocation rule might vary according to his physiological condition and social or ecological environment. Thus, there may also be more subtle variation in male reproductive tactics. Here, I show that the reproductive effort (estimated as residual change in condition) of male collared flycatchers was affected by the size of their forehead patch (a secondary sexual character), age and date of arrival at the breeding grounds. Among early males (i.e. males with a high likelihood of both attracting more than one female and obtaining extra-pair copulations), large-patched males made a relatively large reproductive effort and as a result were in worse condition at the time of feeding offspring as compared to small-patched males. Furthermore, among early breeders, young males and males with experimentally increased forehead patch size made a relatively high effort. By contrast, regardless of age and badge size, there were no such patterns observed among late breeders. These results suggest that collared flycatchers use different reproductive tactics depending on both internal and external factors, and that the size of a secondary sexual trait may not only indicate variation in individual condition but also predict how resources will be allocated between pre- and post-mating reproductive activities.     

Endocrine mediation of vertebrate male alternative reproductive tactics: the next generation of studies

In many species of animals, males may achieve reproductive successvia one of several alternative reproductive tactics. Over thepast decade or so, there has been a concerted effort to investigateendocrine mechanisms that underlie such discrete behavioral(and often morphological) variation. In vertebrates, the firstgeneration of studies focused on potential organizational oractivational effects of steroid hormones (Moore, 1991; Mooreet al., 1998). Some of these studies have made it clear that,in addition to circulating hormone levels, one must also considerother aspects of the endocrine system, including hormone receptors,binding globulins and potential interactions among endocrineaxes. In this paper, I review recent work on endocrine mechanismsand suggest possibilities for future investigation. I highlighthow individual variation in sensitivity to environmental conditions,particularly with respect to various stressors, may accountfor the existence of alternative male reproductive phenotypes.Along these lines, I briefly explain the logic behind our workwith male phenotypes of longear sunfish (Lepomis megalotis)that is aimed at determining the tissue-specific distributionand activity of two enzymes that are common to androgen andglucocorticoid metabolism. A major goal of our work is to examinethe potential role of steroidogenic enzymes in the transductionof environmental information to influence the expression ofalternative male reproductive phenotypes.     

Optimal life‐history schedule in a metapopulation with juvenile dispersal

Previous models have predicted that when mortality increases with age, older individuals should invest more of their resources in reproduction and produce less dispersive offspring, as both their future reproductive value and their prospect of competing with their own sib decline. Those models assumed stable population sizes. We here study for the first time the evolution of age‐specific reproductive effort and of age‐specific offspring dispersal rate in a metapopulation with extinction‐recolonization dynamics and juvenile dispersal. Our model explores the evolutionary consequences of disequilibrium in the age structure of individuals in local populations, generated by disturbances. Life‐history decisions are then shaped both by changes with age in individual performances, and by changes in ecological conditions, as young and old individuals do not live on average in the same environments. Lower juvenile dispersal favours the evolution of higher reproductive effort in young adults in a metapopulation with extinction‐recolonization compared with a well‐mixed population. Contrary to previous predictions for stable structured populations, we find that offspring dispersal should generally increase with maternal age. This is because young individuals, who are overrepresented in recently colonized populations, should allocate more to reproduction and less to dispersal as a strategy to exploit abundant recruitment opportunities in such populations.     

Partitioning of Dry Matter and Mineral Nutrients During a Reproductive Cycle of the Mistletoe Amyema linophyllum (Fenzl.) Tieghem Parasitizing Casuarina obesa Miq.

Budgets for utilization of dry matter, nitrogen and a rangeof mineral elements were constructed for the reproductive season(September 1988–May 1989) of plants of the mistletoe Amyemalinophyllum (Loranthaceae) parasitizing the swamp she oak (Casuarinaobesa Miq.) at Gingin, W. Australia. Shed buds comprised 55%of the allotment of dry matter to reproduction, shed flowers7%, abscised perianths and styles 15%, prematurely shed fruits15%, and successfully ripened fruits a mere 12%. Commitmentto reproductive biomass peaked sharply in October, while thegenerally higher rate of allocation to vegetative biomass declinedfrom beginning to end of the 9-5 month reproductive cycle. Investmentsof dry matter in new leaves and secondary thickening of previousseason's stems were several-fold greater budget items than productionof new stems and shedding of leaves. There was no evidence ofpre-senescence retrieval of N, P, and K from leaves, and concentrationsof Ca, Mg, Na, and Cl increased steadily in dry matter withleaf age. Values for reproductive effort (RE) for dry matterand specific mineral elements were calculated as commitmentto reproduction divided by commitment to reproduction plus vegetativebiomass (? 100). Due to highly differential partitioning ofcertain elements between reproductive and vegetative parts,RE values for minerals for the reproductive season ranged widely,viz. 7% for Ca, 10% for Mn, 15% for Mg, 17% for N, 25% for Kand Zn, 26% for Cu, and 35% for P. The comparable RE for drymatter was 29%. The weight ratio for net intake of nutrientelements from the host by A. linophyllum for the reproductiveseason was 21?5:20?2:6?6:1?6:1 (N:K:Ca:Mg:P), while the meanweight ratio for the concentrations of these elements in xylem(tracheal) sap of the Casuarina host was 13?9:15?6:4?1:30:1,respectively. The data are discussed in relation to the demonstrationof a direct lumen-to-lumen tracheary continuity between hostand mistletoe in mature regions of the haustorial interface. Key words: Mistletoe, resource allocation, mineral nutrition, reproductive effort, host:parasite relationships     

Reproductive Effort and Reproductive Values in Periodic Environments

Life-history theory concerns the optimal spread of reproduction over an organism's life span. In variable environments, there may be extrinsic differences between breeding periods within an organism's life, affecting both offspring and parent and giving rise to intergenerational trade-offs. Such trade-offs are often discussed in terms of reproductive value for parent and offspring. Here, we consider parental life-history optimization in response to varying offspring values of a population regulated by territoriality, where the quality of the environment varies periodically. Periods are interpreted as either within-year (seasonality) or between-years variation (cyclicity). The evolutionarily stable strategy in a general model with two-phased periodicity in the environment can generate either higher or lower effort in the more favorable of the two phases; hence knowing survival prospects of offspring does not suffice for predicting reproductive effort-the future of all descendants and the parent must be tracked. We also apply our method to data on the Ural owl Strix uralensis, a species preying on cyclically fluctuating voles. The observed dynamics are best predicted by assuming delayed reproductive costs and Type II functional response. Accounting for varying offspring values can lead to cases where both reproductive effort and recruitment of offspring are higher in the phase when voles are not maximally abundant, a pattern supported by our data.     

Reproductive strategies in snakes

Snakes of both sexes display remarkable flexibility and diversity in their reproductive tactics. Many features of reproduction in female snakes (such as reproductive mode and frequency, seasonality and multiple mating) allow flexible maternal control. For example, females can manipulate not only the genotypes of their offspring (through mate choice or enhanced sperm competition) but also the phenotypes of their offspring (through allocation 'decisions', behavioural and physiological thermoregulation, and nest-site selection). Reliance on stored energy ('capital') to fuel breeding results in low frequencies of female reproduction and, in extreme cases, semelparity. A sophisticated vomeronasal system not only allows male snakes to locate reproductive females by following scent trails, but also facilitates pheromonally mediated mate choice by males. Male-male rivalry takes diverse forms, including female mimicry and mate guarding; combat bouts impose strong selection for large body size in males of some species. Intraspecific (geographical) variation and phenotypic plasticity in a wide array of reproductive traits (offspring size and number; reproductive frequency; incidence of multiple mating; male tactics such as mate guarding and combat; mate choice criteria) provide exceptional opportunities for future studies.     

Reproductive investment in pre-industrial humans: the consequences of offspring number, gender and survival

The number and gender of offspring produced in a current reproductive event can affect a mother's future reproductive investment and success. I studied the subsequent reproductive outcome of pre-industrial (1752-1850) Finnish mothers producing twins versus singletons of differing gender. I predicted that giving birth to and raising twins instead of singletons, and males instead of females, would incur a greater reproductive effort and, hence, lead to larger future reproductive costs for mothers. I compared the mothers' likelihood of reproducing again in the future, their time to next reproduction and the gender and survival of their next offspring. I found that mothers who produced twins were more likely to stop breeding or breed unsuccessfully in the future as compared with women of a similar age and reproductive history who produced a same-gender singleton child. As predicted, the survival and gender of the offspring produced modified the costs of reproduction for the mothers. Giving birth to and raising males generally appeared to be the most expensive strategy, but this effect was only detected in mothers who produced twins and, thus, suffering from higher overall costs of reproduction.     

Alternative reproductive tactics in snail shell‐brooding cichlids diverge in energy reserve allocation

Life history theory predicts that the amount of resources allocated to reproduction should maximize an individual's lifetime reproductive success. So far, resource allocation in reproduction has been studied mainly in females. Intraspecific variation of endogenous energy storage and utilization patterns of males has received little attention, although these patterns may vary greatly between individuals pursuing alternative reproductive tactics (ARTs). ARTs are characterized by systematic variation of behavioral, physiological, and often morphological traits among same‐sex conspecifics. Some individuals may rely on previously accumulated reserves, because of limited foraging opportunities during reproduction. Others may be able to continue foraging during reproduction, thus relying on reserves to a lesser extent. We therefore predicted that, if male tactics involve such divergent limitations and trade‐offs within a species, ARTs should correspondingly differ in energy reserve allocation and utilization. To test this prediction, we studied short‐term and long‐term reserve storage patterns of males in the shell‐brooding cichlid Lamprologus callipterus. In this species, bourgeois males investing in territory defense, courtship, and guarding of broods coexist with two distinct parasitic male tactics: (1) opportunistic sneaker males attempting to fertilize eggs by releasing sperm into the shell opening when a female is spawning; and (2) specialized dwarf males attempting to enter the shell past the spawning female to fertilize eggs from inside the shell. Sneaker males differed from other male types by showing the highest amount of accumulated short‐term and long‐term fat stores, apparently anticipating their upcoming adoption of the nest male status. In contrast, nest males depleted previously accumulated energy reserves with increasing nest holding period, as they invest heavily into costly reproductive behaviors while not taking up any food. This conforms to a capital breeder strategy. Dwarf males did not accumulate long‐term fat stores at all, which they can afford due to their small behavioral effort during reproduction and their continued feeding activity, conforming to an income breeder strategy. Our data confirm that the resource storage patterns of males pursuing ARTs can diverge substantially, which adds to our understanding of the coexistence and maintenance of alternative reproductive patterns within species.     

Reproductive parasitism of broodcare helpers in a cooperatively breeding fish

Large male helpers in the cooperatively breeding cichlid Neolamprologus pulchergain reproductive success by parasitizing the reproductive effort ofmale territory owners. Under controlled, experimental conditionswe examined the genetic relatedness between the members of broodpairs (n = 14), their male helpers (n = 8), and offspring (n= 292) in seven families. We used multilocus DNA fingerprintingto check for potential reproductive parasitism by male helpersand to assess their fertilization success. Of offspring producedin these families, 10.3% were sired by helpers. In parasitizedbroods, helper fertilization success varied between 12.5% and35.8%. Male helpers parasitized parental reproduction when theirbody size exceeded 4.5 cm standard length (SL), even thoughsexual maturity may be reached much earlier (3.5 cm SL). Twoof three parasitic helpers were punished by severe aggressiveattacks when parasitizing the reproduction of breeders, whichled to their expulsion from the territory. This study demonstratesa potential fitness benefit to broodcare helpers that is oftenneglected. It also points to the delicate balance that may exist betweencooperative and competitive behavior in cooperatively breeding species.