Trade-offs between offspring fitness and future reproduction of adult female black brent

1.?Successful reproduction requires numerous decisions, and some of which may require trade-offs between current and future reproduction. We studied effects of choice of foraging patches on gosling growth and future breeding by mothers in black brent (Branta bernicla nigricans) geese. 2.?Specific foraging areas consistently produced high-quality goslings over 21?years. We found a consistent ranking of gosling mass, corrected for age, across brood rearing areas (BRAs) and years [Akaike model weights, Σw(i) =?1·00 for models including additive effects of BRA and year]. Growth of goslings largely determines their future fitness, so areas where goslings grew most rapidly also produced goslings with the highest mean fitness. 3.?We used a multistate robust design capture-mark-recapture approach to estimate the probability of transitioning from a breeding state to a non-breeding (unobservable) state as a function of quality of BRA. 4.?In the best supported model, transition from a breeding state to a non-breeding state was positively related to gosling growth rates across BRAs. Thus, future reproduction was lower for females using BRAs that produced higher-quality goslings. Our results are consistent with trade-offs by individual brent between fitness of their current offspring and their own reproductive value.     

Individual heterogeneity in fitness in a long‐lived herbivore

Heterogeneity in the intrinsic quality and nutritional condition of individuals affects reproductive success and consequently fitness. Black brant (Branta bernicla nigricans) are long‐lived, migratory, specialist herbivores. Long migratory pathways and short summer breeding seasons constrain the time and energy available for reproduction, thus magnifying life‐history trade‐offs. These constraints, combined with long lifespans and trade‐offs between current and future reproductive value, provide a model system to examine the role of individual heterogeneity in driving life‐history strategies and individual heterogeneity in fitness. We used hierarchical Bayesian models to examine reproductive trade‐offs, modeling the relationships between within‐year measures of reproductive energy allocation and among‐year demographic rates of individual females breeding on the Yukon‐Kuskokwim Delta, Alaska, using capture–recapture and reproductive data from 1988 to 2014. We generally found that annual survival tended to be buffered against variation in reproductive investment, while breeding probability varied considerably over the range of clutch size‐laying date combinations. We provide evidence for relationships between breeding probability and clutch size, breeding probability and nest initiation date, and an interaction between clutch size and initiation date. Average lifetime clutch size also had a weak positive relationship with apparent survival probability. Our results support the use of demographic buffering strategies for black brant. These results also indirectly suggest associations among environmental conditions during growth, fitness, and energy allocation, highlighting the effects of early growth conditions on individual heterogeneity, and subsequently, lifetime reproductive investment.     

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.     

Long-term shifts in the cyclicity of outbreaks of a forest-defoliating insect

Optimisation of reproductive investment is crucial for Darwinian fitness, and detailed long-term studies are especially suited to unravel reproductive allocation strategies. Allocation strategies depend on the timing of resource acquisition, the timing of resource allocation, and trade-offs between different life-history traits. A distinction can be made between capital breeders that fuel reproduction with stored resources and income breeders that use recently acquired resources. In capital breeders, but not in income breeders, energy allocation may be decoupled from energy acquisition. Here, we tested the influence of extrinsic (weather conditions) and intrinsic (female characteristics) factors during energy storage, vitellogenesis and early gestation on reproductive investment, including litter mass, litter size, offspring mass and the litter size and offspring mass trade-off. We used data from a long-term study of the viviparous lizard, Lacerta (Zootoca) vivipara. In terms of extrinsic factors, rainfall during vitellogenesis was positively correlated with litter size and mass, but temperature did not affect reproductive investment. With respect to intrinsic factors, litter size and mass were positively correlated with current body size and postpartum body condition of the previous year, but negatively with parturition date of the previous year. Offspring mass was negatively correlated with litter size, and the strength of this trade-off decreased with the degree of individual variation in resource acquisition, which confirms theoretical predictions. The combined effects of past intrinsic factors and current weather conditions suggest that common lizards combine both recently acquired and stored resources to fuel reproduction. The effect of past energy store points out a trade-off between current and future reproduction.     

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.     

Physiological costs and carry-over effects of avian interspecific brood parasitism influence reproductive tradeoffs

Although models of co-evolution between brood parasites and their hosts primarily focus upon the cost to hosts in the current reproductive bout, the impact of brood parasitism may carry over to future reproductive attempts by altering resource allocation. Glucocorticoid stress hormones help mediate resource allocation to reproduction, yet they have rarely been examined in brood parasitic systems. Here we determined if shifts in parental care and corticosterone had carry-over effects on future reproductive effort in the rufous-and-white wren (Thryophilus rufalbus), a host of the Central American striped cuckoo (Tapera naevia). We found that parasitized parents had significantly higher stress-induced, but not baseline, corticosterone than natural parents during the fledgling stage, which was associated with changes in parental care. The high investment in current reproduction while parasitized may be due to the value of fledged chicks in tropical systems. This maladaptive response by parasitized parents was associated with delayed re-nesting and a reduced likelihood of nesting in the subsequent breeding season. Although a reduction in future reproductive effort can result from a combination of factors, this work suggests that fitness costs of brood parasitism are mediated by changes in corticosterone and parental care behavior that carry over into subsequent breeding seasons.     

Environmental Conditions during Breeding Modify the Strength of Mass-Dependent Carry-Over Effects in a Migratory Bird

In many animals, processes occurring in one season carry over to influence reproductive success and survival in future seasons. The strength of such carry-over effects is unlikely to be uniform across years, yet our understanding of the processes that are capable of modifying their strength remains limited. Here we show that female light-bellied Brent geese with higher body mass prior to spring migration successfully reared more offspring during breeding, but only in years where environmental conditions during breeding were favourable. In years of bad weather during breeding, all birds suffered reduced reproductive output irrespective of pre-migration mass. Our results suggest that the magnitude of reproductive benefits gained by maximising body stores to fuel breeding fluctuates markedly among years in concert with conditions during the breeding season, as does the degree to which carry-over effects are capable of driving variance in reproductive success among individuals. Therefore while carry-over effects have considerable power to drive fitness asymmetries among individuals, our ability to interpret these effects in terms of their implications for population dynamics is dependent on knowledge of fitness determinants occurring in subsequent seasons.      

When to parasitize? A dynamic optimization model of reproductive strategies in a cooperative breeder

We consider a cooperatively breeding group and find the optimal pattern of reproductive parasitism by a subordinate helper as a function of its body size, and hence the share of reproduction obtained by the subordinate. We develop the model for the social system of the cooperatively breeding cichlid fish Neolamprologus pulcher but the general framework is also applicable to other cooperative systems. In addition to behaving cooperatively by sharing tasks, sexually mature male cichlid helpers may directly parasitize the reproduction of dominant breeders in the group. We investigate the relative influence of life history and behavioural variables including growth, parasitism capacity, future reproductive fitness benefits and costs, relatedness and expulsion risk on the optimal reproductive strategy of subordinates. In a detailed analysis of the parameter space we show that a male helper should base its decision to parasitize primarily on an increase in expulsion risk resulting from reproductive parasitism (punishment), intra-group relatedness and the parasitism capacity. If expulsion risk is high then helpers should not parasitize reproduction at medium body size but should parasitize either when small or large.     

Antipredator behavior and the asset-protection principle

Many species of animals face the continual problem of balancingthe trade-off between reducing predation risks and maintainingor increasing their reproductive fitness. The terms of the trade-offare often asymmetric: each separate behavioral decision maylead to only a marginal increase in fitness, but may place theorganism's entire future reproduction in jeopardy. Consequently,the organism's reproductive value is an important componentof most antipredator decision problems. In this paper reproductivevalue is considered as an asset in need of protection. The "asset-protectionprinciple" states that the larger the current reproductive asset,the more important it becomes to protect it. Because reproductivevalue is usually age and condition dependent, optimal antipredatorbehavior also often depends on these variables. I use a uniformmodeling technique (dynamic programming) to address a varietyof issues related to antipredator behavior     

Male feeding contribution facilitates multiple brooding in a biparental songbird

Despite the cost of lost mating opportunities, biparental care is routinely observed across different groups of animals. Theory predicts that paternal care will increase reproductive success, yet many empirical studies have failed to find a direct link. Most studies have focused on the effect of paternal care on current breeding attempts, but male contributions may benefit future reproduction. Species producing clutches or litters more than once per season (i.e. multiple breeding attempts per season) are suitable for investigating whether paternal care contributes to current or future reproductive success, or both. We investigated the importance of the male's feeding contribution to multiple brooding in Japanese Tits Parus minor in northern Japan, where approximately 50% of pairs were known to reproduce multiple times within a breeding season. Male feeding contribution (proportion of provisioning delivered by the male) was positively correlated with the probability of the female multiple brooding and with nestling body mass. However, it was not correlated with fledging success in the current breeding attempt. Our results demonstrate the importance of male parental care for annual reproductive success in this multi‐brooded species and provide insights into the evolution of biparental care.     

Redhead reproductive strategy choices: a dynamic state variable model

Female redhead ducks (Aythya americana) exhibit one of the highest frequenciesof facultative parasitic egg laying, extending reproductive choiceswithin a season beyond nesting only. The occurrence of alternative strategieson a population level within and among years and the factorsthat influence choices are not well documented or understood.We developed a dynamic state variable model to predict reproductivestrategy choice and the influence of female age, body mass,food availability, and host availability on strategy choice.The model predicts a general distribution of strategy choiceby body mass and a strong influence of both age and host availability onstrategy choice. As body mass increases, females choose morecostly reproductive strategies from nonbreeding to parasitizingto nesting to a dual strategy, which is defined as a parasiticallylaid clutch of eggs followed by another clutch laid in the females'own nest. Comparatively, food availability only influenced strategychoice by slightly increasing the use of more costly strategies.Predictions of strategy choice by body mass reflect relationships similarto those proposed by others. Previous studies of the influenceof food availability on observed parasitic frequencies producedmixed and often conflicting results. We propose that femaleredheads are assessing the host environment before making reproductivechoices and food availability functions to fine tune this assessmentby encouraging or discouraging more costly strategies at a lowerbody mass.     

Failures of reproductive suppression in dwarf mongooses (Helogale parvula): accident or adaptation?

In many communally breeding species, only the dominant femalenormally breeds, while subordinates tolerate reproductive suppression(these are "despotic" species, in the terminology of Brown,1987; Macdonald and Moehlman, 1983; Vehrencamp, 1983). Yet inmany species for which reproductive suppression is the norm(across a wide variety of taxa), subordinates do occasionallybreed. Because reproduction by subordinates is atypical forthese species, it is often regarded as simple failure of thenormal mechanisms of suppression. An alternate hypothesis isthat subordinate pregnancies represent an evolutionary compromisebetween dominant and subordinate, in which dominants concedetheir monopoly on reproduction in order to retain helpers. Weuse data from a long-term study of dwarf mongooses (Helogaleparvula) in Serengeti National Park, Tanzania, to test thishypothesis, using an inclusive fitness model adapted from oneby Vehrencamp (1983). We find that the incidence of subordinatepregnancy closely matches that predicted by the model, suggestingthat the mechanisms that underlie reproductive suppression indwarf mongooses are finely adjusted to the social and demographicenvironment. [Behav Ecol 1991; 2: 7–15]     

Twelve fundamental life histories evolving through allocation‐dependent fecundity and survival

An organism's life history is closely interlinked with its allocation of energy between growth and reproduction at different life stages. Theoretical models have established that diminishing returns from reproductive investment promote strategies with simultaneous investment into growth and reproduction (indeterminate growth) over strategies with distinct phases of growth and reproduction (determinate growth). We extend this traditional, binary classification by showing that allocation‐dependent fecundity and mortality rates allow for a large diversity of optimal allocation schedules. By analyzing a model of organisms that allocate energy between growth and reproduction, we find twelve types of optimal allocation schedules, differing qualitatively in how reproductive allocation increases with body mass. These twelve optimal allocation schedules include types with different combinations of continuous and discontinuous increase in reproduction allocation, in which phases of continuous increase can be decelerating or accelerating. We furthermore investigate how this variation influences growth curves and the expected maximum life span and body size. Our study thus reveals new links between eco‐physiological constraints and life‐history evolution and underscores how allocation‐dependent fitness components may underlie biological diversity.     

Do baseline glucocorticoids simultaneously represent fitness and environmental quality in a declining aerial insectivore?

Glucocorticoids (GCs) are often interpreted as indicators of disturbance, habitat quality, and fitness in wild populations. However, since most investigations have been unable to examine habitat variability, GC levels, and fitness simultaneously, such interpretations remain largely unvalidated. We combined a quantification of two habitat types, a manipulation of foraging ability (feather‐clipping just prior to nestling rearing), multiple baseline plasma GC measures, and multi‐year reproductive monitoring to experimentally examine the linkages between habitat quality, GCs, and fitness in female tree swallows Tachycineta bicolor. Control females experiencing the higher early‐season food resources of inland–pasture habitat laid larger clutches, but fledged an equal number but lower mass offspring compared to those in riparian–cropland habitat. Despite these differences in reproductive success, females nesting in the two habitat types did not differ in baseline GC levels at the early‐ or late‐breeding stage. Feather‐clipping reduced provisioning rate in both habitat types. However, baseline GC levels were affected in a habitat‐specific way; only individuals in inland–pasture habitats showed an increase in GCs. Despite this difference in GC levels, the manipulation did not influence offspring mass, reproductive output, adult return rate (a proxy for survival) to the following year, or reproductive success in the subsequent year. Nonetheless, regardless of treatment, individuals with higher GC levels during the late breeding stage returned in the following year with higher GC levels at incubation, indicating a long‐term effect on future GC levels. Our results indicate that environmental changes (e.g. foraging conditions) can have consequences for body condition, behaviour, and current and future baseline GC levels without concomitant influences on fitness, and that differences in fitness components between habitats may not be reflected in baseline GC levels. These results illustrate that baseline GCs may not simultaneously reflect environmental quality and fitness, potentially limiting their application in ecological and conservation settings.     

A state-based model of sperm allocation in a group-breeding salamander

We developed a dynamic program of optimal sperm allocation for group-breeding species. Using the small-mouthed salamander,Ambystoma texanum, as a model organism, we considered how spermatophoredeposition is affected by sperm reserves, male and female numberin breeding aggregations, and time during the breeding season.Parameters for part of the model were based on field data ofbreeding-pond arrival times for both sexes and on laboratoryspermatophore deposition data. Our model included simulationsof three different seasonal patterns of female arrival rate: decreasing (as in A. texanum), increasing, and uniform. General predictions are (1) Increased male competitor numbers at breedingaggregations should cause a reduction in spermatophore allocation.(2) Increased female numbers at breeding aggregations shouldincrease spermatophore allocation. (3) The effect of currentsperm reserve levels on sperm allocation depends on the seasonaldistribution of the mean number of females per male during the breeding season: (3a) If relative female availability decreasesover time, males with low sperm reserves should limit allocationearly in the season but should deposit maximal sperm loadslate in the season; (3b) if female availability increases overtime, males with low sperm loads should limit allocation throughoutthe entire breeding season; and (3c) if female availabilityis constant, sperm reserves are predicted to have little effect on spermatophore allocation tactics. We discuss model predictionsin the context of current sperm allocation theory.     

Experimental evidence of long‐term reproductive costs in a colonial nesting seabird

Trade‐offs between current and future reproduction are central to the evolution of life histories. Experiments that manipulate brood size provide an effective approach to investigating future costs of current reproduction. Most manipulative studies to date, however, have addressed only the short‐term effects of brood size manipulation. Our goal was to determine whether survival or breeding costs of reproduction in a long‐lived species manifest beyond the subsequent breeding season. To this end, we investigated long‐term survival and breeding effects of a multi‐year reproductive cost experiment conducted on black‐legged kittiwakes Rissa tridactyla, a long‐lived colonial nesting seabird. We used multi‐state capture–recapture modeling to assess hypotheses regarding the role of experimentally reduced breeding effort and other factors, including climate phase and colony size and productivity, on future survival and breeding probabilities during the 16‐yr period following the experiment. We found that forced nest failures had a positive effect on breeding probability over time, but had no effect on long‐term survival. This apparent canalization of survival suggests that adult survival is the most important parameter influencing fitness in this long‐lived species, and that adults should pay reproductive costs in ways that do not compromise this critical life history parameter. When declines in adult survival rate are observed, they may indicate populations of conservation concern.     

Temporal variation in fitness payoffs promotes cooperative breeding in long-tailed tits Aegithalos caudatus

Cooperative breeding is paradoxical because some individuals forego independent reproduction and instead help others to reproduce. The ecological constraints model states that such behavior arises because of constraints on independent reproduction. Spatial variation in constraints has been shown to co-vary with the incidence of cooperative breeding in correlational and experimental studies. Here, we examine whether temporally variable ecological constraints can act in a similar way to promote cooperative breeding in the atypical system of long-tailed tits Aegithalos caudatus. In this species, individuals may switch reproductive tactics from breeding to helping within the same breeding season. Using 7 yr of field data, we show that reproductive success declined seasonally because of declines in brood size, nestling weight, and juvenile survival. The survival to breeding age of chicks from nests with helpers was higher than for chicks from nests without helpers, and since helpers usually helped at the nest of a close relative, they accrued inclusive fitness benefits. We used these data to model the expected fitness payoffs of breeding and helping at different times during the season. The model shows that late in the breeding season, the fitness payoff from a kin-directed helping tactic becomes greater than that from independent breeding. The behavioral switch predicted by the model is consistent with the observed switch from breeding to helping, which shows that cooperative breeding may evolve as a way of making the best of a bad job at the end of a temporally constrained breeding season.     

Size‐dependent resource allocation and sex allocation in herbaceous perennial plants

Individuals within a population often differ considerably in size or resource status as a result of environmental variation. In these circumstances natural selection would favour organisms not with a single, genetically determined allocation, but with a genetically determined allocation rule specifying allocation in relation to size or environment. Based on a graphical analysis of a simple evolutionarily stable strategy (ESS) model for herbaceous perennial plants, we aim to determine how cosexual plants within a population should simultaneously adjust their reproductive allocation and sex allocation to their size. We find that if female fitness gain is a linear function of resource investment, then a fixed amount of resources should be allocated to male function, and to post‐breeding survival as well, for individuals above a certain size threshold. The ESS resource allocation to male function, female function, and post‐breeding survival positively correlate if both male and female fitness gains are a saturating function of resource investment. Plants smaller than the size threshold are expected to be either nonreproductive or functionally male only.     

Trade-off between current reproductive effort and delay to next reproduction in the leatherback sea turtle

The trade-off between current and future reproduction plays an important role in demographic analyses. This can be revealed by the relationship between the number of years without reproduction and reproductive investment within a reproductive year. However, estimating both the duration between two successive breeding season and reproductive effort is often limited by variable recapture or resighting effort. Moreover, a supplementary difficulty is raised when nonbreeder individuals are not present sampling breeding grounds, and are therefore unobservable. We used capture–recapture (CR) models to investigate intermittent breeding and reproductive effort to test a putative physiological trade-off in a long-lived species with intermittent breeding, the leatherback sea turtle. We used CR data collected on breeding females on Awa:la-Ya:lima:po beach (French Guiana, South America) from 1995 to 2002. By adding specific constraints in multistate (MS) CR models incorporating several nonobservable states, we modelled the breeding cycle in leatherbacks and then estimated the reproductive effort according to the number of years elapsed since the last nesting season. Using this MS CR framework, the mean survival rate was estimated to 0.91 and the average resighting probability to 0.58 (ranged from 0.30 to 0.99). The breeding cycle was found to be limited to 3 years. These results therefore suggested that animals whose observed breeding intervals are greater than 3 years were most likely animals that escaped detection during their previous nesting season(s). CR data collected in 2001 and 2002 allowed us to compare the individual reproductive effort between females that skipped one breeding season and females that skipped two breeding seasons. These inferences led us to conclude that a trade-off between current and future reproduction exists in leatherbacks nesting in French Guiana, likely linked to the resource provisioning required to invest in reproduction.     

Egg investment in response to helper presence in cooperatively breeding Tibetan ground tits

Life‐history theory predicts a trade‐off between current and future reproduction to maximize lifetime fitness. In cooperatively breeding species, where offspring care is shared between breeders and helpers, helper presence may influence the female breeders’ egg investment, and consequently, survival and future reproductive success. For example, female breeders may reduce egg investment in response to helper presence if this reduction is compensated by helpers during provisioning. Alternatively, female breeders may increase egg investment in response to helper presence if helpers allow the breeders to raise more or higher quality offspring successfully. In the facultatively cooperative‐breeding Tibetan ground tit Pseudopodoces humilis, previous studies found that helpers improve total nestling provisioning rates and fledgling recruitment, but have no apparent effects on the number and body mass of fledglings produced, while breeders with helpers show reduced provisioning rates and higher survival. Here, we investigated whether some of these effects may be explained by female breeders reducing their investment in eggs in response to helper presence. In addition, we investigated whether egg investment is associated with the female breeder's future fitness. Our results showed that helper presence had no effect on the female breeders’ egg investment, and that egg investment was not associated with breeder survival and reproductive success. Our findings suggest that the responses of breeders to helping should be investigated throughout the breeding cycle, because the conclusions regarding the breeders’ adjustment of reproductive investment in response to being helped may depend on which stage of the breeding cycle is considered.