Heterogeneity In Individual Quality Research Articles

Reproductive senescence and mating tactic interact and conflict to drive reproductive success in a passerine.

An understanding of the drivers of individual fitness is a fundamental component of evolutionary ecology and life-history theory. Reproductive senescence, mate and mating tactic choice and latent heterogeneity in individual quality interact to affect individual fitness. We sought to disentangle the effects of these fitness drivers, where longitudinal data are required to understand their respective impacts. We used reproductive allocation and success data from a long-term (1989-2018) study of white-throated dippers Cinclus cinclus in Switzerland to simultaneously examine the effects of female and male age, mating tactic, nest initiation date and individual heterogeneity on reproductive performance. We modelled quadratic and categorical effects of age on reproductive parameters. The probability of polygyny increased with age in both sexes before declining in older age classes. Similarly, hatching probability in monogamous pairs and the number of nestlings hatched in both monogamous and polygynous pairs increased with female age before declining later in life. As predicted, offspring survival in monogamous pairs increased with male age before declining in older age classes, but male age had no effect on offspring survival in polygynous nesting attempts. Our results demonstrate that parental age, mating tactic and individual heterogeneity all affect reproductive success, and that the impacts of senescent decline are expressed across different demographic components as a function of sex-specific senescent decline and mating tactic.

Factors affecting lifetime reproduction, long-term territory-specific reproduction, and estimation of habitat quality in northern goshawks

One measure of habitat quality is a species’ demographic performance in a habitat and the gold standard metric of performance is reproduction. Such a measure, however, may be misleading if individual quality is a fitness determinant. We report on factors affecting lifetime reproduction (LR), the total number of lifetime fledglings produced by an individual, and long-term territory-specific reproduction in a multi-generational study of northern goshawks (Accipiter gentilis). LR increased with longer lifespans and more breeding attempts and was strongly correlated with the number of recruits in two filial generations indicating that LR was a good fitness predictor. Extensive differences in LR attested to heterogeneity in individual quality, a requisite for the ideal pre-emptive distribution model (IPD) of habitat settling wherein high quality individuals get the best habitats forcing lower quality individuals into poorer habitats with lower reproduction. In response to 7‒9-year prey abundance cycles, annual frequency of territory occupancy by breeders was highly variable and low overall with monotonic increases in vacancies through low prey years. Occupancy of territories by breeders differed from random; some appeared preferred while others were avoided, producing a right-skewed distribution of total territory-specific fledgling production. However, mean fledglings per nest attempt was only slightly lower in less versus more productive territories, and, contrary to IPD predictions of increases in annual territory-specific coefficients of variation (CV) in reproduction as breeder densities increase, the CV of production decreased as density increased. Rather than habitat quality per se, conspecific attraction elicited territory selection by prospecting goshawks as 70% of settlers comprised turnovers on territories, resulting in occupancy continuity and increased territory-specific reproduction. Top-producing territories had as few as 2 long-lived (high LR) and up to 6 short-lived (low LR) sequential breeders. While individual quality appeared to effect territory-specific heterogeneity in reproductive performance, our data suggests that differences in individual quality may be washed-out by a random settling of prospectors in response to conspecific attraction.

Heterogeneity in individual quality in birds: overall patterns and insights from a study on common terns

While life‐history theory predicts a tradeoff between reproduction and survival, positive covariance, indicative of heterogeneity in individual quality, is often reported among individuals from natural populations. We review longitudinal studies of wild bird populations that test the relationship between annual reproductive success and lifespan and find the majority to report a positive correlation, while none reports a negative correlation. Heterogeneity in individual quality in resource acquisition, masking resource‐based tradeoffs, therefore appears to be common in birds. Considering that there is little evidence for heritable variation in fitness, heterogeneity in individual quality among adults may be due to life‐long effects of developmental conditions. In a 20‐year case study on common terns Sterna hirundo, we test for life‐long effects of cohort quality and within‐cohort nest quality, but find no significant effects on long‐term proxies of quality. Since other studies do find strong life‐long effects of developmental conditions, we suggest that the brood reduction strategy adopted by common terns, causing the majority of offspring to die rapidly after hatching, efficiently reduces variation in offspring quality at independence. As such, a brood reduction strategy may contribute to reduced heterogeneity in adult survival in stochastic environments, both suggested to be more common and adaptive in long‐lived species. Further study is required to assess heterogeneity in individual reproduction, especially in relation to environmental stochasticity and species’ life‐history strategies, in order to assess whether the relative strength of selection in early and late life may indeed affect the magnitude of heterogeneity in individual quality over life, and how this is mediated by parent–offspring conflict.

The interaction between reproductive cost and individual quality is mediated by oceanic conditions in a long-lived bird

Environmental variability, costs of reproduction, and heterogeneity in individual quality are three important sources of the temporal and interindividual variations in vital rates of wild populations. Based on an 18-year monitoring of an endangered, recently described, long-lived seabird, Monteiro's Storm-Petrel (Oceanodroma monteiroi), we designed multistate survival models to separate the effects of the reproductive cost (breeders vs. nonbreeders) and individual quality (successful vs. unsuccessful breeders) in relation to temporally variable demographic and oceanographic properties. The analysis revealed a gradient of individual quality from nonbreeders, to unsuccessful breeders, to successful breeders. The survival rates of unsuccessful breeders (0.90 +/- 0.023, mean +/- SE) tended to decrease in years of high average breeding success and were more sensitive to oceanographic variation than those of both (high-quality) successful breeders (0.97 +/- 0.015) and (low-quality) nonbreeders (0.83 +/- 0.028). Overall, our results indicate that reproductive costs act on individuals of intermediate quality and are mediated by environmental harshness.

Effects of environmental variability and breeding experience on northern elephant seal demography

Demographic rates of animals (i.e., survival and breeding success) generally increase with experience early in life, but temporal variation in the effect of experience on demography is not well understood. The demographic difference between inexperienced versus experienced breeders can be accentuated during poor environmental conditions when food is scarce, or the difference can remain constant regardless of environmental fluctuation. I tested the hypothesis that environmental variation accentuates the difference between inexperienced and experienced breeders using 20 years of capture–mark–recapture data for northern elephant seals (Mirounga angustirostris) from the Farallon Islands, California. I estimated year-specific survival probabilities, breeding propensity (the probability that an individual will breed in year x), and breeding success of primiparous (inexperienced) and multiparous (experienced) females. Primiparous breeders did not suffer more than experienced breeders during years of environmental stress. The selection hypothesis (a decrease in heterogeneity in individual quality within cohorts over time, based on selection pressure) could explain the experience-related improvement in survival and breeding success. Lower variances in survival of multiparous breeders suggest that primiparous adults constitute a more heterogeneous portion of the population, and the 1st breeding event might act as a selective process leading to a more homogeneous pool of multiparous breeders.

To breed or not to breed: a seabird's response to extreme climatic events

Intermittent breeding is an important life-history strategy that has rarely been quantified in the wild and for which drivers remain unclear. It may be the result of a trade-off between survival and reproduction, with individuals skipping breeding when breeding conditions are below a certain threshold. Heterogeneity in individual quality can also lead to heterogeneity in intermittent breeding. We modelled survival, recruitment and breeding probability of the red-footed booby (Sula sula), using a 19 year mark-recapture dataset involving more than 11,000 birds. We showed that skipping breeding was more likely in El-Niño years, correlated with an increase in the local sea surface temperature, supporting the hypothesis that it may be partly an adaptive strategy of birds to face the trade-off between survival and reproduction owing to environmental constraints. We also showed that the age-specific probability of first breeding attempt was synchronized among different age-classes and higher in El-Niño years. This result suggested that pre-breeders may benefit from lowered competition with experienced breeders in years of high skipping probabilities.

Individual quality, early‐life conditions, and reproductive success in contrasted populations of large herbivores

Variations among individuals in phenotypic quality and fitness often confound analyses of life-history strategies assessed at the population level. We used detailed long-term data from three populations of large herbivores with generation times ranging from four to nine years to quantify heterogeneity in individual quality among females, and to assess its influence on mean annual reproductive success over the lifetime (MRS). We also determined how environmental conditions in early life shaped individual quality and tested A. Lomnicki's hypothesis that variance in individual quality should increase when environmental conditions deteriorate. Using multivariate analyses (PCA), we identified one (in sheep and deer) or two (in goats) covariations among life-history traits (longevity, success in the last breeding opportunity, adult mass, and social rank) as indexes of individual quality that positively influenced MRS of females. Individual quality was reduced by unfavorable weather, low resource availability, and high population density in the year of birth. Early-life conditions accounted for 35-55% of variation in individual quality. In roe deer, we found greater variance in individual quality for cohorts born under unfavorable conditions as opposed to favorable ones, but the opposite was found in bighorn sheep and mountain goats. Our results demonstrate that heterogeneity in female quality can originate from environmental conditions in early life and can markedly influence the fitness of females in species located at different positions along the slow-fast continuum of life-history strategies.

Effects of individual quality, reproductive success and environmental variability on survival of a long‐lived seabird

1. Heterogeneity in individual quality (i.e. individuals having different performance levels that are consistent throughout life) can drive the demography of iteroparous species, but quality in the context of environmental variability has rarely been evaluated. 2. We investigated the demographic responses of a long-lived seabird, the Adélie penguin (Pygoscelis adeliae), to contrasting environmental conditions as a function of reproductive success, breeding quality (BQ) and experience. A continuous index of BQ (BQI) was developed to reflect an individual's ability, relative to others, to produce viable offspring. 3. First, we assessed the relative importance of costs of reproduction vs. heterogeneity in quality by comparing survival and reproductive probabilities among deferred, successful and unsuccessful breeders under 'demanding' conditions using multistate capture-mark-recapture modelling. Then, we quantified the influence of BQI on adult survival among experienced breeders vs. the whole study population under both 'normal' and 'demanding' conditions. 4. Higher survival rates were exhibited by successful (74-76%) compared to unsuccessful breeders (64%); the former also more frequently reproduced successfully at year t + 1. 5. From 1997 to 2006, adult survival ranged from 64-79%, with BQI accounting for 91% of variability in the entire study population, but only 17% in experienced breeders. The weakened relationship between BQI and survival in experienced breeders supports the theory that selection during the first reproductive event accounts for a more homogeneous pool of experienced breeders. 6. No significant effect of environmental covariates on survival was evident, suggesting that what appeared to be demanding conditions were within the range that could be buffered by this species. 7. For the first time in seabirds, a quadratic relationship between adult survival and BQI showed that adult survival is shaped by both heterogeneity in quality and reproductive costs. Our study confirms that population demographic patterns are affected by factors at the individuals' level (e.g., individual quality) that are obscured at population-scale levels.

Individual variation in reproductive costs of reproduction: high‐quality females always do better

1. Although life-history theory predicts substantial costs of reproduction, individuals often show positive correlations among life-history traits, rather than trade-offs. The apparent absence of reproductive costs may result from heterogeneity in individual quality. 2. Using detailed longitudinal data from three contrasted ungulate populations (mountain goats, Oreamnos americanus; bighorn sheep, Ovis canadensis; and roe deer, Capreolus capreolus), we assessed how individual quality affects the probability of detecting a cost of current reproduction on future reproduction for females. We used a composite measure of individual quality based on variations in longevity (all species), success in the last breeding opportunity before death (goats and sheep), adult mass (all species), and social rank (goats only). 3. In all species, high-quality females consistently had a higher probability of reproduction, irrespective of previous reproductive status. In mountain goats, we detected a cost of reproduction only after accounting for differences in individual quality. Only low-quality female goats were less likely to reproduce following years of breeding than of nonbreeding. Offspring survival was lower in bighorn ewes following years of successful breeding than after years when no lamb was produced, but only for low-quality females, suggesting that a cost of reproduction only occurred for low-quality females. 4. Because costs of reproduction differ among females, studies of life-history evolution must account for heterogeneity in individual quality.

Survival costs of reproduction vary with age in North American red squirrels

The costs of reproduction are expected to be higher under unfavourable conditions, so that breeding in years of low food supply should have important costs. In addition, the costs of reproduction may be contingent on the age of individuals, and young growing and old senescent individuals should suffer higher costs than the prime-age ones. We tested these predictions by investigating the costs of reproduction as a function of food availability and age in female North American red squirrels using the long-term data on survival and reproduction. We found that the costs of reproduction were independent of food supply, and we did not detect any trade-off between the current and future reproduction. We also did not detect any survival cost of reproduction for the prime-age females, but found evidence for survival costs in yearlings and old (6 years or above) females with successfully breeding individuals having a lower chance of survival compared with unsuccessful or non-breeding ones. These results supported our prediction that the costs of reproduction depended on the age of female red squirrels and were higher in young growing and old senescent individuals. Our study also indicated that, in contrast to large herbivores, heterogeneity in individual quality and viability selection in red squirrels do not affect the study of trade-offs and of the age variation in life-history traits.

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.

Population dynamics in a long‐lived seabird: I. Impact of breeding activity on survival and breeding probability in unbanded king penguins

Understanding the trade-off between current reproductive effort, future survival and future breeding attempts is crucial for demographic analyses and life history studies. We investigated this trade-off in a population of king penguins (Aptenodytes patagonicus) marked individually with transponders using multistate capture-recapture models. This colonial seabird species has a low annual proportion of non-breeders (13%), despite a breeding cycle which lasts over 1 year. To draw inferences about the consequences of non-breeding, we tested for an effect of reproductive activity on survival and on the probability of subsequent breeding. We found that birds non-breeding in year t show the same survival rate as breeders (two-states analysis: breeding and non-breeding). However, breeders had a lower probability of breeding again the following year. This negative phenotypic correlation suggests the existence of reproductive costs affecting future breeding probability, but it might also be strengthened by late arrival for courtship in year t. A three-state analysis including breeding success revealed that failed breeders in year t have a lower probability to reproduce successfully in year t + 1 than non-breeders in year t, providing some evidence for the existence of reproductive costs. Moreover, successful breeders showed higher survival probability. This positive phenotypic correlation between current reproduction and subsequent survival supports the hypothesis of an heterogeneity in individual quality. Males breeding in year t had a lower probability to breed again in year t + 1 than females, suggesting higher reproductive costs for this sex. Such additional costs might be due to higher male parental investment in the final phase of chick-rearing, which also delays the arrival of males in year t + 1, and decreases their breeding probability. Our study is the first to explore the breeding biology and the demography of penguins without the disturbance of flipper-bands.

Stratification based on reproductive state reveals contrasting patterns of age‐related variation in demographic parameters in the kittiwake

Heterogeneity in individual quality can be a major obstacle when interpreting age‐specific variation in life‐history traits. Heterogeneity is likely to lead to within‐generation selection, and patterns observed at the population level may result from the combination of hidden patterns specific to subpopulations. Population‐level patterns are not relevant to hypotheses concerning the evolution of age‐specific reproductive strategies if they differ from patterns at the individual level. We addressed the influence of age and a variable used as a surrogate of quality (yearly reproductive state) on survival and breeding probability in the kittiwake. We found evidence of an effect of age and quality on both demographic parameters. Patterns observed in breeders are consistent with the selection hypothesis, which predicts age‐related increases in survival and traits positively correlated with survival. Our results also reveal unexpected age effects specific to subgroups: the influence of age on survival and future breeding probability is not the same in nonbreeders and breeders. These patterns are observed in higher‐quality breeding habitats, where the influence of extrinsic factors on breeding state is the weakest. Moreover, there is slight evidence of an influence of sex on breeding probability (not on survival), but the same overall pattern is observed in both sexes. Our results support the hypothesis that age‐related variation in demographic parameters observed at the population level is partly shaped by heterogeneity among individuals. They also suggest processes specific to subpopulations. Recent theoretical developments lay emphasis on integration of sources of heterogeneity in optimization models to account for apparently “sub‐optimal” empirical patterns. Incorporation of sources of heterogeneity is also the key to investigation of age‐related reproductive strategies in heterogeneous populations. Thwarting “heterogeneity's ruses” has become a major challenge: for detecting and understanding natural processes, and a constructive confrontation between empirical and theoretical studies.