Age-specific Reproductive Success Research Articles

Natal environmental conditions modulate senescence of antler length in roe deer

It is now broadly admitted that female reproductive senescence – a decline in reproductive performance with increasing age – occurs in most species, at least among birds and mammals. Although information is more limited, male reproductive senescence has been regularly inferred from the decline in the size or performance of phenotypic traits that underly male reproductive success, particularly secondary sexual traits. However, the degree to which environmental conditions influence the pattern of senescence in sexual traits remains largely unknown. From the analysis of two long-term studies of populations of European roe deer (Capreolus capreolus) subjected to markedly different environmental contexts in the wild, we tested the hypothesis that harsh natal and/or current conditions should lead to earlier and/or stronger rates of senescence in the length of fully-grown antlers than good natal and/or current conditions. We found evidence of similar patterns of antler length senescence in both populations, with an onset of senescence around 7 years of age and a decrease of length by about 1–1.5 cm per additional year of life from 7 years of age onwards. We found that good early-life conditions delay senescence in antler length in roe deer. Our results also revealed that senescent males seem to be unable to allocate substantially to antler growth, confirming that antler size is, therefore, an honest signal of male individual quality. By modulating age-specific allocation to secondary sexual traits, natal and current conditions could influence female mate choice and male–male competition over mates, and as a result age-specific reproductive success, and should be accounted for when studying the dynamics of sexual selection.

Precipitation during two weeks in spring influences reproductive success of first-year females in the long-lived Natterer's bat.

Bats are characterized by low reproductive rates in contrast with most of other small mammals. This makes their populations vulnerable when inclement environmental conditions such as cold and rainy weather impair the reproductive success of females. The fine-scale effect of weather on bats, however, remains largely unknown. Using a sliding window analysis approach on an 18-year individualized dataset on six Natterer's bat (Myotis nattereri) colonies, we investigated the effect of fine-scale weather conditions on age-specific reproductive success. We found that increased precipitation during a short time window in spring strongly reduced the probability of successful reproduction of first-year (FY) females. Our data suggest that this time window is concomitant with implantation or early pregnancy, before substantial investment into embryo development. In addition, larger FY had higher reproductive success, suggesting that reproduction may be condition dependent in young females. Reproductive success of older females was not affected by either weather or individual parameters. Our results show that changes in precipitation pattern may compromise the reproductive success of FY females. Further studies are needed to better understand the impact of weather conditions on reproductive success in long-lived bats under climate change scenarios.

Variance in lifetime reproductive success of male polar bears

Abstract Despite the important role that population density plays in ecological and evolutionary processes, studies of solitary species that occur at low densities remain scarce. In the context of mating systems, density is expected to influence the ability of males to find and monopolize mates, in turn, influencing variance in lifetime mating/reproductive success and the opportunity for selection. Herein, we investigate variance in male lifetime mating success (LMS), lifetime reproductive success (LRS), and the mating system of a sexually dimorphic carnivore that occurs at low densities, the polar bear (Ursus maritimus). Across 17 cohorts, born from 1975 to 1991, male LMS ranged from 0 to10 mates and LRS from 0 to 14 cubs; 40% of known-age males were not known to have reproduced. The opportunity for sexual selection (Is = 1.66, range = 0.60–4.99) and selection (I = 1.76, range: 0.65–4.89) were low compared to species with similar levels of sexual size dimorphism. Skew in male LRS was also low but significant for most cohorts indicating nonrandom reproductive success. Age-specific reproductive success was biased toward males from 11 to 17 years of age, with variation in fecundity (54%) but not longevity (10%) playing an important role in male reproduction. Our results support a growing body of evidence that suggests that male-biased size dimorphism and polygynous mating systems need not be associated with high variance in male mating and/or reproductive success.

Older mothers produce more successful daughters

Annual reproductive success and senescence patterns vary substantially among individuals in the wild. However, it is still seldom considered that senescence may not only affect an individual but also affect age-specific reproductive success in its offspring, generating transgenerational reproductive senescence. We used long-term data from wild yellow-bellied marmots (Marmota flaviventer) living in two different elevational environments to quantify age-specific reproductive success of daughters born to mothers differing in age. Contrary to prediction, daughters born to older mothers had greater annual reproductive success on average than daughters born to younger mothers, and this translated into greater lifetime reproductive success. However, in the favorable lower elevation environment, daughters born to older mothers also had greater age-specific decreases in annual reproductive success. In the harsher higher elevation environment on the other hand, daughters born to older mothers tended to die before reaching ages at which such senescent decreases could be observed. Our study highlights the importance of incorporating environment-specific transgenerational parent age effects on adult offspring age-specific life-history traits to fully understand the substantial variation observed in senescence patterns in wild populations.

Tall young females get ahead: size-specific fecundity in wild kangaroos suggests a steep trade-off with growth.

When resources are limited, organisms face allocation conflicts. Indeterminate growth creates a persistent conflict with reproduction, as growth may enhance future reproduction, but diverts resources from current reproduction. Little is known about allocation trade-offs in mammals with indeterminate growth. We studied growth and reproduction in adult female eastern grey kangaroos (Macropus giganteus), an iteroparous mammal with indeterminate growth. Allocation trajectories varied with age and size: for 4-year-old females, fecundity increased from 30 to 82% from shortest to average-sized individuals. Older females had high fecundity regardless of size. The smallest females grew 30% more annually than average-sized females, but females that reached average size at an older age had lower growth rates. Environmental conditions affected allocation to size and reproduction. Rainy springs increased fecundity from 61 to 84% for females that had previously reproduced, but rainy winters reduced leg growth. Females in better relative condition grew 40% more than average, whereas most young of females below average relative condition failed to survive to 10months of age. These results highlight an age-specific trade-off between growth and reproduction. Tall young females benefit from a smaller trade-off between somatic growth and early fecundity than shorter females of the same age, but older females appear to favor reproduction over growth regardless of size. Our study highlights how individual heterogeneity determines trade-offs between life-history components. We speculate that cohort effects affect age-specific reproductive success in this long-lived mammal.

Age-specific reproductive success and cost in female Alpine ibex.

In female mammals, reproduction requires high energy expenditure because of gestation and lactation, possibly leading to a fitness cost. Several studies, however, failed to find the expected negative correlation between current and future reproductive success, likely because of individual heterogeneity in reproductive potential. We compared reproductive performance and costs of reproduction for 40 female Alpine ibex in one established population with 29 females translocated from the same population to a new colony. We investigate factors affecting pregnancy, fecundity and overwinter survival of juveniles, after accounting for individual heterogeneity. In both populations, prime-aged females experienced a strong reproductive cost. Senescent females, however, showed no evidence of reproductive costs. The colonizing population showed lower reproductive cost and better age-specific reproductive performance than the established population. We found a general pattern of low age-specific fecundity and reproductive success that was affected by environmental constraints. Age-specific reproductive success was unrelated to longevity. Although about 84% of adult females appeared to conceive, independently of environmental constraints, energy was allocated to reproduction in a highly conservative manner, leading to low age-specific fecundity (only 36 and 21% of prime-aged and senescent females were seen with a kid) but high kid survival (100% to weaning and 92% to 1 year). Our results suggest that females embarked on lactation only if they had a very high probability of raising their offspring. Our study highlights how reproductive performance and costs in this species vary with age and environment, and are the result of a highly conservative reproductive tactic.

Decomposing variation in male reproductive success: age‐specific variances and covariances through extra‐pair and within‐pair reproduction

Age-specific variances and covariances in reproductive success shape the total variance in lifetime reproductive success (LRS), age-specific opportunities for selection, and population demographic variance and effective size. Age-specific (co)variances in reproductive success achieved through different reproductive routes must therefore be quantified to predict population, phenotypic and evolutionary dynamics in age-structured populations. While numerous studies have quantified age-specific variation in mean reproductive success, age-specific variances and covariances in reproductive success, and the contributions of different reproductive routes to these (co)variances, have not been comprehensively quantified in natural populations. We applied 'additive' and 'independent' methods of variance decomposition to complete data describing apparent (social) and realised (genetic) age-specific reproductive success across 11 cohorts of socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia). We thereby quantified age-specific (co)variances in male within-pair and extra-pair reproductive success (WPRS and EPRS) and the contributions of these (co)variances to the total variances in age-specific reproductive success and LRS. 'Additive' decomposition showed that within-age and among-age (co)variances in WPRS across males aged 2-4 years contributed most to the total variance in LRS. Age-specific (co)variances in EPRS contributed relatively little. However, extra-pair reproduction altered age-specific variances in reproductive success relative to the social mating system, and hence altered the relative contributions of age-specific reproductive success to the total variance in LRS. 'Independent' decomposition showed that the (co)variances in age-specific WPRS, EPRS and total reproductive success, and the resulting opportunities for selection, varied substantially across males that survived to each age. Furthermore, extra-pair reproduction increased the variance in age-specific reproductive success relative to the social mating system to a degree that increased across successive age classes. This comprehensive decomposition of the total variances in age-specific reproductive success and LRS into age-specific (co)variances attributable to two reproductive routes showed that within-age and among-age covariances contributed substantially to the total variance and that extra-pair reproduction can alter the (co)variance structure of age-specific reproductive success. Such covariances and impacts should consequently be integrated into theoretical assessments of demographic and evolutionary processes in age-structured populations.

Effects of Age on Female Reproductive Success inDrosophila bipectinata

Female age influence on mating success, courtship activities, mating latency, copulation duration, fecundity, ovarioles number, and wing length has been studied using isofemale lines of Drosophila bipectinata collected at three different localities. It was observed that in all localities, middle-aged D. bipectinata females had significantly greater mating success, showed less rejection responses to courting male, mated faster, copulated longer, and had greater fecundity and ovariole number than young and old-aged females. Further, old-aged females had comparatively less fitness traits than young age females. This research suggests the occurrence of age specific female reproductive success as follows: middle-aged > young > old-aged.

Reproductive improvement and senescence in a long-lived bird

Heterogeneity within a population is a pervasive challenge for studies of individual life-histories. Population-level patterns in age-specific reproductive success can be broken down into relative contributions from selective disappearance, selective appearance of individuals into the study population, and average change in performance for survivors (average ontogenetic development). In this article, we provide an exact decomposition. We apply our formula to data on the reproductive performance of a well characterized population of common terns (Sterna hirundo). We show that improvements with age over most of adult life and senescence at old ages are primarily due to a genuine change in the mean among surviving individuals rather than selective disappearance or selective appearance of individuals. Average ontogenetic development accounts for approximately 87% of the overall age-specific population change.

Age—related reproductive effort in bighorn sheep ewes

The “terminal investment” hypothesis predicts that reproductive effort should increase with age as life expectancy, and therefore residual reproductive potential, decreases. Several studies, however, have found that reproductive success decreases with age because of senescence. We monitored the age-specific reproductive success of individually marked bighorn sheep ewes at Sheep River, Alberta, from 1982 to 2006. Lamb production increased from 2 to 4 y of age, then remained at approximately 88% until age 13 y, when it began to decline. Lamb survival was higher for ewes aged 4 to 12 y than for ewes aged 2 or 3 y. Reproductive senescence began at 13 y of age but was restricted to a decrease in lamb production. There were no differences in lamb survival between prime-aged and older ewes. The onset of reproductive senescence is about 5 y later than the onset of survival senescence. Positive correlations between reproductive success before 9 y of age and longevity, and between reproductive success before and after 9 y of age, suggest that ewes that survived to the onset of reproductive senescence were mostly of high phenotypic quality. Our data provide no clear support for the terminal investment hypothesis. Future tests of this hypothesis should account for individual heterogeneity in phenotypic quality.

Delayed Breeding Affects Lifetime Reproductive Success Differently in Male and Female Green Woodhoopoes

In cooperatively breeding species, many individuals only start breeding long after reaching physiological maturity [1], and this delay is expected to reduce lifetime reproductive success (LRS) [1-3]. Although many studies have investigated how nonbreeding helpers might mitigate the assumed cost of delayed breeding (reviewed in [3]), few have directly quantified the cost itself [4, 5] (but see [6, 7]). Moreover, although life-history tradeoffs frequently influence the sexes in profoundly different ways [8, 9], it has been generally assumed that males and females are similarly affected by a delayed start to breeding [7]. Here, we use 24 years of data to investigate the sex-specific cost of delayed breeding in the cooperatively breeding green woodhoopoe (Phoeniculus purpureus) and show that age at first breeding is related to LRS differently in males and females. As is traditionally expected, males that started to breed earlier in life had greater LRS than those that started later. However, females showed the opposite pattern: Those individuals that started to breed later in life actually had greater LRS than those that started earlier. In both sexes, the association between age at first breeding and LRS was driven by differences in breeding-career length, rather than per-season productivity. We hypothesize that the high mortality rate of young female breeders, and thus their short breeding careers, is related to a reduced ability to deal with the high physiological costs of reproduction in this species. These results demonstrate the importance of considering sex-specific reproductive costs when estimating the payoffs of life-history decisions and bring into question the long-held assumption that delayed breeding is necessarily costly.

TESTING THREE MODELS ON THE ADAPTIVE SIGNIFICANCE OF PROTANDRIC SIMULTANEOUS HERMAPHRODITISM IN A MARINE SHRIMP

Protandric simultaneous hermaphroditism, as reported for shrimps in the genus Lysmata, is a sexual system in which individuals invariably reproduce as males first and later in life as simultaneous hermaphrodites. I tested three models (i.e., sex-dependent energetic costs, sex-dependent mortality rates and sex-dependent time commitments) in an attempt to explain the adaptive value of protandric simultaneous hermaphroditism in the shrimp L. wurdemanni. Specific assumptions and predictions of each model were evaluated using manipulative experiments. In the laboratory, males grew faster than simultaneous hermaphrodites of the same size and age, an indication that the female function incurs higher energetic costs of reproduction than the male function. Also, large SHPs were more successful in monopolizing food than small males. The sex-dependent growth rate and size-dependent resource holding power agree with predictions of the sex-dependent energetic cost model. The time that simultaneous hermaphrodites required for replenishing their sperm reservoirs after mating as males was much shorter (2 days) than the time required to brood one clutch of embryos (11 days). Also, small simultaneous hermaphrodites experienced heavier mortality due to predatory fishes than large ones. The sex-dependent reproductive time commitment and size-dependent mortality agree with predictions of the sex-dependent time commitment model. Conversely, I found no evidence that the sex-dependent mortality model explains protandric simultaneous hermaphroditism in the studied species. In contrast to model predictions, mortality due to predatory fishes suffered by simultaneous hermaphrodites was not greater than that suffered by males of the same body size. In L. wurdemanni, the relationship between sex-specific investment and reproductive success seems to change during ontogeny in a way that is consistent with an adaptive adjustment of sex allocation to improve age-specific reproductive success.

TESTING THREE MODELS ON THE ADAPTIVE SIGNIFICANCE OF PROTANDRIC SIMULTANEOUS HERMAPHRODITISM IN A MARINE SHRIMP

Protandric simultaneous hermaphroditism, as reported for shrimps in the genus Lysmata, is a sexual system in which individuals invariably reproduce as males first and later in life as simultaneous hermaphrodites. I tested three models (i.e., sex-dependent energetic costs, sex-dependent mortality rates and sex-dependent time commitments) in an attempt to explain the adaptive value of protandric simultaneous hermaphroditism in the shrimp L. wurdemanni. Specific assumptions and predictions of each model were evaluated using manipulative experiments. In the laboratory, males grew faster than simultaneous hermaphrodites of the same size and age, an indication that the female function incurs higher energetic costs of reproduction than the male function. Also, large SHPs were more successful in monopolizing food than small males. The sex-dependent growth rate and size-dependent resource holding power agree with predictions of the sex-dependent energetic cost model. The time that simultaneous hermaphrodites required for replenishing their sperm reservoirs after mating as males was much shorter (2 days) than the time required to brood one clutch of embryos (11 days). Also, small simultaneous hermaphrodites experienced heavier mortality due to predatory fishes than large ones. The sex-dependent reproductive time commitment and size-dependent mortality agree with predictions of the sex-dependent time commitment model. Conversely, I found no evidence that the sex-dependent mortality model explains protandric simultaneous hermaphroditism in the studied species. In contrast to model predictions, mortality due to predatory fishes suffered by simultaneous hermaphrodites was not greater than that suffered by males of the same body size. In L. wurdemanni, the relationship between sex-specific investment and reproductive success seems to change during ontogeny in a way that is consistent with an adaptive adjustment of sex allocation to improve age-specific reproductive success.

AGE-SPECIFIC REPRODUCTIVE SUCCESS: EVIDENCE FOR THE SELECTION HYPOTHESIS

Age-specific reproductive success has been demonstrated in many species. Three hypotheses have been raised to explain this general phenomenon: the experience hypothesis based on age-specific reproductive experience, the effort hypothesis based on age-specific reproductive effort, and the selection hypothesis based on progressive disappearance of phenotypes due to variation in individual productivity and survival. We used data from a long-term study of Leach's storm-petrels (Oceanodroma leucorhoa) to present a single test of mutually exclusive predictions about the relationship between early breeding success and longevity. There should be no correlation between early breeding success and longevity under the experience hypothesis, a negative correlation under the effort hypothesis, and a positive correlation under the selection hypothesis. We found a significant (P < 0.0001) positive relationship between success in the first two breeding attempts and longevity in this population of long-lived seabirds, strongly suggesting that low-productivity parents were also less likely to survive early breeding. These data provide some of the strongest support to date for the selection hypothesis.

A longitudinal study of age-specific reproductive output and body condition among male rhesus macaques, Macaca mulatta.

In many mammalian species, male reproductive success appears to climb sharply at young adulthood, form a brief plateau during prime ages, and decline among older animals, a pattern often attributed to reduced physical condition with ageing. However, solid evidence to either substantiate or refute this profile among nonhuman primates is lacking. Here, we combine a decade of genetic analysis of paternity among free-ranging rhesus macaques, Macaca mulatta, with information about body condition in order to evaluate how changes in morphology might govern age-specific reproduction among males. We show that age-specific reproductive success traverses the same life history profile as found in other mammals, but reductions in reproductive output with advanced age were associated with reduced chances of survivorship rather than accompanied by diminished body condition. We demonstrate that variance in male age at onset of reproduction is three times greater than variance in female age at onset of reproduction. We provide the first evidence from primates that age-specific reproductive output among males is not a consequence of age-related changes in body condition, but reflects social and demographic factors.

The benefits of costly signaling: Meriam turtle hunters

Hunting, particularly when it involves large game that is extensively shared, has been suggested to serve as a form of costly signaling by hunters, serving to attract mates and allies or to deter competitors. Empirical evidence presented elsewhere on turtle hunting practiced by Meriam people of Torres Strait, Australia, supports several key predictions of the costly signaling account. Here we present evidence from the same study bearing on another key prediction, that signalers (hunters) gain social and reproductive benefits. Specifically, we find that successful hunters gain social recognition, have an earlier onset of reproduction, achieve higher age-specific reproductive success, and gain higher quality mates, who also achieve above-average reproductive success. Meriam hunters also average more mates (women who bear their offspring) and more co-resident sexual partners than other men, and these partners (but not mates) are significantly younger. Several lines of evidence thus support the idea that hunting is a form of costly signaling in this population. Alternative hypotheses involving reciprocity (from grateful recipients of meat) and direct offspring provisioning by hunters are not consistent with available evidence, but in the absence of experimental manipulation we cannot rule out a role for phenotypic correlation. Copyright 2003.

Experimental evidence of environmental effects on age-specific reproductive success: the importance of resource quality.

Age-specific access to high-quality resources (e.g. territory or nest site) might be an important determinant for improved reproductive performance with increasing age. I experimentally investigated the effects of territory quality versus other age-related improvements in breeding competence (e.g. foraging skills, breeding experience and local knowledge) on age-specific reproductive success. Territory quality (i.e. territory field layer height) was manipulated in year 2 of northern wheatears (Oenanthe oenanthe) that were breeding in the same territory in two consecutive years. Changing territory quality by changing field layer height had a strong effect on within-individual change in the reproductive success of wheatears. This effect was mainly due to a corresponding change in nest predation risk. When territory quality was kept constant (i.e. no between-year change in territory field layer height), within-individual reproductive success did not change between subsequent years. Thus, age-related improvements in foraging skills, breeding experience and local familiarity had no significant effect on within-individual changes in reproductive success. Increased reproductive success with increased age in northern wheatears is therefore mainly explained by an improved access to high-quality territories with increasing age. I conclude that age-dependent access to high-quality breeding resources might be a widespread phenomenon in nature.

Experimental evidence that age-specific reproductive success is independent of environmental effects

An age–specific improvement in reproductive performance has been reported in many iteroparous breeders. However, whether this is a consequence of intrinsic differences in competence amongst age classes or extrinsic differences in the environment they experience is unclear since the timing of breeding within a season generally also differs with age. To disentangle these effects, we experimentally manipulated the timing of breeding in shags, Phalacrocorax aristotelis . Old and young individuals thus reared their chicks at the same time both early and late in the breeding season. When breeding in the same environmental conditions, old pairs performed consistently better than young pairs. These data clearly demonstrate that the age–related differences in reproductive performance are not a result of environmental effects, but rather a consequence of intrinsic differences in brood rearing capacity.

The Effects of Prolonged Fasting of the Body Composition and Reproductive Success of Female Polar Bears (Ursus maritimus)

1. In total, pregnant Polar Bears that enter maternity dens in late summer/autumn may fast for up to 8 months in addition to meeting the nutritional demands of gestation and lactation. We quantified the nutritional costs of this prolonged 'reproductive fast' and examined the effect of variation in maternal body condition on reproductive success. 2. Prior to entering dens, pregnant females were obese, containing as much as 1 kg of fat/kg of lean body mass (LBM). Among bears, LBM increased with body fat mass. This accumulation of LBM may be necessary in order to transport the large fat stores required for fasting, and may also provide a pool of protein essential for reproduction. 3. While fasting, bears lost 43% of body mass. Of the total energy expended on maintenance and reproduction, 93% was drawn from fat stores. This dependency upon fat conforms to the pattern of nutrient metabolism seen among other species adapted to prolonged fasting. Maternal metabolic rate was less than the predicted resting metabolic rate which illustrates the effectiveness of denning as an energy-conserving strategy. 4. Body fat was critically important for reproductive success. In particular, offspring body weight was very strongly related to the size of maternal fat stores before denning. Fatter bears produced heavier cubs which would be more likely to survive. 5. Among bears, pre-denning body condition was positively associated with age. Within the observed range (4-21 years), age-specific reproductive success should thus be highest among older bears. Such an effect could arise if : (1) the body condition of individual bears tends to improve with age and experience or (2) animals of poorer quality and condition die at a younger age.

Age‐Specific Weaning Success of Northern Elephant Seals in Relation to Previous Breeding Experience

We studied the effect of age and previous breeding experience on the probability of successful reproduction in female northern elephant seals (Mirounga angustirostris). Reproductive data, collected over a 12—yr period, were analyzed by multiple logistic regression to describe the functional relationships among the variables. We also examined the relationships among age, experience, date of breeding, and reproductive success to determine if differences in timing explain age—specific productivity. Finally, we investigated the relationship among age, experience, and maternal behavior to determine if correlates of reproductive effort could be related to age— and experience—specific patterns of reproductive success. Reproductive success increased between the maternal ages of 3 and 7 yr and then levelled off, demonstrating an asymptotic relationship. However, the relationship between reproductive success and age, after statistically controlling for previous experience, showed instead that success increased linearly throughout an animal's lifetime. In contrast, after statistically controlling for age, reproductive success was related to experience in a parabolic fashion; success increased with experience for the first few breeding attempts, but declined later in an animal's reproductive lifetime. The effects of experience depended on age: among young animals experience was apparently beneficial, but among old animals greater experience was deleterious. These results suggest experience—related senescence. Timing of breeding was related to experience, rather than age, in a curvilinear fashion; arrival and parturition dates were later for inexperienced and very experienced females, and were earliest for moderately experienced animals. Young animals that gave birth later in the season experienced reduced reproductive success; we observed no such decline in older animals. Thus, among young females, arriving and giving birth earlier each year was adaptive. Aggressiveness and dominance increased with age and experience, but we were unable to separate the effects of age and experience. We contend that the experience—related drop in reproductive success reflects the cost of reproduction. Breeding at a young age and/or continuously appears to result in lower reproductive success later in life. Furthermore, curvature in age—specific reproductive success can be explained by experience—related senescence. This result has general applicability, suggesting that age—related senescence instead may be due to reproductive "burn—out". These results indicate that previous breeding experience and differences in individual quality do not explain the pattern of increasing reproductive success with age in northern elephant seals, and provide indirect support for the hypothesis that animals increase reproductive effort as they age to offset a concomitant decrease in residual reproductive value.