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.     

Reproductive costs of sons and daughters in Rocky Mountain bighorn sheep

Differential maternal investment theory predicts that in sexuallydimorphic and polygynous species mothers should invest morein sons than in daughters. We tested the hypothesis that bighornewes that raise sons incur greater reproductive costs than ewesthat raise daughters. Although ewe mass gain during lactationand subsequent winter body mass loss were independent of lambsex, lambs born the year following the weaning of a son hadlower survival than lambs born after a daughter. The effectsof lamb sex on subsequent reproductive success of ewes becamemore evident at high population density. Lamb sex did not affectmaternal survival. Population density, weather, and ewe agedid not alter the relationship between lamb sex and subsequentreproductive success of the ewe. The year after weaning a son,ewes were more likely to have a daughter than a son, while ewesthat had previously weaned a daughter had similar numbers ofsons and daughters. Our results show that for bighorn sheepewes, sons have a greater life-history cost than daughters,suggesting a differential maternal investment in the sexes.     

Determinants and consequences of age of primiparity in bighorn ewes

Because variation in age of first reproduction can have major effects on individual fitness and population dynamics, it is important to understand what maintains that variability. Although early primiparity is assumed to be costly, it is sometimes associated with high lifetime reproductive success. We used a long‐term study on bighorn sheep Ovis canadensis to determine what variables affect age at first reproduction, investigate the impact of primiparity on body resources and quantify the reproductive performance of primiparous ewes. We then examined the consequences of delayed primiparity on adult body mass, longevity and lifetime reproductive success. Environmental conditions during early development, body mass as a yearling, genotype and maternal effects affected age of primiparity. Primiparous ewes lost more mass in winter and gained less mass in summer than multiparous ewes. Small yearling ewes that postponed reproduction attained similar adult mass than heavy yearling ewes who reproduced at a younger age. Early primiparity did not reduce longevity and was positively associated with lifetime reproductive success. Starting to reproduce as soon as possible appears to maximize fitness of females. When early life conditions are unfavorable, however, delayed primiparity allows greater body growth and likely maximizes survival. The combination of a conservative reproductive strategy and maternal effects on age of primiparity may partly delay population recovery following density‐dependent declines.     

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.     

Mass‐dependent reproductive strategies in wild bighorn ewes: a quantitative genetic approach

In the Ram Mountain bighorn sheep (Ovis canadensis) population, ewes differing by more than 30% in body mass weaned lambs with an average mass difference of only 3%. Variability in adult body mass was partly due to additive genetic effects, but inheritance of weaning mass was weak. Maternal effects could obscure genetic effects in the phenotypic expression of weaning mass, particularly if they reflected strategies of maternal expenditure that varied according to ewe mass. We performed a quantitative genetic analysis to assess genetic and environmental influences on ewe mass and on maternal expenditure. We used the mean daughters/mother regression method and Derivative Free Restricted Maximum Likelihood models to estimate heritability (h²) of ewe mass and indices of maternal expenditure. We found additive genetic effects on phenotypic variation in maternal mass, in lamb mass at weaning (absolute maternal expenditure) and in weaning mass relative to maternal mass at weaning (relative maternal expenditure). Heritability suggests that maternal expenditure has the potential to evolve. The genetic correlation of ewe mass and absolute maternal expenditure was weak, while ewe mass and relative maternal expenditure were strongly negatively correlated. These results suggest additive genetic effects on mass‐dependent reproductive strategies in bighorn ewes. Mass‐dependent reproductive strategies could affect lamb survival and phenotypic variation in adult mass. As population density increased and reproduction became costlier, small females reduced maternal expenditure more than large females. Constraints on reproductive strategy imposed by variations in resource availability are therefore likely to differ according to ewe mass. A general trend for a decrease in maternal expenditure relative to maternal size in mammals suggests that size‐dependent negative maternal effects may be common.     

Condition-dependent reproductive success in bighorn ewes

Individual bighorn ewes ( Ovis canadensis ) at 4–14 years of age were 1.5% heavier preceding years when they weaned a lamb than preceding years when their lamb died before weaning. Intra-individual differences in mass between years of successful and unsuccessful reproduction appeared independent of a ewe's multiyear average mass. Relative mass loss both in the winter before and in the winter after a given repro-ductive episode increased with reproductive success. Long-term monitoring of individual mass and reproductive success is a promising technique to study life histories in capital breeders, because it allows to partially account for differences in reproductive potential.     

Density-dependence vs. density-independence - linking reproductive allocation to population abundance and vegetation greenness

1. Recent studies have shown that optimal reproductive allocation depends on both climatic conditions and population density. We tested this hypothesis using six years of demographic data from eight reindeer (Rangifer tarandus) populations coupled with data on population abundance and vegetation greenness [measured using the Enhanced Vegetation Index (EVI)]. 2. Female spring body mass positively affected summer body mass gain, and lactating females were unable to compensate for harsh winters as efficiently as barren ones. Female spring body mass was highly sensitive to changes in population abundance and vegetation greenness and less dependent on previous autumn body mass and reproductive status. Lactating females were larger than barren females in the spring. Moreover, female autumn body mass was positively related to female autumn body mass and reproductive success and was not very sensitive to changes in vegetation greenness and population abundance. 3. Offspring autumn body mass was positively related to both maternal spring and autumn body mass, and as predicted from theory, offspring were more sensitive to changes in vegetation greenness and population abundance than adult females. A lagged cost of reproduction was present as larger females who were barren, the previous year produced larger offspring than equally sized females that successfully reproduced the previous year. 4. Reproductive success was negatively related to female autumn body mass and positively related to female spring body mass. Moreover, females who successfully reproduced the previous year experienced the highest reproductive success. The fact that negative density-dependence was only present for females that had successfully reproduced the previous year further support the hypothesis that reproduction is costly. 5. This study shows that female reindeer buffer their reproductive allocation according to expected winter conditions and that their buffering abilities were limited by population abundance and a lagged cost of reproduction and enhanced by vegetation greenness.     

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.     

Selection for reproductive rate in Rambouillet sheep: Estimated genetic change in reproductive rate

Rambouillet sheep were selected for high or low reproductive rate based on an index of reproductive rate, reproductive INDEX = dam's total lifetime lambs born/(age in years-1). Selected ewes were first born in 1969. A random bred control line was established from the remaining foundation ewes with the first ewes born in 1973. Genetic variances were estimated with REML procedures for reproductive index and number of lambs born or weaned either per ewe exposed for breeding or per ewe lambing. Heritability of reproductive index was 0.26. Heritability for number of lambs born were 0.11 and 0.12 and for number of lambs weaned were 0.04 and 0.04 per ewe exposed for breeding and per ewe lambing, respectively. Breeding values for the reproductive index were estimated using the full animal model (BLUP) with the complete numerator relationship matrix on reproductive index, with fixed effect of year of birth of ewe and breeding values for number of lambs born or weaned either per ewe exposed for breeding or per ewe lambing, estimated with the fixed effects of year of birth of ewe and age of ewe and the random effect of permanent environmental effect among repeated lambing records. Genetic change was estimated as the regression of breeding value for reproductive index and number of lambs born or weaned either per ewe exposed for breeding or per ewe lambing on year of birth of the ewe. High and low lines both responded to selection for reproductive index as compared to the control line (P<0.01). The high line increased at a rate of b = 0.0134 ± 0.0006 reproductive index units and the low line decreased at a rate of b = − 0.0098 ± 0.0005 reproductive index units per year. Response to selection for reproductive index resulted in b = − 0.0074 ± 0.0007 and b = 0.0163 ± 0.0006 lambs per ewe exposed for breeding, and b = − 0.0041 ± 0.0002 and b = 0.0075 ± 0.0002 lambs weaned per ewe exposed for breeding in the low and high lines, respectively. There was a greater response to selection in the high line compared to the low line. These results indicated that the reproductive index did respond to selection.     

Producing sons reduces lifetime reproductive success of subsequent offspring in pre-industrial Finns

Life-history theory states that reproductive events confer costs upon mothers. Many studies have shown that reproduction causes a decline in maternal condition, survival or success in subsequent reproductive events. However, little attention has been given to the prospect of reproductive costs being passed onto subsequent offspring, despite the fact that parental fitness is a function of the reproductive success of progeny. Here we use pedigree data from a pre-industrial human population to compare offspring life-history traits and lifetime reproductive success (LRS) according to the cost incurred by each individual's mother in the previous reproductive event. Because producing a son versus a daughter has been associated with greater maternal reproductive cost, we hypothesize that individuals born to mothers who previously produced sons will display compromised survival and/or LRS, when compared with those produced following daughters. Controlling for confounding factors such as socio-economic status and ecological conditions, we show that those offspring born after elder brothers have similar survival but lower LRS compared with those born after elder sisters. Our results demonstrate a maternal cost of reproduction manifested in reduced LRS of subsequent offspring. To our knowledge, this is the first time such a long-term intergenerational cost has been shown in a mammal species.     

Determinants and long‐term costs of early reproduction in males of a long‐lived polygynous mammal

In long‐lived polygynous species, male reproductive success is often monopolized by a few mature dominant individuals. Young males are generally too small to be dominant and may employ alternative tactics; however, little is known about the determinants of reproductive success for young males. Understanding the causes and consequences of variability in early reproductive success may be crucial to assess the strength of sexual selection and possible long‐term trade‐offs among life‐history traits. Selective pressures driven by fluctuating environmental conditions may depend on age class. We evaluated the determinants of reproduction in male bighorn sheep (Ovis canadensis) aged 2–4 years using 30 years of individual‐level data. These young males cannot defend estrous ewes and use alternative mating tactics. We also investigated how the age of first detected reproduction was correlated to lifetime reproductive success and longevity. We found that reproductive success of males aged 3 years was positively correlated to body mass, to the proportion of males aged 2–4 years in the competitor pool, and to the number of females available per adult male. These results suggest that reproductive success depends on both competitive ability and population age–sex structure. None of these variables, however, had significant effects on the reproductive success of males aged 2 or 4 years. Known reproduction before the age of five increased lifetime reproductive success but decreased longevity, suggesting a long‐term survival cost of early reproduction. Our analyses reveal that both individual‐level phenotypic and population‐level demographic variables influence reproductive success by young males and provide a rare assessment of fitness trade‐offs in wild polygynous males.     

Age-dependent reproductive costs and the role of breeding skills in the Collared flycatcher

This study addressed whether there are any age‐related differences in reproductive costs. Of especial interest was whether young individuals increased their reproductive effort, and thereby their reproductive cost, as much as older birds when brood size was enlarged. To address these questions, a brood‐size manipulation experiment with reciprocal cross‐fostering of nestlings of young and middle‐aged female Collared flycatchers, Ficedula albicollis, was performed on the Swedish island of Gotland. Nestlings’ body mass, tarsus length and survival were recorded to estimate the parental ability and parental effort of the experimental female birds. Female survival and clutch size were recorded in the following years to estimate reproductive costs. We found that middle‐aged female flycatchers coped better with enlarged broods than younger females or invested more in reproduction. In the following year, young female birds that had raised enlarged broods laid smaller clutches than the females from all the other experimental groups. This result shows that the young female birds pay higher reproductive costs than the middle‐aged females. Both young and middle‐aged female flycatchers seemed to increase their reproductive effort when brood size was increased. However, such an increase resulted in higher reproductive costs for the young females. The difference in reproductive costs between birds of different ages is most likely a result of insufficient breeding skills of the young individuals.     

Effect of PMSG dosage on the reproductive performance of adult ewes and ewe lambs bred at a progestagen-PMSG synchronized estrus

The effect of dose of pregnant mares' serum gonadotropin (PMSG) on the reproductive performance of adult ewes and ewe lambs and lamb survival at birth after treatment with fluorogestone acetate (FGA)-impregnated intravaginal sponges and PMSG (250 IU or 500 IU) to synchronize estrus was evaluated. Ewes were exposed to rams for breeding at the synchronized and subsequent estrous cycles. The flock, comprised of three synthetic strains and two control breeds, was maintained in a controlled environment and exposed to an artificial light regimen which alternated at 4-mo intervals from 16h of light daily to 9h of light daily. Trials were conducted during January, May and September at the end of a 9-h daylength cycle. Adult ewes were bred in May and 8 mo later in January. Ewe lambs were bred in September at 6.5 to 7.5 mo of age. The overall reproductive performance of the adult ewes was similar at the two breedings: fertility approximately 90%, prolificacy approximately 2.7, fecundity approximately 240% and lambs born alive approximately 2.4. Dosage of PMSG had no effect. Reproductive performance of ewe lambs was lower and there was a strain x treatment interaction, suggesting greater variability in response. The results indicate there is no advantage to using a higher dose of PMSG in ewes with a natural relatively high fecundity. Moreover, the use of the artificial photoperiod appears to overcome the natural seasonal variation in reproductive performance.     

Resource-dependent reproductive adjustment and the stability of consumer-resource dynamics

This study explored a consumer-resource model including reproductive and nonreproductive subpopulations of the consumer to consider whether resource-dependent reproductive adjustment by the consumer would stabilize consumer-resource dynamics. The model assumed that decreasing (increasing) resource availability caused reproductive suppression (facilitation), and that the reproductive consumer had a higher mortality rate than the nonreproductive one (i.e., a trade-off between reproduction and survival). The model predicted that the variability would be reduced when the consumer had a strong tendency to suppress reproduction in response to low resource availability or when the cost of reproduction was high, although consumer extinction became more likely. Furthermore, when the consumer-resource dynamics converged to limit cycles, reproductive adjustment enhanced the long-term average of the consumer density. It was also predicted that if reproductive suppression enhanced resource consumption efficiency (i.e., a trade-off between reproduction and foraging), then it would destabilize the system by canceling the stabilizing effect of the reproductive adjustment itself. These results suggest that it is necessary not only to identify the costs of reproduction, but also to quantify the changes in individual-level performances due to reproduction in order to understand the ecological consequences of reproductive adjustment.     

Increasing reproductive rates in tropical sheep by means of embryo transfer

One to three embryos were transferred to three groups each of 12 Kenya Merino ewes to establish if uterine capacity is a limiting factor to reproductive performance in this breed of sheep, in a tropical environment. A fourth group of 12 ewes received three embryos following superovulation. Multiple transfers increased the number of lambs born per pregnant ewe. However, although superovulation significantly (P<0.01) increased endogenous progesterone levels in Group 4 recipient ewes, it did not improve either their conception or lambing rates. Peri- and post-natal losses increased with the number of embryos trnasferred and with the litter size. Consequently, the same number of lambs were weaned per recipient ewe in all four groups. It is concluded that although the uterine capacity of the Kenyan Merino ewes is higher than their natural ovulation rates require, increasing the litter size will not necessarily increase the number of lambs weaned.     

Helper effects on pup lifetime fitness in the cooperatively breeding red wolf (Canis rufus)

The evolutionary maintenance of cooperative breeding systems is thought to be a function of relative costs and benefits to breeders, helpers and juveniles. Beneficial effects of helpers on early-life survivorship and performance have been established in several species, but lifetime fitness benefits and/or costs of being helped remain unclear, particularly for long-lived species. We tested for effects of helpers on early- and late-life traits in a population of reintroduced red wolves (Canis rufus), while controlling for ecological variables such as home-range size and population density. We found that the presence of helpers in family groups was positively correlated with pup mass and survival at low population density, but negatively correlated with mass/size at high density, with no relation to survival. Interestingly, mass/size differences persisted into adulthood for both sexes. While the presence of helpers did not advance age at first reproduction for pups of either sex, females appeared to garner long-term fitness benefits from helpers through later age at last reproduction, longer reproductive lifespan and a greater number of lifetime reproductive events, which translated to higher lifetime reproductive success. In contrast, males with helpers exhibited diminished lifetime reproductive performance. Our findings suggest that while helper presence may have beneficial short-term effects in some ecological contexts, it may also incur long-term sex-dependent costs with critical ramifications for lifetime fitness.     

Fertility in South Australian commercial Merino flocks: sources of reproductive wastage

To identify reasons for low fertility in the Merino in South Australia, we defined the extent and sources of reproductive wastage in flocks of maiden (n=14) and mature age (n=54) Merino ewes managed on 43 properties over 4 year. In a second study, reproductive wastage was examined in a very high ovulating flock of mature age South Australian Merino ewes heterozygous for the FecB gene, mated to lamb in either the autumn or spring. Losses in the latter flock were examined in less detail than the large-scale study, but allowed wastage to be partitioned between pre- and peri/post-natal sources. In the first experiment, reproductive wastage between mating and weaning was estimated at 59.7 potential lambs or ova lost per 100 ewes exposed to rams, representing 42.4% of ova shed. The main source of wastage occurred at lambing (55.6% of total loss), with death of twins a major contributor (35.3% of total loss). Other important sources of wastage were from partial failure of multiple ovulation (PFMO; 20.4% of total loss) and from ewes mating but not lambing (13.2% of total loss). Reproductive wastage did not vary with either age of ewe (maiden versus mature) or season of mating (October-December versus January-March). Mean ovulation rate, estimated as 141 per 100 ewes ovulating (range 100-200), varied with age of ewe (129 versus 144; maiden versus mature) but not with season of mating or year (1990-1991). Values for fertility, fecundity and lamb survival were 90, 127 and 73%, respectively. Fecundity of maiden ewes was lower than that of mature ewes (116 versus 130). Survival of single and twin lambs between birth and tail docking was 83 and 56%, respectively. Net reproductive efficiency, or lambs weaned per 100 ewes exposed to rams, averaged 81 (range 31-122). In the second experiment, mean ovulation rate of FecB Merino ewes was 316 per 100 ewes ovulating, with 242 ova (potential lambs) lost between ovulation and tail docking. This loss was equally shared between pre- and peri/post-natal sources (123 versus 119), and demonstrates severe limitation of the Merino to successfully bear and rear multiple litters. We concluded that future research in commercial Merino flocks be focused on lamb mortality, particularly of twins, and on PFMO, the major source of embryo loss.     

Reproductive performance in female common hamsters

We monitored individual reproductive timing and output in a common hamster population in Vienna over a 3-year period. Animals were live-trapped, weighed, individually marked, and reproductive status was determined at capture. Costs of reproduction were investigated by measuring body condition shortly before hibernation and overwinter survival. Our results indicated that early emerging females had more litters and weaned more offspring per season. Body mass throughout the active season did not differ significantly between females with high and low reproductive output. High reproductive output seemed to affect the duration of the active season. Successful females had a longer postreproduction period before hibernation than less successful ones, probably serving to balance the costs of reproductive effort by extended preparation for hibernation. Also, females that had emerged early in spring and had high reproductive success were more likely to survive the subsequent winter. Hence, we found female common hamsters to vary strongly in maternal investment capacity and to tailor reproductive strategies accordingly.     

Early development, adult mass, and reproductive success in bighorn sheep

Despite considerable empirical and theoretical work on the individualand population consequences of early development, little isknown about the correlations between early mass and adult sizeor lifetime reproductive success of free-ranging mammals. Usinga 26-year study of bighorn sheep (Ovis canadensis), we examinedhow mass as a lamb and mass gain as a yearling affected adultmass for both sexes, horn length of males and lifetime reproductivesuccess of females at different population densities. Mass asa 3-week-old lamb was either weakly or not correlated withadult mass, horn length of adult males, or the number of lambsweaned over a ewe's lifetime. Weaning mass was correlated withmost of these variables when the number of ewes in the populationwas taken into account. When weaning mass was controlled throughpartial correlation, mass as a yearling was correlated with adult mass of ewes but not with ewe reproductive success orwith adult mass or horn length of rams. Lamb mass and numberof ewes explained more of the variance in adult characteristicsfor males than for females. Our results suggest that mass gainduring lactation, possibly but not necessarily related to theamount of maternal care received, affects adult mass and reproductive success. Females appear better able than males to compensatefor poor early development, likely by postponing their firstreproduction. Mass gain over several years and the number ofewes in the population strongly affect adult mass of both sexesand therefore can have profound effects on reproductive successof this long-lived species with a multi-year growth period.     

Determinants of reproductive success in female Columbian ground squirrels

Summary We studied the reproductive success of female Columbian ground squirrels (Spermophilus columbianus) in southwestern Alberta for nine years. We defined reproductive success as the number of offspring surviving their first hibernation, classified as yearlings. The number of weaned juveniles explained one third of the variance in number of yearlings at emergence from their first hibernation the following spring, and much of the variance in individual reproductive success originated after weaning. Weight of adult females at emergence from hibernation was correlated with annual reproductive success. The mother's survival beyond weaning and the subsequent winter's snow accumulation had positive effects on annual reproductive success, whereas population density and summer temperature had negative effects. We found no effects on annual reproductive success of date of litter emergence, weight at emergence as a yearling, presence or absence of adult kin, distance from the natal site, location within the study area, winter temperature or summer precipitation. Age of first breeding did not affect lifetime reproductive success, which ranged from 0 to 19 yearlings produced over a lifetime. The greatest source of variation in lifetime reproductive success for females surviving to breeding age was offspring survival, followed by reproductive lifespan.