Hormonal manipulation of offspring number: maternal effort and reproductive costs

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

Mating does not influence reproductive investment, in a viviparous lizard

Mating is crucial for females that reproduce exclusively sexually and should influence their investment into reproduction. Although reproductive adjustments in response to mate quality have been tested in a wide range of species, the effect of exposure to males and mating per se has seldom been studied. Compensatory mechanisms against the absence of mating may evolve more frequently in viviparous females, which pay higher direct costs of reproduction, due to gestation, than oviparous females. To test the existence of such mechanisms in a viviparous species, we experimentally manipulated the mating opportunity of viviparous female lizard, Lacerta (Zootoca) vivipara. We assessed the effect of mating on ovulation, postpartum body condition and parturition date, as well as on changes in locomotor performances and body temperatures during the breeding cycle. Female lizards ovulated spontaneously and mating had no influence on litter size, locomotor impairment or on selected body temperature. However, offspring production induced a more pronounced locomotor impairment and physical burden than the production of undeveloped eggs. Postpartum body condition and parturition dates were not different among females. This result suggests that gestation length is not determined by an embryonic signal. In the common lizard, viviparity is not associated with facultative ovulation and a control of litter size after ovulation, in response to the absence of mating.     

Senescence and costs of reproduction in the life history of a small precocial species

Species following a fast life history are expected to express fitness costs mainly as increased mortality, while slow‐lived species should suffer fertility costs. Because observational studies have limited power to disentangle intrinsic and extrinsic factors influencing senescence, we manipulated reproductive effort experimentally in the cavy (Cavia aperea) which produces extremely precocial young. We created two experimental groups: One was allowed continuous reproduction (CR) and the other intermittent reproduction (IR) by removing males at regular intervals. We predicted that the CR females should senesce (and die) earlier and produce either fewer and/or smaller, slower growing offspring per litter than those of the IR group. CR females had 16% more litters during three years than IR females. CR females increased mass and body condition more steeply and both remained higher until the experiment ended. Female survival showed no group difference. Reproductive senescence in litter size, litter mass, and reproductive effort (litter mass/maternal mass) began after about 600 days and was slightly stronger in CR than IR females. Litter size, litter mass, and offspring survival declined with maternal age and were influenced by seasonality. IR females decreased reproductive effort less during cold seasons and only at higher age than CR females. Nevertheless, offspring winter mortality was higher in IR females. Our results show small costs of reproduction despite high reproductive effort, suggesting that under ad libitum food conditions costs depend largely on internal regulation of allocation decisions.     

Food restriction affects maternal investment but not neonate phenotypes in a viviparous lizard

Food availability significantly affects an animal's energy metabolism,and thus its phenotype,survival,and reproduction.Maternal and offspring responses to food conditions are critical for understanding population dynamics and life-history evolution of a species.In this study,we conducted food manipulation experiments in field enclosures to identify the effect of food restriction on female reproductive traits and postpartum body condition,as well as on hatchling phenotypes,in a lacertid viviparous lizard from the Inner Mongolian desert steppe of China.Females under low-food availability treatment (LFT) had poorer immune function and body condition compared with those under high-food availability treatment (HFT).The food availability treatments significantly affected the litter size and litter mass of the females,but not their gestation period in captivity or brood success,or the body size,sprint speed,and sex ratio of the neonates.Females from the LFT group had smaller litter sizes and,therefore,lower litter mass than those from the HFT group.These results suggest that female racerunners facing food restriction lay fewer offspring with unchanged body size and locomotor performance,and incur a cost in the form of poor postpartum body condition and immune function.The flexibility of maternal responses to variable food availability represents an important life strategy that could enhance the resistance of lizards to unpredictable environmental change.     

Maternal investment during pregnancy in wild meerkats

Maternal investment in offspring development is a major determinant of the survival and future reproductive success of both the mother and her young. Mothers might therefore be expected to adjust their investment according to ecological conditions in order to maximise their lifetime fitness. In cooperatively breeding species, where helpers assist breeders with offspring care, the size of the group may also influence maternal investment strategies because the costs of reproduction are shared between breeders and helpers. Here, we use longitudinal records of body mass and life history traits from a wild population of meerkats (Suricata suricatta) to explore the pattern of growth in pregnant females and investigate how the rate of growth varies with characteristics of the litter, environmental conditions, maternal traits and group size. Gestational growth was slight during the first half of pregnancy but was marked and linear from the midpoint of gestation until birth. The rate of gestational growth in the second half of pregnancy increased with litter size, maternal age and body mass, and was higher for litters conceived during the peak of the breeding season when it is hot and wet. Gestational growth rate was lower in larger groups, especially when litter size was small. These results suggest that there are ecological and physiological constraints on gestational growth in meerkats, and that females may also be able to strategically adjust their prenatal investment in offspring according to the likely fitness costs and benefits of a particular breeding attempt. Mothers in larger groups may benefit from reducing their investment because having more helpers might allow them to lower reproductive costs without decreasing breeding success.     

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.     

Determinants of reproductive success in female adders,Vipera berus

Summary Female lifetime reproductive success in a small population of individually-marked adders in southern Sweden was studied over a period of seven years. Reproductive characteristics varied little from year to year and were consistent through time in individual females. Most females mature at four years of age and reproduce every two years. The total number of offspring produced by a female depends on her adult body size (and thus, litter size) and longevity (and thus, number of litters per lifetime). Adult body size in females is influenced mainly by subadult growth rates. Offspring size depends on maternal body size and a tradeoff between offspring size and offspring number. Maternal age does not affect litter sizes and offspring sizes except through ontogenetic changes in maternal body size.Survival of females after parturition is low because of the high energy costs of reproduction, compounded by low feeding rates of gravid females because of their sedentary behaviour at this time. About one-half of females produce only a single litter during their lifetimes, although some females live to produce four or five litters. On a proximate basis, rates of energy accumulation for growth (in subadults) and reproduction (in adults) may be the most important determinants of fitness in female adders.     

The cost of reproduction induced by body size at birth and breeding density

Body size at birth has implications for the quality of individuals throughout their life. Although large body size is generally considered an advantage, the relationship between body size at birth and long-term fitness is often complicated. Under spatial or temporal variation in environmental conditions, such as the seasonally changing densities of Fennoscandian vole populations, selection should favor variation in offspring phenotypes, as different qualities may be beneficial in different conditions. We performed an experiment in which a novel hormonal manipulation method was used to increase phenotypic variance in body size at birth in the bank vole (Myodes glareolus). The effects of body size on the future fitness of young males and females were then studied at varying population densities in outdoor enclosures. Our results show that small body size at birth and high breeding density increase the survival costs of reproduction. However, there was no interaction between the effects of body size and density on survival, which suggests that the fitness effects of body size were strong enough to persist under environmental variation. Moreover, litter size and the probability of breeding were more sensitive to variation in breeding density than offspring size. Therefore, it is unlikely that individual fitness could be optimized by adjusting offspring body size to the prevailing population density through adaptive maternal effects. Our results highlight the significance of the costs of reproduction in the evolution of life-history traits, and give strong experimental support for the long-term fitness effects of body size at birth.     

Reproductive effort and costs of reproduction in female European ground squirrels

Reproductive effort, factors affecting reproductive output and costs of reproduction were studied in primiparous yearling compared to multiparous older female European ground squirrels (Spermophilus citellus). Yearling females weaned smaller litters than older ones. Litter size increased with posthibernation body mass at the expense of slightly lighter young for yearling but not for older mothers. In older females, on the other hand, emergence body mass influenced offspring mass, whereas litter size was affected by oestrus date. High reproductive effort entailed reproductive costs in terms of reduced subsequent fecundity but not subsequent survival for both yearling and older females. The production of large litters and long duration of lactation delayed subsequent oestrus, which, in turn, correlated negatively with litter size. During the second half of lactation, oestradiol levels were significantly elevated, indicating the initiation of follicular maturation processes. Oestradiol levels during that time correlated negatively with current, but positively with subsequent litter size. We therefore assume that inhibitory effects of lactation on gonadal development may mediate the negative relationship between reproductive effort and subsequent reproductive timing in adults. This effect is absent in yearlings because they are reproducing for the first time. Reproductive output in yearlings was influenced by interactions between structural growth and puberty. Received: 22 March 1999 / Accepted: 7 June 1999     

Increasing returns in the life history of Columbian ground squirrels

1. We examined positive associations and trade-offs of maternal and reproductive traits in a population of Columbian ground squirrels, Spermophilus columbianus .
2. Structural size, body condition, mother's personal allocation to body mass during reproduction, and timing of littering were estimated for live-trapped reproductive females that were observed during an 8-year period, and were compared to litter mass, litter size, and average pup mass using path analyses.
3. Mothers exhibited age-structured traits that influenced reproductive patterns. Yearling mothers were significantly smaller, bred later, and had smaller litters than older females. Mothers that gained more body mass during reproduction and older mothers in good body condition that were structurally large had larger litters.
4. Early seasonal timing of littering was an important positive influence on successful reproduction by older mothers only in early breeding seasons and in years when conditions for reproduction were good for all females.
5. The number of offspring that survived to 1 year of age was most strongly associated with litter mass and litter size; date of breeding was of secondary influence, with earlier litters exhibiting greater success.
6. In general, mothers that gained the most in body mass during reproduction were concurrently more successful in weaning large litters (perhaps due to better quality of foraging habitat).
7. In addition to expected reproductive trade-offs, reproduction by Columbian ground squirrels exhibited positive associations of life-history traits that may reflect evolutionary increasing returns.     

Survival costs of reproduction predict age-dependent variation in maternal investment

Life-history theory predicts that older females will increase reproductive effort through increased fecundity. Unless offspring survival is density dependent or female size constrains offspring size, theory does not predict variation in offspring size. However, empirical data suggest that females of differing age or condition produce offspring of different sizes. We used a dynamic state-variable model to determine when variable offspring sizes can be explained by an interaction between female age, female state and survival costs of reproduction. We found that when costs depend on fecundity, young females with surplus state increase offspring size and reduce number to minimize fitness penalties. When costs depend on total reproductive effort, only older females increase offspring size. Young females produce small offspring, because decreasing offspring size is less expensive than number, as fitness from offspring investment is nonlinear. Finally, allocation patterns are relatively stable when older females are better at acquiring food and are therefore in better condition. Our approach revealed an interaction between female state, age and survival costs, providing a novel explanation for observed variation in reproductive traits.     

Reproductive versus ecological advantages to larger body size in female snakes, Vipera aspis

Body size can influence an organism's microevolutionary fitness either via ecological factors (ecological selection) or changes in reproductive output (sexual or fecundity selection). Published studies on sexual dimorphism in reptiles have generally focussed on sexual-selective forces on males, under the implicit assumption that the intensity of fecundity selection in females (and hence, overall selection on female body size) is likely to be relatively consistent among lineages. In this paper, we explore the degree to which larger body size enhances ecological attributes (e.g., food intake, growth, survival) and reproductive output (reproductive frequency, litter size, offspring size, offspring viability) in free-ranging female aspic vipers, Vipera aspis . The less-than-annual reproductive frequency of these animals allows us to make a direct comparison between females in years during which they concentrate on "ecological" challenges (especially building energy reserves) versus reproductive challenges (producing a litter). Because female snakes have limited abdominal space to hold the clutch (litter), we expect that fecundity should depend on body size. However, our data show that larger body size had a more consistent effect on ecological attributes (such as feeding rates and "costs of reproduction") than on reproductive output per se. Indeed, total reproductive output was maximised at intermediate body sizes. These results suggest that variation in female body size among and within species (and hence, in the degree of sexual dimorphism) may be driven by the ecological as well as reproductive consequences of body size variation in both sexes.     

Energy versus risk: costs of reproduction in free‐ranging pythons in tropical Australia

Abstract Data from a 12‐year field study have allowed us to quantify ‘costs of reproduction’ in a natural population of water pythons (Liasis fuscus) in tropical Australia. Both sexes of pythons cease feeding during the reproductive season. For males, this involves fasting for a 6 week period. Adult males lose weight rapidly over this period (approximately 17% of their body mass) but regain condition in the following months, and do not experience reduced survival. In contrast, reproductive adult females cease feeding for 3 months, lose an average of 44% of their body mass over this period, and experience increased mortality. A causal link between reproductive output and reduced female survival is supported by (i) a decrease in survival rates at female maturation; (ii) a correlation between survival rates and frequency of reproduction, in a comparison among different size classes of adult pythons; and (iii) a lowered survival rate for females that allocated more energy to reproduction. Hence, both sexes experience substantial energy costs of reproduction, but a relatively higher energy cost translates into a survival cost only in females. Such non‐linearities in the relationship between energy costs and survival costs may be widespread, and challenge the value of simple energy‐based measures of 'reproductive effort’.     

The effects of size, age and a cost of early breeding on reproduction in female mountain hares

Both age and size may influence female reproductive performance in mammals, and successful early reproduction may lead to reduced success at later attempts. The effects of age, size and early reproduction on distribution of reproductive effort throughout a single breeding season was examined in female mountains hares Lepus timidus L. Hind foot length was used as an index of body size, because, unlike body weight, it did not fluctuate with reproductive status. Fifty-six female carcasses were collected from March to October 1984, and their litters were assigned to one of three chronologically equal'litter periods'(1–3) of equal length. Whereas number of ova shed was always independent of age, large females shed more ova than did smaller females in litter periods 1 and 2. Prenatal mortality of ova and embryos was highest during litter period 1, when it was independent of age and size. Although prenatal mortality remained high in first year females in litter period 2, there was an overall decline through to the final litter period when it was negligible. Total number of young produced through the season increased with skeletal size in old females (age > 1), but not significantly in first year females. It is concluded that large size, rather than age, favours early reproduction in mountain hares. Every additional offspring produced in litter periods 1 and 2 reduced that female's production in period 3. After correcting for this cost of early reproduction the number of young produced in the final litter period also increased with maternal size.     

Fathers, fat, and maternal energetics in a biparental hamster: paternal presence determines the outcome of a current reproductive effort and adipose tissue limits subsequent reproductive effort

Djungarian hamster females, Phodopus campbelli, are severely constrained in their ability to reproduce successfully and lose 20% of their body weight by the time pups are weaned. In the wild and in the laboratory, biparental care improves maternal reproductive success. Two experiments quantified the effects of paternal presence and partial lipectomy [surgical depletion of parametrial white adipose tissue (PWAT) on day 8 of the 18-day gestation] on maternal energy balance, reproductive success, and investment in a subsequent reproductive attempt. Paired females reproduced successfully, maintained body weight, and invested in a second litter. Removal of the male decreased pup survival, growth, and readiness for dispersal by 18 days of age. Solitary females lost 10% of their body weight by the birth and a further 10% by day 18 after the birth. Thus, paternal presence balanced maternal energy budgets during reproduction and prevented a 20% loss in body weight. Equivalent weight loss occurs in response to other maternal stressors, therefore 20% may be the maximum tolerable weight loss in this species. Fresh weight of interscapular brown adipose tissue was predicted by the extent of maternal hyperthermia but not by maternal energy balance or lipectomy. Partial lipectomy did not adversely affect the female or the first litter but decreased the probability of investment in a second reproductive attempt and halved the size of the second litter. This effect may have been due to the 0.1% of body weight amount of lipid removed or may reflect a specialized role for PWAT in adjusting maternal investment.     

Ectoparasites and fitness of female Columbian ground squirrels

Parasites play an important role in the evolution of host traits via natural selection, coevolution and sexually selected ornaments used in mate choice. These evolutionary scenarios assume fitness costs for hosts. To test this assumption, we conducted an ectoparasite removal experiment in free-living Columbian ground squirrels (Urocittelus columbianus) in four populations over three years. Adult females were randomly chosen to be either experimentally treated with anti-parasite treatments (spot-on solution and flea powder, N = 61) or a sham treatment (control, N = 44). We expected that experimental females would show better body condition, increased reproductive success and enhanced survival. Contrary to our expectations, body mass was not significantly different between treatments at mating, birth of litter or weaning of young. Further, neither number nor size of young at weaning differed significantly between the two treatments. Survival to the next spring for adult females and juveniles was not significantly different between experimental and control treatments. Finally, annual fitness was not affected by the treatments. We concluded that females and their offspring were able compensate for the presence of ectoparasites, suggesting little or no fitness costs of parasites for females in the different colonies and during the years of our experiments.     

Differences in Patterns of Reproductive Allocation between the Sexes in Nicrophorus orbicollis

Organisms are selected to maximize lifetime reproductive success by balancing the costs of current reproduction with costs to future survival and fecundity. Males and females typically face different reproductive costs, which makes comparisons of their reproductive strategies difficult. Burying beetles provide a unique system that allows us to compare the costs of reproduction between the sexes because males and females are capable of raising offspring together or alone and carcass preparation and offspring care represent the majority of reproductive costs for both sexes. Because both sexes perform the same functions of carcass preparation and offspring care, we predict that they would experience similar costs and have similar life history patterns. In this study we assess the cost of reproduction in male Nicrophorus orbicollis and compare to patterns observed in females. We compare the reproductive strategies of single males and females that provided pre- and post-hatching parental care. There is a cost to reproduction for both males and females, but the sexes respond to these costs differently. Females match brood size with carcass size, and thus maximize the lifetime number of offspring on a given size carcass. Males cull proportionately more offspring on all carcass sizes, and thus have a lower lifetime number of offspring compared to females. Females exhibit an adaptive reproductive strategy based on resource availability, but male reproductive strategies are not adaptive in relation to resource availability.     

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.     

Maternal effort and male quality in the bank vole, Clethrionomys glareolus.

Parental investment in reproduction is adjusted according to potential benefits in terms of offspring survival and/or mating success. If male quality affects the reproductive success of a female, then females mating with high-quality males should invest more in reproduction. Although the subject has been of general interest, further experimental verification of the hypothesis is needed. We studied whether female bank voles (Clethrionomys glareolus) adjusted their maternal effort according to male quality, measured as mating success. To enable the measurement of maternal effort during nursing separately from male genetic effects the litters were cross-fostered. Further, the genetic background of male quality was examined. Male quality did not correlate with litter size or offspring size at birth. Offspring growth was positively related to food consumption and milk production of mothers. However, these direct measurements of maternal effort were independent of male quality. Male mating success appeared to be significantly heritable indicating that there are genetic benefits. Still, females did not adjust maternal effort according to the genetic quality of their offspring. We suggest that female bank voles gain significant genetic benefits from mating with high-quality males whereas they cannot improve their reproductive success by increasing maternal effort.     

Patterns of spatio-temporal variation in the survival rates of a viviparous lizard: the interacting effects of sex,reproductive trade-offs,aridity, and human-induced disturbance

Examination of the spatial and temporal variation in survival rates provides insight on how the action of natural selection varies among populations of single species. In this study, we used mark-recapture data from seven populations of the viviparous lizard Sceloporus grammicus in Central Mexico and a multi-model inference framework to examine interpopulation variation in the survival of adult males and females. We aimed to analyze the potential effects of aridity, human-induced disturbance, and reproductive costs on the survival rates of these lizards. For females in particular, we also searched for a negative relationship between litter size (adjusted for female size) and female survival. Our results demonstrate seasonal changes in survival for males and females. In three out of our seven study sites female survival decreased during the birthing season. In contrast, male survival did not appear to decrease during the mating season. We found an interaction between site-specific aridity and reproductive season affecting female survival. A decrease in female survival during the birthing season was observed in relatively arid sites. In one of these arid sites we found a negative effect of size-adjusted litter size on female survival: females producing more offspring than those expected for their size were more likely to die. This result represents evidence of a physiological trade-off for gravid females occurring in at least one of the studied populations. Interpopulation variation in the degree of human-induced disturbance could not explain the observed patterns of spatial variation in survival rates. Our results demonstrate wide variation in sex-specific survival patterns of this viviparous lizard and provide evidence that negative associations between reproduction and survival are highly dependent on the local environmental conditions.