Reproductive Decisions in Female European Ground Squirrels: Factors Affecting Reproductive Output and Maternal Investment

Physiological and behavioural parameters associated with reproductive effort and success were investigated in female European ground squirrels Spermophilus citellus . The proportion of reproductive (lactating) females in the study population was over 90% and was not related to age. Timing of oestrus and ovulation was found to be affected by the female's emergence date and condition. Females with low emergence mass showed delayed oestrus. Differences in ovulation dates were shown to affect reproductive output in terms of litter size and sex ratio. Early litters were larger and male biased. X-ray techniques were used to determine intrauterine litter size in individual females. The results indicated that litter size and sex ratio were fixed prenatally. Lactation costs were reflected in the intensity of mass loss and duration of lactation. Mass loss varied with litter size, in that females with large litters showed a more rapid loss than others. The second parental investment parameter, lactation duration, varied among individual females and was dependent on the timing of reproduction and litter size (except yearlings). Early born litters, which were, in most cases, larger than later ones, were nursed longer. Prolonged lactation periods affected female condition in that they started prehibernation fattening later and entered hibernation with a lower mass than individuals that had shorter lactation periods. Yearling females probably could not afford the energetic costs of long lactation, independent of their offspring number. These results indicated that females with higher reproductive output and higher investment were unable to compensate these costs before hibernation. Consequences for these individuals could therefore be lower over-winter survival or a delayed oestrus in the following season.     

Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: II. Intraspecific patterns

Based on a year-long field study in northeastern Madagascar, I summarize annual patterns of niche use (food patch size, diet, forest height, and forest site) in two sympatric lemurs, Varecia variegata rubra and Eulemur fulvus albifrons. Furthermore, I examine intraspecific patterns of niche use according to sex, season, and reproductive stage in these two lemurs that differ in terms of energetic investment in reproduction. Lemurs as a group provide a special opportunity to test hypotheses concerning sex differences in niche use. Due to their body size monomorphism and seasonal, synchronous pattern of breeding, it is possible to directly evaluate whether sex differences in diet reflect high energetic investment in reproduction by females. Results confirm the hypothesis that intraspecific variation in niche use (e.g., sex differences, seasonal differences) would be more pronounced in V. v. rubra than in E. f. albifrons, due in large measure to the former's relatively high energetic investment in reproduction: 1a) Dietary sex differences in V. v. rubra are most pronounced during costly reproductive stages and involve acquisition of low-fiber, high-protein plant foods. Females of both species consume more seasonally available low-fiber protein (young leaves, flowers) relative to conspecific males during the hot dry season, but only in V. v. rubra females is this pattern also evident during gestation and lactation. 1b) The diets of female V. v. rubra and female E. f. albifrons are more similar to each other than are the diets of conspecific males and females in the case of V. v. rubra. This is not uniformly the case for female E. f. albifrons. This finding confirms a hypothesis put forward in Vasey ([2000] Am J Phys Anthropol 112:411-431) that energetic requirements of reproductive females drive niche separation more than do the energetic requirements of males. 1c) Both species synchronize most or all of lactation with seasonal food abundance and diversity. E. f. albifrons shows a more protracted period of synchrony, and this may contribute to its wide biogeographic distribution in Madagascar. 2) Sex differences and seasonal differences in microhabitat use reflect intraspecific patterns of thermoregulation, predator avoidance, and in the case of V. v. rubra, reproduction. One important factor selecting for body size monomorphism in lemurs appears to be the tight synchrony between lactation and periods of food abundance afforded by annual, seasonal breeding.     

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.     

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     

Costs of reproduction and terminal investment by females in a semelparous marsupial

Evolutionary explanations for life history diversity are based on the idea of costs of reproduction, particularly on the concept of a trade-off between age-specific reproduction and parental survival, and between expenditure on current and future offspring. Such trade-offs are often difficult to detect in population studies of wild mammals. Terminal investment theory predicts that reproductive effort by older parents should increase, because individual offspring become more valuable to parents as the conflict between current versus potential future offspring declines with age. In order to demonstrate this phenomenon in females, there must be an increase in maternal expenditure on offspring with age, imposing a fitness cost on the mother. Clear evidence of both the expenditure and fitness cost components has rarely been found. In this study, we quantify costs of reproduction throughout the lifespan of female antechinuses. Antechinuses are nocturnal, insectivorous, forest-dwelling small (20-40 g) marsupials, which nest in tree hollows. They have a single synchronized mating season of around three weeks, which occurs on predictable dates each year in a population. Females produce only one litter per year. Unlike almost all other mammals, all males, and in the smaller species, most females are semelparous. We show that increased allocation to current reproduction reduces maternal survival, and that offspring growth and survival in the first breeding season is traded-off with performance of the second litter in iteroparous females. In iteroparous females, increased allocation to second litters is associated with severe weight loss in late lactation and post-lactation death of mothers, but increased offspring growth in late lactation and survival to weaning. These findings are consistent with terminal investment. Iteroparity did not increase lifetime reproductive success, indicating that terminal investment in the first breeding season at the expense of maternal survival (i.e. semelparity) is likely to be advantageous for females.     

The effects of lactation and infant care on adult energy budgets in wild siamangs (Symphalangus syndactylus)

In mammals with biparental care of offspring, males and females may bear substantial energetic costs of reproduction. Adult strategies to reduce energetic stress include changes in activity patterns, reduced basal metabolic rates, and storage of energy prior to a reproductive attempt. I quantified patterns of behavior in five groups of wild siamangs (Symphalangus syndactylus) to detect periods of high energetic investment by adults and to examine the relationships between infant care and adult activity patterns. For females, the estimated costs of lactation peaked at around infant age 4–6 months and were low by infant age 1 year, whereas the estimated costs of infant‐carrying peaked between ages 7 and 12 months, and approached zero by age 16 months. There was a transition from primarily female to male care in the second year of life in some groups. Females spent significantly less time feeding during lactation than during the later stages of infant care, suggesting that female siamangs do not use increased food intake to offset the costs of lactation. Female feeding time was highest between infant ages 16 and 21 months, a period of relatively low female investment in the current offspring that coincided with the period of highest male investment in infant care. This suggests that male care may reduce the costs of infant care for females in the later stages of a reproductive attempt. The female energy gain resulting from male care was likely invested in somatic maintenance and future reproduction, rather than the current offspring. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Familiarity breeds progeny: sociality increases reproductive success in adult male ring-tailed coatis (Nasua nasua)

The ring-tailed coati (Nasua nasua) is the only coati species in which social groups contain an adult male year round, although most males live solitarily. We compared reproductive success of group living and solitary adult male coatis to determine the degree to which sociality affects reproductive success. Coati mating is highly seasonal and groups of female coatis come into oestrus during the same 1-2 week period. During the mating season, solitary adult males followed groups and fought with the group living male. This aggression was presumably to gain access to receptive females. We expected that high reproductive synchrony would make it difficult or impossible for the one group living male to monopolize and defend the group of oestrous females. However, we found that group living males sired between 67-91% of the offspring in their groups. This reproductive monopolization is much higher than other species of mammals with comparably short mating seasons. Clearly, living in a group greatly enhanced a male's reproductive success. At the same time, at least 50% of coati litters contained offspring sired by extra-group males (usually only one offspring per litter); thus, resident males could not prevent extra-group matings. The resident male's reproductive advantage may reflect female preference for a resident male strong enough to fend off competing males.     

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.     

Timely estrus in wild brown mouse lemur females at Ranomafana National Park, southeastern Madagascar

The small-bodied nocturnal mouse lemurs (genus Microcebus) occupy a variety of habitats in Madagascar. Gray (M. murinus) and brown (M. rufus) mouse lemurs have been widely studied both in the wild and captivity. Whereas captive studies revealed an endogenous regulation of reproduction entrained by photoperiod, field studies have suggested that reproductive activation could be affected by additional climatic, physical, or social conditions. I collected data on wild brown mouse lemur females at Ranomafana between 2004 and 2008 to determine: 1) the timing of estrus and estrous periodicities across multiple seasons, and 2) whether additional factors such as body mass, age, or rainfall are correlated with onset of reproduction. In mouse lemur females at Ranomafana, the first seasonal estrus occurs 3-4 weeks after the vernal equinox. I report ~1 month's intra-population variation in the timing of estrus and inter-annual estrous intervals with periodicities of ~365 days. There were significant differences between the onset of reproduction across years. Estrous onset was uncorrelated with body mass, but there was an apparent age effect. There was a significant negative correlation between August rainfall and onset of reproduction when 2004 data were removed from the analysis. Results from this study are consistent with the notion that timing of estrus is photoperiod-dependent. As in captivity, intra-population variation in estrous onset is ~4 weeks in length. In the wild, variation in estrous onset and polyestry (multiple reproductive opportunities per year) appear to be favored under the highly unpredictable conditions of Madagascar's environments. In the wild, variation in estrous onset and polyestry (multiple reproductive opportunities per year) appear to be favored under the highly unpredictable conditions of Madagascar's environments.     

Is oxidative stress a physiological cost of reproduction? An experimental test in house mice

Investment in reproduction is costly and frequently decreases survival or future reproductive success. However, the proximate underlying causes for this are largely unknown. Oxidative stress has been suggested as a cost of reproduction and several studies have demonstrated changes in antioxidants with reproductive investment. Here, we test whether oxidative stress is a consequence of reproduction in female house mice (Mus musculus domesticus), which have extremely high energetic demands during reproduction, particularly through lactation. Assessing oxidative damage after a long period of reproductive investment, there was no evidence of increased oxidative stress, even when females were required to defend their breeding territory. Instead, in the liver, markers of oxidative damage (malonaldehyde, protein thiols and the proportion of glutathione in the oxidized form) indicated lower oxidative stress in reproducing females when compared with non-reproductive controls. Even during peak lactation, none of the markers of oxidative damage indicated higher oxidative stress than among non-reproductive females, although a positive correlation between protein oxidation and litter mass suggested that oxidative stress may increase with fecundity. Our results indicate that changes in redox status occur during reproduction in house mice, but suggest that females use mechanisms to cope with the consequences of increased energetic demands and limit oxidative stress.     

Mating system in mouse lemurs: theories and facts, using analysis of paternity

Among nocturnal Malagasy prosimians, the grey mouse lemur (Microcebus murinus) is considered a solitary species which has a promiscuous mating system. Indirect indicators, such as the lack of sexual dimorphism, the overlapping of male and female home ranges with each other, the synchronism of seasonal oestrus and the high relative testes size of males, support the presence of sperm competition. In captivity, an intense sexual precopulatory competition develops among males, leading to the emergence of a dominant male who fathers the majority of the litters. Although multiple mating did occur, the dominant male achieved the majority of the matings on the first day of oestrus. A 'mate-guarding' behaviour, exhibited by the dominant male, was observed in 11 groups out of 15, on only the first day of the vaginal opening and was significantly more often directed towards younger females. Females also played an important role in sexual competition among males, since their presence enhances the aggressive interactions between males. Difference in aggressive behaviours of females, in response to male sexual solicitations, suggests female mate choice. Compared with data from wild animals, it may be hypothesised that alternative mating strategies can be used by male grey mouse lemurs to enhance their reproductive success, depending on the availability and distribution of receptive females.     

Pregnancy in female house mice exposed to urinary chemosignals from other females.

Seven experiments were performed to investigate pregnancy termination, urinary chemosignals, and litter sex ratio variation in female house mice. Experiments tested the effects of urine from adult and prepubertal females, housed individually or in groups, on successful insemination and litter production by females treated at different times and for different periods during the 3 weeks before mating and during gestation. Treatment of females with urine from adult females housed eight per cage or with urine pooled from eight adult females housed individually for 2 or 3 weeks before mating resulted in fewer successful pregnancies and significantly more female-biased litters. Treatment with urine from adult or prepubertal females housed eight per cage or with urine pooled from eight mice housed individually for the first 6 days of gestation or throughout pregnancy resulted in a significant increase in the rate of pregnancy termination. These treatments resulted in lower body weights at birth and slower growth rates in all males and in some females. Puberty was delayed in female progeny from urine-treated dams in five of seven experiments, and these young females attained first oestrus at greater mean body weights than mice in other treatments. These findings indicate that, in mice, at high population density, communication via a urinary chemosignal can alter reproduction in recipient females. Availability of, and competition for, resources such as food would be greater at higher densities, possibly lowering the probability of reproductive success. Pregnancy termination and delays in reproduction and attainment of sexual maturity might lead to greater successful reproduction at a later time.     

Monogamy as a Rule Rather than Exception in Nocturnal Lemurs: the Case of the Fat-tailed Dwarf Lemur, Cheirogaleus medius

According to present hypotheses on the evolution of life history traits and social systems in Malagasy lemurs, nocturnality and infant parking are associated with a solitary lifestyle and a polygynous mating system. However, theoretically extreme seasonality of reproduction could limit the number of females that can be monopolized by a given male and thus hinder the evolution of polygyny. The aim of this ongoing study is to test these contrasting expectations by looking at the social and mating system of the fat-tailed dwarf lemur Cheirogaleus medius . This species hibernates for up to 7 mo, so that time for breeding and raising offspring is extremely limited.
A mark-recapture study in western Madagascar was combined with observations and radio-tracking of 36 individuals during the rainy seasons from 1995 to 1998. According to these data, fat-tailed dwarf lemurs live in permanent sleeping groups consisting of a male and a female (n = 8) or one male and two females (n = 1). One or two offspring from the previous year were frequently observed to sleep together with an adult pair. Members of each sleeping group were the exclusive users of their nest holes and home ranges. During the birth season, males and females took turns at baby-sitting their offspring. Females without paternal help were unable to raise their offspring successfully. Since females did not exhibit oestrus synchrony, the ultimate selective factor favouring pair-living could be obligate paternal investment. The results, together with the lack of sexual size dimorphism and relatively small testis size, suggest that the fat-tailed dwarf lemur lives in family groups with a monogamous mating system. A review of the mating systems of nocturnal lemurs shows that monogamy appears to be the rule rather the exception.     

Fecundity,Offspring Longevity,and Assortative Mating: Parametric Tradeoffs in Sexual and Life History Strategy

Genetic diversification of offspring represents a bet-hedging strategy that evolved as an adaptation to unpredictable environments. The benefits of sexual reproduction come with severe costs. For example, each offspring only carries half of each parent's genetic makeup through direct descent. The lower the reproductive rate, the more substantial the cost when considering the proportion of genes represented in subsequent generations. Positive assortative mating represents a conservative bet-hedging strategy that offsets some of these costs and preserves coadapted genomes in stable and predictable environments, whereas negative assortative mating serves the inverse function of genetic diversification in unstable and unpredictable environments.     

Fecundity, offspring longevity, and assortative mating: parametric tradeoffs in sexual and life history strategy

Genetic diversification of offspring represents a bet-hedging strategy that evolved as an adaptation to unpredictable environments. The benefits of sexual reproduction come with severe costs. For example, each offspring only carries half of each parent's genetic makeup through direct descent. The lower the reproductive rate, the more substantial the cost when considering the proportion of genes represented in subsequent generations. Positive assortative mating represents a conservative bet-hedging strategy that offsets some of these costs and preserves coadapted genomes in stable and predictable environments, whereas negative assortative mating serves the inverse function of genetic diversification in unstable and unpredictable environments.     

Paternity Determination in Two Groups of Eulemur fulvus mayottensis: Implications for Understanding Mating Strategies

We used random amplified polymorphic DNA (RAPD) to determine paternity in two groups of brown lemurs (Eulemur fulvus mayottensis). We analyzed the results in relation to behavioral data on observed copulations, dominance relationships among adult males, and female behavior. The association between paternity determination and behavioral sampling shows that paternity determination is a crucial tool for understanding the mating strategies and reproductive success in the studied species. In brown lemurs, dominance relationships between males are correlated with reproductive success, but male social dominance could be altered by female choice as suggested by the ability of subordinate males to sire offspring in the presence of a dominant male.     

Aspects of reproduction in the eastern rufous mouse lemur (Microcebus rufus) and their implications for captive management

The eastern rufous mouse lemur is one of the smallest primate species. It inhabits the eastern rain forest of Madagascar. Its reproductive biology has not been examined because of its rarity in laboratories. We present the first data on reproduction and variation in reproductive success from a breeding colony of wild‐caught Microcebus rufus. The eastern rufous mouse lemur shows a seasonal change in testicular size and in the occurrence of estrus. Females had 2.5 cycles (range, one to four) per season. The estrous cycle length was 59 days (range, 51–66), the duration of vaginal opening during estrus was 7.5 days (range, 5–8), receptivity occurred on the third day of estrus, gestation length was 56.5 days (range, 56–57), litter size was two neonates (range, one to three). The frequency and duration of mating behavior varied widely among the pairs. Copulation seemed to occur on a single day per estrus within the first to fourth hour after light change to red light. In four cases (three pairs), copulation lasted between 15 and 240 seconds. Breeding success can be increased by choosing mates carefully. Microcebus rufus seems to be a seasonal breeder like its sibling species Microcebus murinus. In wild‐caught animals, males seemed to adapt quickly (first season) to the conditions of captivity, whereas in the females, individual variation (first to third season) in reproductive activity was observed. Air humidity of >60% seems to facilitate the breeding success in wild‐caught pairs. First pregnancy and successful rearing of offspring occurred in the second and fourth year of captivity in two of three females. Wild‐caught eastern rufous mouse lemurs seemed to demonstrate variation in adapting to the conditions of captivity with regard to sex and individuality. Zoo Biol 20:157–167, 2001. © 2001 Wiley‐Liss, Inc.     

Determinants of reproductive success in voles: space use in relation to food and litter size manipulation

Spacing behaviour of female mammals is suggested to depend on the distribution and abundance of food. In addition, food limitation has been found to constrain the reproductive success of females. However, whether females maximize their reproductive success by adjusting space use in relation to current food availability and reproductive effort (e.g. litter size) has not been experimentally studied. We examined these questions by manipulating simultaneously food resources (control vs. food supplementation) and litter sizes (control vs. plus two pups) of territorial female bank voles (Clethrionomys glareolus) in large outdoor enclosures. Females with supplementary food had smaller home ranges (foraging area) and home range overlaps than control females, whereas litter size manipulation had no effect on space use. In contrast, the size of territory (exclusive area) was not affected by food supplementation or litter size manipulation. As we have previously shown elsewhere, extra food increases the reproductive success of bank vole females in terms of size and proportion of weaned offspring. According to the present data, greater overlap of female home ranges had a negative effect on reproductive success of females, particularly on survival of offspring. We conclude that higher food availability increases the reproductive success of bank vole females, and this effect may be mediated through lower vulnerability of offspring to direct killing and/or detrimental effects from other females in the population. Moreover, it seems that when density of conspecifics is controlled for, home range sizes of females, but not territoriality, is related to food resources in Clethrionomys voles.     

Time spent in distinct life history stages has sex‐specific effects on reproductive fitness in wild Atlantic salmon

In species with complex life cycles, life history theory predicts that fitness is affected by conditions encountered in previous life history stages. Here, we use a 4‐year pedigree to investigate if time spent in two distinct life history stages has sex‐specific reproductive fitness consequences in anadromous Atlantic salmon (Salmo salar). We determined the amount of years spent in fresh water as juveniles (freshwater age, FW, measured in years), and years spent in the marine environment as adults (sea age, SW, measured in sea winters) on 264 sexually mature adults collected on a river spawning ground. We then estimated reproductive fitness as the number of offspring (reproductive success) and the number of mates (mating success) using genetic parentage analysis (>5,000 offspring). Sea age is significantly and positively correlated with reproductive and mating success of both sexes whereby older and larger individuals gained the highest reproductive fitness benefits (females: 62.2% increase in offspring/SW and 34.8% increase in mate number/SW; males: 201.9% offspring/SW and 60.3% mates/SW). Younger freshwater age was significantly related to older sea age and thus increased reproductive fitness, but only among females (females: ?33.9% offspring/FW and ?32.4% mates/FW). This result implies that females can obtain higher reproductive fitness by transitioning to the marine environment earlier. In contrast, male mating and reproductive success was unaffected by freshwater age and more males returned at a younger age than females despite the reproductive fitness advantage of later sea age maturation. Our results show that the timing of transitions between juvenile and adult phases has a sex‐specific consequence on female reproductive fitness, demonstrating a life history trade‐off between maturation and reproduction in wild Atlantic salmon.     

Limitation of reproductive success by food availability and litter size in the bank vole,Clethrionomys glareolus

Food limitation has been suggested as one of the most important factors affecting life history evolution in terrestrial vertebrates. However, this inference is based mainly on evidence from birds, and reproductive trade-offs may differ among groups with different forms of parental care. To study whether the costs of enlarged litters (decreased mass of offspring) would appear when food is not limiting, we performed outdoor enclosure experiments in which we manipulated simultaneously the litter size (control versus litter plus two pups) and food availability (control versus food-supplemented) of female bank voles, Clethrionomys glareolus. The weaning success of females increased significantly in response to supplementary food. When females were provided with extra food, no differences were observed in body masses of weanlings of control and enlarged litters. Further, food-supplemented females grew to larger sizes during nursing than unsupplemented females. Our experiment suggests that energetic requirements during nursing constrain the number of offspring that can be raised successfully in a particular breeding attempt. The results also indicate that unlimited food resources may increase future reproductive potential of females because they can use more energy for somatic growth.