Proximate and ultimate explanations of mammalian sex allocation in a marsupial model

Offspring sex ratios in mammals vary in potentially adaptive yet unpredictable ways. An integrative approach that simultaneously examines proximate and ultimate explanations of mammalian sex ratios would greatly advance the field. We examined the importance of maternal glucose and stress hormones for offspring sex (male or female) as mechanisms associated with the Trivers–Willard and the local resource competition hypotheses of sex allocation. We tested this framework in a marsupial mammal, the tammar wallaby (Macropus eugenii). Mothers that were better able to maintain body condition over the driest part of the year, a presumptive proxy for local resource availability, were more likely to produce daughters (the philopatric sex), consistent with local resource competition. Maternal glucose was correlated with offspring sex, but in the opposite direction than we predicted—higher maternal glucose was associated with female pouch young. These patterns, however, were not consistent across the 2 years of our study. Maternal stress hormone metabolites measured from fecal samples did not predict glucose or offspring sex. A causative glucose mechanism may underlie an adaptive strategy for mothers with high local resources (high glucose) to produce philopatric daughters that will benefit from inheriting resource access. Examining species-specific relationships between glucose and offspring sex across mammals could provide crucial insight into the disparate ecological and selective pressures faced by mammals with respect to offspring sex ratio.     

Mixed sex allocation strategies in a polytocous mammal,the house mouse (<Emphasis Type="Italic">Mus musculus</Emphasis>)

The issue of adaptive adjustment of offspring sex ratio (proportion of male births) in polytocous mammals, producing several offspring per litter, is controversial because females of these species can maximize their fitness mainly by adjusting offspring number. To address this issue, we examined the effect of maternal condition at mating, experimentally decreased by pre-mating food restriction, on the sex ratio variation in 137 female mice. We tested two basic sex allocation hypotheses plausible for polytocous mammals: (1) the Myers hypothesis, predicting that cheaper sex should be favored in poor environmental conditions to maximize offspring number; and (2) the Williams hypothesis, predicting maximum fitness returns by adjusting size- and sex-specific composition of the litter according to the maternal condition. The food-restricted mothers produced larger litters with a higher proportion of cheaper daughters than the control mothers. By contrast, the control mothers optimized size and sex composition of the litter according to their weight at mating. In addition, the offspring of the food-restricted mothers suffered less from pre-weaning mortality than those of the control mothers. Therefore, when comparing the groups, the Myers hypothesis had a general significance while the Williams hypothesis was plausible only for the control mothers. Furthermore, some of the food-restricted mothers partly coped with the pre-mating food restriction and increased the proportion of sons in the litter with the increasing maternal weight loss (during the period of food restriction). The sex ratio variation was thus a result of three sex allocation strategies depending on the maternal condition at mating.     

Sex bias or equal opportunity? Patterns of maternal investment in bison

Summary In polygynous mammals, it may be adaptive for mothers to invest more in sons and/or to adjust the sex ratio of offspring in relation to body condition. Calving patterns were examined over an 8-year period (1982–1989) for a population of Bison bison in which barren females are not selectively culled. From these data, we tested predictions of the sex ratio adjustment hypothesis as well as two assumptions: (1) that offspring weight at the end of the period of parental investment (PI) is correlated with later condition, and (2) that maternal and offspring condition during the period of PI are correlated. In contrast to predictions, there was little evidence that mothers in better condition bear more sons. Short- and long-term measures of maternal condition (previous reproductive status, age, dominance status, pre-pubertal body weight, age at first reproduction, birth date, and the duration of the mother's own suckling period) were little related to offspring sex ratio, although the last calves of old females were nearly always female. Similarly, there was little evidence for sex-biased PI. Weights at about 7 months of age were greater for males than females; males also had somewhat later birth dates, suggesting either longer gestation or later conception. However, maternal reproductive costs, as measured by subsequent fecundity, weight loss, and interbirth intervals, did not vary with calf sex. Both assumptions of the model received some support. However, while maternal condition was correlated with offspring condition, there may be sex differences in investment patterns. Mothers appear better able to influence the condition of daughters than of sons. This sex difference may negate any benefit from male-biased investment.     

Sex allocation in a monomorphic seabird with a single-egg clutch: test of the environment, mate quality, and female condition hypotheses

Sex allocation theory posits that mothers should preferentially invest in sons when environmental conditions are favorable for breeding, their mates are of high quality, or they are in good body condition. We tested these three hypotheses in rhinoceros auklets (Cerorhinca monocerata), monomorphic seabirds that lay a single-egg clutch, in 2 years that differed in environmental conditions for breeding. Results supported the environment and mate quality hypotheses, but these effects were interactive: offspring sex was independent of paternal traits in the poor year for breeding, while females mated to larger and more ornamented males reared more sons in the better year. Conversely, offspring sex was unrelated to female condition, as indexed by hatching date. We propose that good rearing conditions enable females to rear sons possessing the desirable phenotypic attributes of their mates. Results also supported two critical assumptions of sex allocation theory: (1) dimorphism in offspring condition at independence: daughters fledged with higher baseline levels of corticosterone than sons and (2) differential costs of rearing sons versus daughters: mothers rearing sons when environmental conditions were poor completed parental care in poorer condition than mothers rearing daughters in the same year and mothers rearing either sex when conditions were better. These novel results may help to explain the disparate results of previous studies of avian sex allocation.     

Variation in offspring sex ratio among individual Weddell seal (<Emphasis Type="Italic">Leptonychotes weddellii</Emphasis>) females of different quality

The Trivers–Willard model predicts that in polygynous species, superior-quality females will maximize their fitness by producing male offspring. Using a sample of 1,780 Weddell seal (Leptonychotes weddellii) pups recorded over 31 years, we investigated relationships between offspring sex ratio and maternal age, reproductive experience, an index of maternal lifetime reproductive output, and annual environmental variations. We found evidence that females with higher index of lifetime reproductive output were more likely to produce male than female offspring but found only weak evidence that large-scale environmental variations influenced sex ratios. Our results suggest that mothers manipulate offspring sex to maximize their own fitness, and inherent maternal quality may influence offspring sex. These findings support the Trivers–Willard sex-allocation model. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Baboons adjust secondary sex ratio in response to predictors of sex-specific offspring survival

Summary Most theories of sex ratio adjustment assume that parents will adjust the sex ratio of births (secondary sex ratio) in a manner that maximizes offspring reproductive success (as long as this does not jeopardize parental reproductive success). Survival to maturity is typically the largest component of variance in offspring reproductive success. This should make environmental predictors of sex-specific offspring survival strong predictors of secondary sex ratio adjustment. We tested this survivorship maximization hypothesis for secondary sex ratio adjustment using data from a 17-year demographic study of 315 yellow baboon infants at Mikumi National Park, Tanzania. Sex differences were found in the degree to which several social and ecological conditions affected infant survival to 1 year. Female, but not male, infant survival was inversely correlated with birth order and the proportion of infant females in their birth cohort. Male, but not female, infant survival was inversely correlated with the amount of rainfall early in the year (January) and the proportion of infant males in their birth cohort; male survival also was positively correlated with maternal dominance rank. The consistency and timing of these effects across years suggested that such information was, in fact, available to females around the time of conception. Most importantly, social and ecological conditions that predicted improved survivorship of a given sex also were positively correlated with production of that sex. Early births were female-biased; and low January rainfall was correlated with a male-biased sex ratio, becoming increasingly female-biased as January rainfall increased. However, no sex ratio effects were correlated with maternal rank. Data supported the hypothesis that females adjusted secondary sex ratio in a manner that maximized sex-specific infant survival. This hypothesis also offered a plausible explanation for some of the contradictory data that have arisen from studies of maternal rank effects on sex ratio both within and between species.Correspondence to: S. K. Wasser     

Variation in litter size: a test of hypotheses in Richardson's ground squirrels

We studied litter size variation in a population of Richardson's ground squirrels (Spermophilus richardsonii) in Alberta, Canada, from 1987 to 2004. Litter size at first emergence of juveniles from the natal burrow ranged from 1 to 14; the most common litter sizes, collectively accounting for 41.0% of 999 litters, were 6 and 7. The number of offspring surviving to adulthood (attained on emergence from hibernation as yearlings) increased with increasing litter size, a result that was not predicted by Lack's "optimal litter size" hypothesis, Mountford's "cliff-edge" effect, or the "bad-years" effect. Contrary to the negative effects predicted by the "cost of reproduction" hypothesis, litter size had no significant influence on survival of mothers to the subsequent year or on the size of the subsequent litter. Rather, our results best fit the predictions of the "individual optimization" hypothesis, which suggests that litter size is determined by the body condition and environmental circumstances of each mother. Supporting this hypothesis, survival of individual offspring was not significantly associated with litter size. Additionally, year-to-year changes in maternal body mass at mating were positively associated with concurrent changes in litter size (r = 0.56), suggesting that litter size depends on the body condition of the mother. Because the mean number of recruits to adulthood increased as litter size increased (r2 = 0.96) and litter size increased with maternal condition, offspring productivity was greater for mothers in better body condition.     

The impact of behavioral and physiological maternal effects on offspring sex ratio in the common snapping turtle,<Emphasis Type="Italic"> Chelydra serpentina</Emphasis>

Theory suggests that maternal effects are especially important in organisms with environmentally-sensitive sex-determining mechanisms. However, there is no substantive body of empirical evidence to confirm this conjecture. We integrated field and laboratory studies to jointly evaluate the significance of behavioral (nest-site choice) and physiological (yolk hormone allocation) maternal effects on offspring sex ratio in the common snapping turtle (Chelydra serpentina), a species with temperature-dependent sex determination (TSD). Of the 16 microhabitat variables measured, only three (south, east, and total overstory vegetation cover) were significantly correlated with nest temperature: cooler nests were located under more vegetation cover. In turn, these microhabitat predictors of nest temperature, and nest temperature itself, may influence nest sex ratio: shadier, cooler nests were more likely to produce a higher proportion of male offspring than less shady, warmer nests. Analysis of eggs from these same nests incubated in a common garden design in the laboratory revealed that clutch sex ratio was unaffected by levels of yolk estradiol, yolk testosterone, or their interaction. Examination of both behavioral and physiological maternal effects revealed no concordant impact on offspring sex ratio. However, eggs from nests that produced male-biased sex ratios in the field yielded higher proportions of males under constant-temperature conditions in the laboratory. Our study confirms the importance of behavioral maternal effects in nature on offspring sex ratios in species with TSD, while also revealing the potential presence of a predisposition for sex-ratio production underlying TSD in this system.Communicated by S. Krackow     

Variations in the birth sex ratio and neonatal mortality in a natural herd of horses

Variations in birth sex ratios and sex differences in juvenile mortality occur in a number of mammalian species, and in many cases have been linked to resource availability. Most of these biases in offspring sex ratios concern polygynous species with pronounced sexual dimorphism, and where females only are philopatric. Data on species with unusual life-history strategies, such as slight sexual dimorphism or dispersal by both sexes, are of particular interest. In this study of a natural herd of horses (Equus caballus) which experienced an eruptive cycle, and therefore a period of nutritional stress, male offspring had higher neonatal mortality rates in nutritionally poor years than in good ones, whereas “year quality” had no effect on the mortality of female offspring; year quality could therefore be used by mares as predictor of sex-specific offspring survival. We show that the environmental conditions that predicted lower survival of males were negatively related to their production: the birth sex ratio the following year was female-biased; and mares were less likely to produce a son when they had produced a son the preceding year. There was no significant effect of mother's parity, age or rank, or the timing of conception or birth on offspring sex ratios. The mechanism leading to biases in the birth sex ratio could have been the loss of male embryos by mares that did not foal. As there was no evidence for selective abortion of male foetuses in females that did foal the next year, it is not necessary to invoke maternal adjustment, though this remains a possibility. Finally, there was a suggestion that male offspring were more costly to raise than females, since mothers that reared a son in poor years tended to experience an increase in the interbirth interval between their two subsequent offspring. Received: 28 December 1996 / Accepted after revision: 27 July 1997     

Offspring sex ratio variation in the bridled nailtail wallaby, Onychogalea fraenata

The bridled nailtail wallaby is a sexually size dimorphic, promiscuous, solitary macropod. Sex ratios of pouch young were studied at two sites over 3 years, beginning with 14 months of severe drought. Females that were in better condition were more likely to have sons, and condition was dependent on body size. Females at one site were heavier, were consequently in better condition, and produced more sons than females at the other site. Females that declined in condition had more daughters during the most severe part of the drought than females that maintained condition, but endoparasite infection did not affect the pouch young sex ratio. Age also appeared to affect sex ratio adjustment, because weight was strongly influenced by age. Sex ratio bias was not caused by early offspring mortality, but occurred at conception. Mothers did not appear to bias energy expenditure on sons or daughters; males and females did not differ in condition at the end of pouch life. Pouch young sex ratio variation was most consistent with the Trivers-Willard hypothesis, but could also have been influenced by local resource competition, since sons dispersed further than daughters. Offspring condition was related to survival, and was correlated with maternal condition. Received: 14 April 1998 / Accepted after revision: 10 November 1998     

Birth sex ratios in toque macaques and other mammals: integrating the effects of maternal condition and competition

Mammalian life histories suggest that maternal body condition and social dominance (a measure of resource-holding potential) influence the physical and social development of offspring, and thereby their reproductive success. Predictably, a mother should produce that sex of offspring which contributes most to her fitness (as measured by the number of her grandchildren) and that she is best able to raise within the constraints imposed by her condition, social rank, and environment. Such combined effects were investigated by monitoring variations in body condition (weight) and behavior of female toque macaques, Macaca sinica of Sri Lanka, in a changing forest environment over 18 years. Maternal rank, by itself, had no influence on offspring sex, but did affect maternal body condition. The combined effects of rank and condition indicated the following: mothers in robust condition bore more sons, whereas those in moderate condition bore more daughters, but both effects were expressed most strongly among mothers of high rank. Where the consequences of low rank were felt most acutely, as shown by poor condition, mothers underproduced daughters. Environmental quality directly influenced rank and condition interactions, and thus sex ratios. These relationships, and data from other mammals suggest an empirically and theoretically consistent pattern of sex allocation in mammals. New predictions integrate effects, proposed by Trivers and Willard, that are rooted in male mate competition, which is universal among polygynous mammals, with those of local resource competition (and/or female reproductive competition), which are not universal and differ in intensity between the socioecologies and local environments of different species. Received: 30 May 1998 / Accepted after revision: 29 August 1998     

Pup production,sex ratios,and survivorship in African wild dogs, <Emphasis Type="Italic">Lycaon pictus</Emphasis>

The local resource enhancement (LRE) model predicts that in cooperatively breeding species, sex ratios will be biased in favor of the more helpful sex. In this study, we assess the assumptions underlying the LRE model in a population of cooperatively breeding wild dogs (Lycaon pictus) in Northern Botswana monitored over a 15-year period. In this population, litter size and pup survival to 1 year are strongly affected by pack size and the breeding female’s age, but adult males have a stronger and more linear effect on females’ reproductive performance than do adult females. This asymmetry in the benefits derived from male and female helpers is reflected in male-biased sex ratios in litters at the time pups emerge from the den. Sex ratio biases are most pronounced in the litters of the youngest mothers who live in significantly smaller packs than older females. The presence of potential rivals for the dominant female’s position depresses pup production at the time of emergence, suggesting that competition among females for breeding positions may also contribute to the selective forces affecting birth sex ratios.     

Effects of elevated yolk testosterone levels on survival, growth and immunity of male and female yellow-legged gull chicks

Androgen hormones of maternal origin contained in the eggs of avian species are considered to have positive effects on offspring characteristics and performance. However, negative consequences have also been reported, suggesting that mothers may experience a trade-off between beneficial and detrimental effects of egg androgens to offspring fitness. We studied the effects of elevated yolk testosterone (T) concentration on survival, development and phenotype of male and female yellow-legged gull (Larus michahellis) chicks by injecting egg yolks with physiological doses of the hormone. Elevated yolk T resulted in a male-biased post-hatching sex ratio, T-treated clutches producing a greater proportion of males compared to control ones at day 4 post-hatching, likely resulting from a reduction of female embryonic survival, whereas no effect of hormone treatment on hatching success or short-term chick survival was observed. In addition, T depressed post-hatching body mass in both sexes but had no effects on the intensity of the cell-mediated immune response or skeletal growth. No sex differences in egg characteristics or chick phenotype were detected. Time to hatching was not affected by T, but females originating from first laid eggs hatched earlier than males of the same laying order, independently of hormone treatment. However, the implications of sex differences in hatching times are unclear in the study species. Taken together, our results suggest that female yellow-legged gulls may be constrained in transferring androgens to their eggs by negative consequences on the viability of female offspring and growth of chicks of the two sexes.     

Group histories and offspring sex ratios in ringtailed lemurs (Lemur catta)

Birth sex ratios were examined for ringtailed lemurs (Lemur catta) at the Duke University Primate Center. This population provides a long-term database of births under a variety of demographic and management conditions, including two semi-freeranging groups between which males transfer freely and females defend stable territorial boundaries. We examined three hypotheses usually considered in studies of primate sex ratio bias. The Trivers-Willard hypothesis predicts that dominant females produce males, local resource competition at the population level (LRC-population) predicts that the dispersing sex (males) will be overproduced in dense populations, and local resource competition among individuals (LRC-individual) predicts that dominant females overproduce the philopatric sex (females). We also examined a fourth hypothesis, local resource enhancement (LRE), which is usually subsumed under LRC-individual in studies of primate sex ratio evolution. LRE predicts that under certain conditions, females will produce the sex that provides later cooperative benefits, such as alliance support for within- or between-group competition. Our data provide support for LRE: females overproduce daughters given prospects of new group formation, either through group fission or threatened expulsion of young mothers. Behavioral data from Duke and also wild populations show that daughters serve mothers as important allies in this context and LRE effects also have been documented in other mammals that experience similar group histories. Nonsignificant trends in the data supported the LRC-population hypothesis, and we suggest that LRC interacts with LRE to explain offspring sex ratios in ringtailed lemurs. Received: 27 August 1999 / Received in revised form: 6 March 2000 / Accepted: 18 March 2000     

Transgenerational plasticity in the sea: context-dependent maternal effects across the life history

Maternal effects can have dramatic influences on the phenotype of offspring. Maternal effects can act as a conduit by which the maternal environment negatively affects offspring fitness, but they can also buffer offspring from environmental change by altering the phenotype of offspring according to local environmental conditions and as such, are a form of transgenerational plasticity. The benefits of maternal effects can be highly context dependent, increasing performance in one life-history stage but reducing it in another. While maternal effects are increasingly well understood in terrestrial systems, studies in the marine environment are typically restricted to a single, early life-history stage. Here, I examine the role of maternal effects across the life history of the bryozoan Bugula neritina. I exposed maternal colonies to a common pollution stress (copper) in the laboratory and then placed them in the field for one week to brood offspring. I then examined the resistance of offspring to copper from toxicant-exposed and toxicant-na?ve mothers and found that offspring from toxicant-exposed mothers were larger, more dispersive, and more resistant to copper stress than offspring from na?ve mothers. However, maternal exposure history had pervasive, negative effects on the post-metamorphic performance (particularly survival) of offspring: offspring from toxicant-exposed mothers had poorer performance after six weeks in the field, especially when facing high levels of intraspecific competition. Maternal experience can have complex effects on offspring phenotype, enhancing performance in one life-history stage while decreasing performance in another. The context-dependent costs and benefits associated with maternally derived pollution resistance may account for why such resistance is induced rather than continually expressed: mothers must balance the benefits of producing pollution-resistant larvae with the costs of producing poorer performing adults (in the absence of pollution).     

Androgen-dependent maternal effects on offspring fitness in zebra finches

There is accumulating evidence that maternal hormones may play a role in offspring sex adjustment, but little is known about the costs of such hormone-mediated mechanisms. Recent studies have reported sex-specific effects of hormones on offspring viability. Specifically, we previously found that elevating the plasma androgen level in mothers results in a male-biased offspring primary sex ratio, but it affects the viability of sons negatively and daughters positively in zebra finches (Taeniopygia guttata; Rutkowska and Cichoń, Anim Behav, 71:1283–1288, 2006). In this study, we studied further fitness consequences of exposure to elevated yolk androgen levels in zebra finches. We measured growth rate and cellular immune response of nestlings that hatched from eggs laid by females injected with testosterone during egg laying and nestlings of unaffected control females. We found that sons of testosterone-treated females grew slower in comparison to sons of control females. The significant interaction between experimental group and offspring sex indicates that sons of testosterone-treated mothers suffered impaired immune responsiveness while daughters seemed to benefit from elevated androgen level in terms of enhanced immune responsiveness. We found no effects of androgens on offspring performance at adulthood—neither fecundity of females nor attractiveness of males was affected. We conclude that the benefits of biasing sex ratio towards males by increasing androgen level in the yolk may be limited due to negative effects on male offspring performance early in life.     

Sex differences in the consequences of maternal loss in a long-lived mammal, the red deer (Cervus elaphus)

In several primates, the presence of mothers affects the growth, survival and reproduction of their offspring, but similar effects have not yet been demonstrated in ungulates. Here, we investigate the effects of the mother’s presence in a population of red deer (Cervus elaphus) on the Isle of Rum, Scotland, which is the subject of a long-term, individual-based study. We compared measures of performance including antler growth in young males and age at first reproduction in females and survival of deer with mothers still alive against those that have lost their mothers (orphans). We show that orphaning both before and after weaning increases the risk of a natural death for both sexes. For males, no maternal benefit was detectable past 24 months of age while, for females, post-weaning benefits continued throughout life. Orphaning resulted in compromised male physical condition as measured by a reduced probability of growing antlers by 16 months of age while no evidence for compromised reproduction was found in females. These results support assertions that post-weaning maternal associations affect the development and survival of offspring.     

No evidence for offspring sex-ratio adjustment to social or environmental conditions in cooperatively breeding purple-crowned fairy-wrens

When fitness returns or production costs vary between male and female offspring, selection is expected to favor females that adjust offspring sex ratio accordingly. However, to what extent vertebrates can do so is the subject of ongoing debate. Here, we explore primary sex ratios in 125 broods of cooperatively breeding purple-crowned fairy-wrens Malurus coronatus. We expected that females might adjust offspring sex ratio because this passerine species experiences considerable variation in social and environmental conditions. (1) However, although helpers substantially increase parental fitness, females (particularly in pairs and small groups) did not overproduce philopatric males (helper-repayment hypothesis). (2) Sex-ratio adjustment based on competition among individuals (helper-competition hypothesis) did not conceal helper-repayment effects or drive sex allocation on its own: while high-quality territories can accommodate more birds, brood sex ratios were independent of territory quality, alone or in interaction with group size. (3) Additionally, males are larger than females and are possibly more costly to produce (costly sex hypothesis), and (4) female offspring may benefit more from long-term effects of favorable conditions early in life (Trivers–Willard hypothesis). Nonetheless, large seasonal variation in food abundance was not associated with a consistent skew in primary sex ratios. Thus, overall, our results did not support the main hypotheses of adaptive sex-ratio adjustment in M. coronatus. We discuss that long-term differential costs and benefits may be insufficient to drive evolution of primary sex-ratio manipulation by M. coronatus females. More investigation is therefore needed to determine the general required sex differences in long-term fitness returns for mechanisms of primary sex-ratio manipulation to evolve.     

Maternal investment in mountain baboons and the hypothesis of reduced care

It has been argued that female mammals should terminate expensive forms of infant care earlier as habitat quality declines. More recently it has been shown that among a variety of mammalian species, early termination of care is also associated with highly favourable conditions. In this paper we present data on maternal investment decisions among baboons (Papio cynocephalus ursinus) inhabiting the Drakensberg Mountains of South Africa, and compare these with data from East African baboon studies. Mothers in the mountain habitat face a set of environmental conditions where the problem of resource allocation to offspring is expected to be particularly acute. We begin by using the model of Altmann (1980) of maternal time budgets to demonstrate that mountain baboon mothers experience greater perturbations to their activity budgets while suckling than do mothers in other populations. They also provide consistently greater levels of care to their infants and do so in the absence of any form of overt conflict over access to the nipple. Although this investment results in a relative lengthening of the interbirth interval (IBI), it is accompanied by relatively higher infant survival. We argue that factors that influence the maternal strategy adopted by mountain baboons include slow infant growth rates and a lack of predation in the habitat which influences probability of offspring survival beyond the immediate postnatal period. We suggest that both “care-dependent” sources of mortality (e.g. female reproductive condition, the amount of milk transferred to offspring) as well as “care independent” sources of mortality (e.g. predation, infectious disease) should be considered in studies of parental investment. Received: 26 May 1997 / Accepted after revision: 9 August 1997     

Lifetime and intergenerational fitness consequences of harmful male interactions for female lizards

Male mating behaviors harmful to females have been described in a wide range of species. However, the direct and indirect fitness consequences of harmful male behaviors have been rarely quantified for females and their offspring, especially for long-lived organisms under natural conditions. Here, lifetime and intergenerational consequences of harmful male interactions were investigated in female common lizards (Lacerta vivipara) using field experiments. We exposed females to male harm by changing the population sex ratio from a normal female-biased to an experimental male-biased sex ratio during the first experimental year. Thereafter, females and their first generation of offspring were monitored during two additional years in a common garden with a female-biased sex ratio. We found strong immediate fitness costs and lower lifetime reproductive success in females subjected to increased male exposure. The immediate fitness costs were partly mitigated by direct compensatory responses after exposure to male excess, but not by indirect benefits through offspring growth, offspring survival, or mating success of offspring. These results support recent empirical findings showing that the direct costs of mating are not outweighed by indirect benefits.