Physiological costs and carry-over effects of avian interspecific brood parasitism influence reproductive tradeoffs

Although models of co-evolution between brood parasites and their hosts primarily focus upon the cost to hosts in the current reproductive bout, the impact of brood parasitism may carry over to future reproductive attempts by altering resource allocation. Glucocorticoid stress hormones help mediate resource allocation to reproduction, yet they have rarely been examined in brood parasitic systems. Here we determined if shifts in parental care and corticosterone had carry-over effects on future reproductive effort in the rufous-and-white wren (Thryophilus rufalbus), a host of the Central American striped cuckoo (Tapera naevia). We found that parasitized parents had significantly higher stress-induced, but not baseline, corticosterone than natural parents during the fledgling stage, which was associated with changes in parental care. The high investment in current reproduction while parasitized may be due to the value of fledged chicks in tropical systems. This maladaptive response by parasitized parents was associated with delayed re-nesting and a reduced likelihood of nesting in the subsequent breeding season. Although a reduction in future reproductive effort can result from a combination of factors, this work suggests that fitness costs of brood parasitism are mediated by changes in corticosterone and parental care behavior that carry over into subsequent breeding seasons.     

Should advertising parental care be honest?

Species with paternal care show less exaggerated sexual ornamentation than those in which males do not care, although direct benefits from paternal care can vastly exceed the indirect benefits of mate choice. Whether condition-dependent handicaps can signal parenting ability is controversial. The good-parent process predicts the evolution of honest signals of parental investment, whereas the differential-allocation model suggests a trade-off between the attractiveness of a mate and his care-provisioning. I show that both alternatives can arise from optimal allocations to advertisement, parental investment and future reproductive value of the male, and that the male''s marginal fitness gain from multiple matings determines which option should apply. The marginal gain is diminishing if opportunities for polygyny or extra-pair copulations are limited. Advertisement is then expected to be modest and honest, indicating genetic quality and condition-dependent parental investment simultaneously. Increasing marginal gains are likely to be related to cases where genetic quality has a significant influence on offspring fitness. This alternative leads to differential allocation with stronger advertisement, more frequent extra-pair copulations, and diminished male care. Reliability is also reduced if allocation benefits have thresholds, e.g. if there is a minimum body condition required for survival, or if females use a polygyny-threshold strategy of mate choice.     

Does a trade‐off between current reproductive success and survival affect the honesty of male signalling in species with male parental care?

Recent theory predicted that male advertisement will reliably signal investment in paternal care in species where offspring survival requires paternal care and males allocate resources between advertisement and care. However, the predicted relationship between care and advertisement depended on the marginal gains from investment in current reproductive traits. Life history theory suggests that these fitness gains are also subject to a trade‐off between current and future reproduction. Here, we investigate whether male signalling remains a reliable indicator of parental care when males allocate resources between current advertisement, paternal care and survival to future reproduction. We find that advertisement is predicted to remain a reliable signal of male care but that advertisement may cease to reliably indicate male quality because low‐quality males are predicted to invest in current reproduction, whereas higher‐quality males are able to invest in both current reproduction and survival to future reproduction.     

Voice pitch alters mate-choice-relevant perception in hunter–gatherers

In humans, voice pitch is thought to be a cue of underlying quality and an important criterion for mate choice, but data from non-Western cultures have not been provided. Here we test attributions to and preferences for voices with raised and lowered pitch in hunter–gatherers. Using a forced-choice playback experiment, we found that both men and women viewed lower pitched voices in the opposite sex as being better at acquiring resources (e.g. hunting and gathering). While men preferred higher pitched women''s voices as marriage partners, women showed no overall preference for voice pitch in men. However, women who were currently breastfeeding had stronger preferences for higher pitched male voices whereas women not currently breastfeeding preferred lower pitched voices. As testosterone is considered a costly signal associated with dominance, heritable immunity to infection and low paternal investment, women''s preferences potentially reflect a trade-off between securing good genes and paternal investment. Men''s preferences for higher pitched female voices are probably due to an evolved preference for markers of fecundity, reflected in voice pitch.     

Infidelity,jealousy, and wife abuse among Tsimane forager–farmers: testing evolutionary hypotheses of marital conflict

The role of men's jealousy over a wife's infidelity in precipitating marital conflict and wife abuse is well documented. The role of women's jealousy over a husband's infidelity has received little attention, which is puzzling given high potential costs to women of withdrawal of paternal investment. We address this gap by investigating marital conflict and wife abuse among Tsimane forager–farmers of Bolivia. We test predictions derived from male jealousy and paternal disinvestment hypotheses, which consider threats and consequences of infidelity by women (male jealousy hypothesis) and men (paternal disinvestment hypothesis). The paternal disinvestment hypothesis proposes that wife abuse is employed by husbands to limit wives' mate retention effort and maintain men's opportunities to pursue extrapair sexual relationships. Interviews were conducted among husbands and wives in the same marriages using a combination of open-ended and structured items. Spouses agree that the most frequently reported type of marital argument is women's jealousy over a husband's infidelity (N=266 arguments). Roughly 60% of abusive events occurred during arguments over men's diversion of household resources (N=124 abusive events). In multivariate analyses, likelihood of wife abuse is greater in marriages where husbands have affairs, where wives are younger, and where spouses spend more time apart (N=60 husbands, 71 wives). While we find strong support for both male jealousy and paternal disinvestment hypotheses, it is men's infidelity, not women's, that precipitates most instances of marital conflict and wife abuse. We conclude that men's aggression towards their wives facilitates men's diversion of family resources for their selfish interests.     

The effect of maternal and paternal immune challenge on offspring immunity and reproduction in a cricket

Trans‐generational immune priming is the transmission of enhanced immunity to offspring following a parental immune challenge. Although within‐generation increased investment into immunity demonstrates clear costs on reproductive investment in a number of taxa, the potential for immune priming to impact on offspring reproductive investment has not been thoroughly investigated. We explored the reproductive costs of immune priming in a field cricket, Teleogryllus oceanicus. To assess the relative importance of maternal and paternal immune status, mothers and fathers were immune‐challenged with live bacteria or a control solution and assigned to one of four treatments in which one parent, neither or both parents were immune‐challenged. Families of offspring were reared to adulthood under a food‐restricted diet, and approximately 10 offspring in each family were assayed for two measures of immunocompetence. We additionally quantified offspring reproductive investment using sperm viability for males and ovary mass for females. We demonstrate that parental immune challenge has significant consequences for the immunocompetence and, in turn, reproductive investment of their male offspring. A complex interaction between maternal and paternal immune status increased the antibacterial immune response of male offspring. This increased immune response was associated with a reduction in son's sperm viability, implicating a trans‐generational resource trade‐off between investment into immunocompetence and reproduction. Our data also show that these costs are sexually dimorphic, as daughters did not demonstrate a similar increase in immunity, despite showing a reduction in ovary mass.     

Control of parental investment changes plastically over time with residual reproductive value

Evolutionary conflict between parents and offspring over parental resource investment is a significant selective force on the traits of both parents and offspring. Empirical studies have shown that for some species, the amount of parental investment is controlled by the parents, whereas in other species, it is controlled by the offspring. The main difference between these two strategies is the residual reproductive value of the parents or opportunities for future reproduction. Therefore, this could explain the patterns of control of parental investment at the species level. However, the residual reproductive value of the parents will change during their lifetime; therefore, parental influence on the amount of investment can be expected to change plastically. Here, we investigated control of parental investment when parents were young and had a high residual reproductive value, compared to when they were old and had a low residual reproductive value using a cross‐fostering experiment in the burying beetle Nicrophorus quadripunctatus. We found that parents exert greater control over parental investment when they are young, but parental control is weakened as the parents age. Our results demonstrate that control of parental investment is not fixed, but changes plastically during the parent's lifetime.     

Male feeding contribution facilitates multiple brooding in a biparental songbird

Despite the cost of lost mating opportunities, biparental care is routinely observed across different groups of animals. Theory predicts that paternal care will increase reproductive success, yet many empirical studies have failed to find a direct link. Most studies have focused on the effect of paternal care on current breeding attempts, but male contributions may benefit future reproduction. Species producing clutches or litters more than once per season (i.e. multiple breeding attempts per season) are suitable for investigating whether paternal care contributes to current or future reproductive success, or both. We investigated the importance of the male's feeding contribution to multiple brooding in Japanese Tits Parus minor in northern Japan, where approximately 50% of pairs were known to reproduce multiple times within a breeding season. Male feeding contribution (proportion of provisioning delivered by the male) was positively correlated with the probability of the female multiple brooding and with nestling body mass. However, it was not correlated with fledging success in the current breeding attempt. Our results demonstrate the importance of male parental care for annual reproductive success in this multi‐brooded species and provide insights into the evolution of biparental care.     

A Novel Quantitative Approach to Women’s Reproductive Strategies

The patterned way in which individuals allocate finite resources to various components of reproduction (e.g. mating effort, reproductive timing and parental investment) is described as a reproductive strategy. As energy is limited, trade-offs between and within aspects of reproductive strategies are expected. The first aim of this study was to derive aspects of reproductive strategies using complete reproductive histories from 718 parous Western Australian women. Factor analysis using a subset of these participants resulted in six factors that represented ‘short-term mating strategy’, ‘early onset of sexual activity’, ‘reproductive output’, ‘timing of childbearing’, ‘breastfeeding’, and ‘child spacing’. This factor structure was internally validated by replication using a second independent subset of the data. The second aim of this study examined trade-offs between aspects of reproductive strategies derived from aim one. Factor scores calculated for each woman were incorporated in generalised linear models and interaction terms were employed to examine the effect of mating behaviour on the relationships between reproductive timing, parental investment and overall reproductive success. Early sexual activity correlates with early reproductive onset for women displaying more long-term mating strategies. Women with more short-term mating strategies exhibit a trade-off between child quantity and child quality not observed in women with a long-term mating strategy. However, women with a short-term mating strategy who delay reproductive timing exhibit levels of parental investment (measured as breastfeeding duration per child) similar to that of women with long-term mating strategies. Reproductive delay has fitness costs (fewer births) for women displaying more short-term mating strategies. We provide empirical evidence that reproductive histories of contemporary women reflect aspects of reproductive strategies, and associations between these strategic elements, as predicted from life history theory.     

Differential Allocation by Female Zebrafish (Danio rerio) to Different-Sized Males – An Example in a Fish Species Lacking Parental Care

Organisms allocate resources to reproduction in response to the costs and benefits of current and future reproductive opportunities. According to the differential allocation hypothesis, females allocate more resources to high-quality males. We tested whether a fish species lacking parental care (zebrafish, Danio rerio) expresses male size-dependent differential allocation in monogamous spawning trials. In addition, we tested whether reproductive allocation by females is affected by previous experience of different-quality males, potentially indicating plasticity in mate choice. To that end, females were conditioned to large, small or random-sized males (controls) for 14 days to manipulate females'' expectations of the future mate quality. Females showed a clear preference for large males in terms of spawning probability and clutch size independent of the conditioning treatment. However, when females experienced variation in male size (random-sized conditioning treatment) they discriminated less against small males compared to females conditioned to large and small males. This might suggest that differential allocation and size-dependent sexual selection is of less relevance in nature than revealed in the present laboratory study.     

Effects of parental care on resource allocation into immune defense and buccal microbiota in mouthbrooding cichlid fishes*

Sexual dimorphism is founded upon a resource allocation trade‐off between investments in reproduction versus other life‐history traits including the immune system. In species with conventional parental care roles, theory predicts that males maximize their lifetime reproductive success by allocating resources toward sexual selection, while females achieve this through prolonging their lifespan. Here, we examine the interrelation between sexual dimorphism and parental care strategies in closely related maternal and biparental mouthbrooding cichlid fishes from East African Lake Tanganyika. We measured cellular immune parameters, examined the relative expression of 28 immune system and life history‐related candidate genes and analyzed the microbiota composition in the buccal cavity. According to our predictions, maternal mouthbrooders are more sexually dimorphic in immune parameters than biparental mouthbrooders, which has possibly arisen through a differential resource allocation into parental care versus secondary sexual traits. Biparental mouthbrooders, on the other hand, which share the costs of parental care, feature an upregulated adaptive immune response and stronger antiviral properties, while their inflammation response is reduced. Overall, our results suggest a differential resource allocation trade‐off between the two modes of parental investment.     

Women’s sexual strategies in pregnancy

Humans exhibit an unusual pattern of sexual behavior compared to other mammalian females. Women's extended sexuality has been hypothesized to be related to a variety of possible benefits, especially non-genetic reproductive benefits, such as securing male investment via reinforced pairbonds or paternity confusion. But sexual behavior also comes at a cost, particularly for pregnant women, in terms of energetic costs, potential disease, and possible harm to the fetus. We hypothesize, therefore, that sexual behavior in pregnant women should reflect adaptive strategies and that pregnant women will be particularly strategic about their sexual behavior in order to maximize potential benefits while minimizing potential costs. One hundred twelve pregnant women completed a survey of their partners' qualities and their sexual desires toward their primary partners and men other than their primary partners. Results showed that women's perceptions of relationship threat positively predicted sexual desire for primary partners, while their perceptions of their partner's investing qualities negatively predicted sexual desire for extra-pair mates. These qualities, as well as cues to partner's genetic quality and gestation age, also interacted in ways that suggest that pregnant women's sexual desires are sensitive to cues of future investment and relationship stability.     

Women's health. The childbearing years and after.

Health and development planners have tended to see women primarily in context of their reproductive role. As a result, solutions to women''s health needs have been restricted to expanding and improving maternal and child health systems. There has recently been a major shift in direction, largely because of the influence of the world conference on population and development held in Cairo in 1994. Dr Guiseppe Benagiano, director of the special programme of research, development and research training in human reproduction based at the WHO, says, "We need to remind ourselves constantly that reproductive health is not simply a biomedical issue but one with serious implications for our general health and by extension, for all our efforts in human social and economic development." The 1993 world development report on health identified the lack of a clear strategy for engaging women in health care and suggested that child health services, prenatal care, treatment of sexually transmitted diseases, and family planning services should be provided jointly at convenient times. In an example of this, the Chilean Institute of Reproductive Medicine now offers integrated family planning services at the same time as child health services, and Thailand is experimenting with mobile health clinics to reach women in their homes. As the proportion of elderly women increases, old age is increasingly being seen as a female issue. With the impact of urbanisation and industrialisation, more of these women are living isolated lives, often suffering from chronic debilitating diseases. In his opening statement to the global commission on women''s health in April 1995 which focused on health conditions of women in old age, Dr Hiroshi Nakajima, the WHO''s director general, said: "Our goal should not be solely to extend lives in the physical sense, but to ensure that the added years are worth living."     

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.     

Paternity cues and mating opportunities: what makes fathers good?

Human males provide facultative paternal investment to their offspring; that is, the male care is not necessary for the survival of his offspring. It is expected that the degree of male investment (1) increases with growing paternity certainty, (2) increases when investment increases the survival and later reproductive prospect of offspring and (3) declines when there are opportunities to mate with multiple females. Using a large sample of adult offspring and their fathers (n = 245), we first investigated the role of two factors possibly involved in the assessment of paternity and subsequently regulating the level of paternal investment: (a) father–child facial resemblance and (b) assortative mating for eye colour. Second, because mating opportunities are inversely related to paternal investment, we also investigated how male facial attractiveness (a cue of mate opportunities) correlates with paternal investment. In line with paternal investment theory, male investment positively correlated with offspring facial resemblance. However, paternal investment were neither higher among blue-eyed couples, nor there were preferences of blue-eyed men to marry with blue-eyed women. Moreover, father facial attractiveness was unrelated to paternal investment. These results indicate that resemblance between offspring and their fathers still plays an important role in paternal investment decision later in offspring’s life.     

A female's past experience with predators affects male courtship and the care her offspring will receive from their father

Differential allocation occurs when individuals adjust their reproductive investment based on their partner''s traits. However, it remains unknown whether animals differentially allocate based on their partner''s past experiences with predation risk. If animals can detect a potential mate''s experience with predators, this might inform them about the stress level of their potential mate, the likelihood of parental effects in offspring and/or the dangers present in the environment. Using threespined stickleback (Gasterosteus aculeatus), we examined whether a female''s previous experience with being chased by a model predator while yolking eggs affects male mating effort and offspring care. Males displayed fewer conspicuous courtship behaviours towards females that had experienced predation risk in the past compared with unexposed females. This differential allocation extended to how males cared for the resulting offspring of these matings: fathers provided less parental care to offspring of females that had experienced predation risk in the past. Our results show for the first time, to our knowledge, that variation among females in their predator encounters can contribute to behavioural variation among males in courtship and parental care, even when males themselves do not encounter a predator. These results, together with previous findings, suggest that maternal predator exposure can influence offspring development both directly and indirectly, through how it affects father care.     

Stress promotes changes in resource allocation to growth and reproduction in a simultaneous hermaphrodite with indeterminate growth

In iteroparous animals, investment in growth is compromised by investment in reproduction, especially in species with indeterminate growth. Life‐history theory predicts that growth should be favoured over reproduction, assuming size‐related fecundity or survival. Hence, increase body condition represents an increase in reproductive potential. Simultaneous hermaphrodites should adjust their resource allocation to each sex function in response to current conditions but, recently, it has been suggested that, in hermaphrodites, gender allocation should be considered as a three‐way trade‐off, including the investment in somatic growth. Due to the higher costs involved, the female function is affected to a greater extent by environmentally stressful conditions rather than the male function. To examine this, we induced stress in the hermaphroditic earthworm Eisenia fetida (Savigny, 1826) and looked for changes in resource allocation in nonreproductive and reproductive individuals. Experimental stress was induced by using tweezers to elicit contractile escape movements. We predicted that stressed earthworms would preferentially allocate resources to growth. In nonreproductive individuals, however, stress had a negative effect on growth, although weight recovery was rapid once manipulation ceased, indicating the importance of body condition, as well as the existence of mechanisms of compensatory growth for growth trajectories in this earthworm species. The response of reproductive individuals was consistent with our expectation: (1) stressed worms maintained their growth rate at the expense of current reproduction and (2) stressed earthworms laid 25% fewer cocoons, which were 30% lighter than cocoons laid by control earthworms. The present results suggest that E. fetida regulates its reproductive effort and that future reproduction has more impact on its fitness than current reproduction. The trade‐off between current and future reproduction should be taken into consideration in models of sex allocation in simultaneous hermaphrodites. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91 , 593–600.     

Sex differences in life history drive evolutionary transitions among maternal,paternal, and bi‐parental care

Evolutionary transitions among maternal, paternal, and bi‐parental care have been common in many animal groups. We use a mathematical model to examine the effect of male and female life‐history characteristics (stage‐specific maturation and mortality) on evolutionary transitions among maternal, paternal, and bi‐parental care. When males and females are relatively similar – that is, when females initially invest relatively little into eggs and both sexes have similar mortality and maturation – transitions among different patterns of care are unlikely to be strongly favored. As males and females become more different, transitions are more likely. If females initially invest heavily into eggs and this reduces their expected future reproductive success, transitions to increased maternal care (paternal → maternal, paternal → bi‐parental, bi‐parental → maternal) are favored. This effect of anisogamy (i.e., the fact that females initially invest more into each individual zygote than males) might help explain the predominance of maternal care in nature and differs from previous work that found no effect of anisogamy on the origin of different sex‐specific patterns of care from an ancestral state of no care. When male mortality is high or male egg maturation rate is low, males have reduced future reproductive potential and transitions to increased paternal care (maternal → paternal, bi‐parental → paternal, maternal → bi‐parental) are favored. Offspring need (i.e., low offspring survival in the absence of care) also plays a role in transitions to paternal care. In general, basic life‐history differences between the sexes can drive evolutionary transitions among different sex‐specific patterns of care. The finding that simple life‐history differences can alone lead to transitions among maternal and paternal care suggests that the effect of inter‐sexual life‐history differences should be considered as a baseline scenario when attempting to understand how other factors (mate availability, sex differences in the costs of competing for mates) influence the evolution of parental care.     

A cost of maternal care in the dung beetle Onthophagus taurus?

Parental care theory assumes that investment in current offspring will trade against future investment. A number of field studies on birds have used clutch size manipulations to demonstrate a survival cost to chick rearing. However, such studies do not account for costs accrued during earlier stages of reproduction because not all aspects of reproductive effort are manipulated by varying the number of nestlings. In this study, we investigate the effect of reproductive effort on female survival in the dung beetle, Onthophagus taurus. By experimentally manipulating mating status and dung availability, we demonstrate that virgin females survive longer than mated females and that the survival of mated females was negatively associated with the number of brood masses produced. Using a novel manipulation of the mating system, we separated the effects of egg production and maternal care on female survival. Previously, we have shown that females provisioning with the assistance of a major male provide relatively less care than unassisted females. However, paternal assistance did not alter the number of brood masses produced and hence the amount of reproductive effort that was allocated to egg production. Therefore, our finding that female survival was increased when receiving paternal assistance provides, to our knowledge, the first definitive evidence that maternal care reduces female lifespan. These results are of major importance to theoretical models on the evolution of parental care.     

Intelligence and mate choice: intelligent men are always appealing

What role does a man's intelligence play in women's mate preferences? Selecting a more intelligent mate often provides women with better access to resources and parental investment for offspring. But this preference may also provide indirect genetic benefits in the form of having offspring who are in better physical condition, regardless of parental provisioning. Intelligence then may serve as both a cue of a mate's provisioning abilities and his overall heritable phenotypic quality. In the current study, we examined the role of a man's intelligence in women's long- and short-term mate preferences. We used a rigorous psychometric measure (men's WAIS scores) to assess intelligence (the first study to our knowledge), in addition to women's subjective ratings to predict mate appeal. We also examined the related trait of creativity, using women's ratings as a first step, to assess whether creativity could predict mate appeal, above and beyond intelligence. Finally, we examined whether preferences for intelligent and creative short-term mates shifted according to a woman's conception risk. Multilevel modeling was used to identify predictors of mate appeal. Study participants (204 women) assessed the long- and short-term mate appeal of videos of 15 men with known measures of intelligence performing verbal and physical tasks. Findings indicate that both intelligence and creativity independently predicted mate appeal across mating contexts, but no conception-risk effects were detected. We discuss implications of these findings for the role of intelligence and creativity in women's mate choices.