PATERNAL CONDITION DRIVES PROGENY SEX‐RATIO BIAS IN A LIZARD THAT LACKS PARENTAL CARE

Sex‐allocation theory predicts that females in good condition should preferentially produce offspring of the sex that benefits the most from an increase in maternal investment. However, it is generally assumed that the condition of the sire has little effect on progeny sex ratio, particularly in species that lack parental care. We used a controlled breeding experiment and molecular paternity analyses to examine the effects of both maternal and paternal condition on progeny sex ratio and progeny fitness in the brown anole (Anolis sagrei), a polygynous lizard that lacks parental care. Contrary to the predictions of sex‐allocation theory, we found no relationship between maternal condition and progeny sex ratio. By contrast, progeny sex ratio shifted dramatically from female‐biased to male‐biased as paternal condition increased. This pattern was driven entirely by an increase in the production of sons as paternal condition improved. Despite strong natural selection favoring large size and high condition in both sons and daughters, we found no evidence that progeny survival was related to paternal condition. Our results emphasize the importance of considering the paternal phenotype in studies of sex allocation and highlight the need for further research into the pathways that link paternal condition to progeny fitness.     

The life-history trade-off between fertility and child survival

Evolutionary models of human reproduction argue that variation in fertility can be understood as the local optimization of a life-history trade-off between offspring quantity and ‘quality’. Child survival is a fundamental dimension of quality in these models as early-life mortality represents a crucial selective bottleneck in human evolution. This perspective is well-rehearsed, but current literature presents mixed evidence for a trade-off between fertility and child survival, and little empirical ground to evaluate how socioecological and individual characteristics influence the benefits of fertility limitation. By compiling demographic survey data, we demonstrate robust negative relationships between fertility and child survival across 27 sub-Saharan African countries. Our analyses suggest this relationship is primarily accounted for by offspring competition for parental investment, rather than by reverse causal mechanisms. We also find that the trade-off increases in relative magnitude as national mortality declines and maternal somatic (height) and extrasomatic (education) capital increase. This supports the idea that socioeconomic development, and associated reductions in extrinsic child mortality, favour reduced fertility by increasing the relative returns to parental investment. Observed fertility, however, falls considerably short of predicted optima for maximizing total offspring survivorship, strongly suggesting that additional unmeasured costs of reproduction ultimately constrain the evolution of human family size.     

Transmission of parental care behavior in African striped mice, Rhabdomys Pumilio

The expression of behavior, including parental care behavior, is influenced by complex interactions of the genes of an organism and the prevailing environmental conditions. Previously, we showed that the development of paternal, but not maternal, care in the African striped mouse, Rhabdomys pumilio, has a significant nongenetic maternal component. Here, we investigate the genetic component of parental care behavior from parents to offspring. We first measured the duration of parental care behavior of mothers and fathers every second day for 11 days postnatally. Subsequently, one son and one daughter from each of these litters were paired with unrelated mates when they were adults and their parental care behavior scored. Using regression models, we then compared parental care behavior of parents and their adult offspring. The transmission of parental care behavior from striped mouse fathers to sons and from mothers to both sons and daughters did not indicate a genetic component. Instead, we found a patrilineal genetic component for parental care in daughters. The reason for this unusual pattern of inheritance is not known, but this finding complements that of our other studies, showing that the expression of maternal care behavior in adult daughters is also not nongenetically influenced by their mothers. We suggest that, although females are constrained to provide maternal care in different social contexts, maternal care behavior may be influenced genetically by the father.     

When it is costly to have a caring mother: food limitation erases the benefits of parental care in earwigs

The aggregation of parents with offspring is generally associated with different forms of care that improve offspring survival at potential costs to parents. Under poor environments, the limited amount of resources available can increase the level of competition among family members and consequently lead to adaptive changes in parental investment. However, it remains unclear as to what extent such changes modify offspring fitness, particularly when offspring can survive without parents such as in the European earwig, Forficula auricularia. Here, we show that under food restriction, earwig maternal presence decreased offspring survival until adulthood by 43 per cent. This effect was independent of sibling competition and was expressed after separation from the female, indicating lasting detrimental effects. The reduced benefits of maternal presence on offspring survival were not associated with higher investment in future reproduction, suggesting a condition-dependent effect of food restriction on mothers and local mother-offspring competition for food. Overall, these findings demonstrate for the first time a long-term negative effect of maternal presence on offspring survival in a species with maternal care, and highlight the importance of food availability in the early evolution of family life.     

The quantitative genetic basis of offspring solicitation and parental response in a passerine bird with biparental care.

The coevolution of parental investment and offspring solicitation is driven by partly different evolutionary interests of genes expressed in parents and their offspring. In species with biparental care, the outcome of this conflict may be influenced by the sexual conflict over parental investment. Models for the resolution of such family conflicts have made so far untested assumptions about genetic variation and covariation in the parental resource provisioning response and the level of offspring solicitation. Using a combination of cross-fostering and begging playback experiments, we show that, in the great tit (Parus major), (i) the begging call intensity of nestlings depends on their common origin, suggesting genetic variation for this begging display, (ii) only mothers respond to begging calls by increased food provisioning, and (iii) the size of the parental response is positively related to the begging call intensity of nestlings in the maternal but not paternal line. This study indicates that genetic covariation, its differential expression in the maternal and paternal lines and/or early environmental and parental effects need to be taken into account when predicting the phenotypic outcome of the conflict over investment between genes expressed in each parent and the offspring.     

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.     

Parental investment and the optimization of human family size

Human reproductive behaviour is marked by exceptional variation at the population and individual level. Human behavioural ecologists propose adaptive hypotheses to explain this variation as shifting phenotypic optima in relation to local socioecological niches. Here we review evidence that variation in fertility (offspring number), in both traditional and modern industrialized populations, represents optimization of the life-history trade-off between reproductive rate and parental investment. While a reliance on correlational methods suggests the true costs of sibling resource competition are often poorly estimated, a range of anthropological and demographic studies confirm that parents balance family size against offspring success. Evidence of optimization is less forthcoming. Declines in fertility associated with modernization are particularly difficult to reconcile with adaptive models, because fertility limitation fails to enhance offspring reproductive success. Yet, considering alternative measures, we show that modern low fertility confers many advantages on offspring, which are probably transmitted to future generations. Evidence from populations that have undergone or initiated demographic transition indicate that these rewards to fertility limitation fall selectively on relatively wealthy individuals. The adaptive significance of modern reproductive behaviour remains difficult to evaluate, but may be best understood in response to rising investment costs of rearing socially and economically competitive offspring.     

Effects of neonatal paternal deprivation or early deprivation on anxiety and social behaviors of the adults in mandarin voles

This study examined whether neonatal paternal deprivation (PD: father was removed and pups were raised just by mother) or early deprivation (ED: pups were raised by both parents except separated from not only the dam but also the peers for three hours a day from PND 0 to 13) has long-term effects on anxiety and social behaviors of adult mandarin voles. Newborn mandarin voles of F2 generation were randomly assigned to one of three groups: bi-parental care (PC: pups were raised by both parents), PD and ED. The parental care behaviors of F1 generation were observed at the age of 0, 13 and 21 days (PND 0, 13, 21) of F2 generation of PC and PD groups. Moreover, each mandarin vole of F2 generation received an open field test and a social interaction test on PND 70 and PND 75, respectively. No significant differences of parental behavior were observed between mothers and fathers from PC families, showing typical parental behavior of socially monogamous rodents. In addition, no significant differences of maternal behaviors were found between mothers from PC and PD families, indicating no maternal compensation towards pups for the absence of the paternal care. In the open field test, mandarin voles from both PD and ED families displayed higher levels of anxiety and lower locomotor activity, relative to offspring of PC family. In the social interaction test, both PD and ED mandarin voles also showed lower levels of social behavior and higher levels of anxiety. Thus, both PD and ED significantly increase anxiety and reduce social behavior of adult mandarin voles, suggesting that variation in parental investment may lead to variation in anxiety and social behaviors in rodents with different mating systems.     

Parentally biased favouritism: why should parents specialize in caring for different offspring?

'Parentally biased favouritism' occurs when the two parents differentially care for individual offspring or kinds of offspring. Examples in birds include brood division and differential investment by the two parents in relation to the size or sex of the offspring. This paper uses mathematical models to investigate which ideas can, in theory, explain parentally biased favouritism. One previous explanation is that the parents differ in their cost of reproduction and that the parent who consequently invests least concentrates its care on the more valuable offspring. However, a mathematical model predicts the total care given by each parent and received by each offspring, not how much each parent cares for each offspring, and hence does not explain parentally biased favouritism. Parentally biased favouritism towards particular types of offspring can be explained by a difference between the parents in the benefits of caring for a given type of offspring or in the effort incurred in providing care to a given type of offspring, but then it is extreme, with at least one of the parents providing care to only one type of offspring. Parentally biased favouritism towards particular individual offspring (brood division) can be explained by parent-offspring conflict or sexual conflict.     

The effect of paternal investment on female fertility intention in South Korea

Life history theory views reproduction as an outcome of resource allocation. The allocation of resources such as parental investments of time, energy and material resources involves trade-offs between number of offspring and timing of reproduction. Within the framework of mammalian parental investment, the outstanding feature of human reproduction is the high level of paternal care. Although empirical evidence suggests that human paternal investment may have evolved as a reproductive strategy to reduce infant and child mortality rates, the effects of actual paternal investment, including allocating time to child care, on female reproductive decisions have received relatively little attention. We examined the trade-off from two perspectives using a representative sample of married South Korean women aged 20–44 in 2005 (n=977). First, paternal investment in domestic labor, including child care and housework, was expected to be associated with women's preference regarding future reproduction. Second, relative paternal investment was expected to increase women's preference for future reproduction, especially among employed women. We found that increased paternal investment in child care and housework remarkably enhanced women's intention to have a second child, especially among employed women. In addition, although family members provide a low percentage of child care in South Korea, such help is likely to be a useful resource for second childbirth among employed women. Somewhat expectedly, older age and longer time since first birth had negative effects on women's second-child intention. There is growing evidence that, in the lowest fertility societies, paternal investment may be an essential resource for promoting future reproductive behavior of women, especially employed women.     

Devoted fathers or selfish lovers? Conflict between mating effort and parental care in a harem‐defending arachnid

When there is a temporal trade‐off between mating effort and parental care, theoretical models predict that intense sexual selection on males leads to reduced paternal care. Thus, high‐quality males should invest more in mating effort because they have higher chances of acquiring mates, whereas low‐quality males should bias their investment towards parental care. Once paternal care has evolved, offspring value should also influence males’ decisions to invest in offspring attendance. Here, we performed a manipulation under field conditions to investigate the factors that influence male allocation in either mating effort or parental care. We predicted that facultative paternal care in the harem‐holding harvestman Serracutisoma proximum would be negatively influenced by male attractiveness and positively influenced by offspring value. We found that attractive males were less likely to engage in egg attendance and that the higher the perceived paternity, the higher the caring frequency. Finally, egg mortality was not related to caring frequency by males, but predation pressure was much lower than that recorded in previous studies with the same population. Thus, the benefits of facultative male care may be conditional to temporal variation in the intensity of egg predation. In conclusion, males adjust their investment in either territory defence or egg attendance according to their recent mating history and perceived paternity. Our findings suggest that exclusive paternal care can evolve from facultative paternal care only if the trade‐off between mating effort and parental care is circumvented.     

The evolution of indicator traits for parental quality: the role of maternal and paternal effects

In systems where individuals provide material resources to their mates or offspring, mate choice based on traits that are phenotypically correlated with the quality of resources provided is expected to be adaptive. Several models have explored the evolution of mating preference where there are direct benefits to choice, but few have addressed how a phenotypic correlation can be established between a male indicator trait and the degree of parental investment. We present a model with three quantitative traits: male and female parental investment and a potential male indicator trait. In our model, the expression of the "indicator" trait in offspring is affected by parental investment. These effects are referred to as maternal or paternal effects, or as "indirect genetic effects" when parental investment is heritable. With genetic variation for degree of parental investment, offspring harbor genes for parental investment that are unexpressed before mating but will affect the investment that they provide when expressed. Because the investment received from the parents affects the expression of the indicator trait, there will be a correlation between the genes for parental investment inherited and the degree of expression of the indicator trait in the offspring. The indicator trait is thus an "honest" signal for the degree of paternal investment.     

Are men really that bad as fathers? The role of men's investments

Human pair-bonding and paternal involvement have long been attributed to the need for biparental rearing of altricial offspring with extended periods of dependency. More recently, researchers have focused on the fertility benefits that pair-bonding offers men and have re-conceptualized paternal care as a stratagem designed to curry favor with the recipient children's mother. These models, however, fail to explain a number of puzzling empirical findings, namely the lack of a significant and robust effect of father-presence cross-culturally, despite what appears to be true paternal involvement. I argue that the record is better explained by conceptualizing reproduction within unions as a joint venture, in which men's contributions are not simply lumped onto women's invariant levels of parental investment, but one in which men's involvement allows wives to reduce their own allocations to parental investment and increase those to fertility (fertility model), thereby maximizing the production of the union, not simply child survivorship.     

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.     

Recognition of Young in A Colonially Nesting Bird

Parents ought to restrict costly parental care to their genetic offspring and, particularly when the risk of misdirecting care is high, parent‐offspring recognition may evolve. I tested whether adult cave swallows, which nest in dense colonies and feed fledglings in mixed‐family groups, discriminate against unrelated young, using temporary chick transfers at two nestling ages and a cross‐fostering experiment. Temporary chick transfers indicated that parents bias feedings toward their own offspring near fledging (18 d) but not at about halfway through the nesting period (10 d). I also examined how parents learn to identify their offspring by cross‐fostering young 3 d after hatching and testing parental response 2 wks later. Adults did not favor their own offspring over unrelated nestlings when both were unfamiliar to the focal parents. However, when parents encountered two of their own offspring, one of which was reared by foster parents, they preferentially fed the familiar nestling. By recognizing young, cave swallow parents reduce some risks of misdirected parental investment (mobile fledglings) but not others (extra‐pair young and intraspecific brood parasitism).     

Quantitative genetics of growth and development time in the burying beetle Nicrophorus pustulatus in the presence and absence of post-hatching parental care

Despite a growing interest in the evolutionary aspects of maternal effects, few studies have examined the genetic consequences of maternal effects associated with parental care. To begin to provide data on nonlaboratory or nondomestic animals, we compared the effect of presence and absence of parental care on phenotype expression of larval mass and development time at different life-history stages in the burying beetle Nicrophorus pustulatus. This beetle has facultative care; parents can feed their larvae through regurgitation of digested carrion or offspring can feed by themselves from previously prepared carrion. To investigate larval responses to these two levels of care, including estimates of additive genetic effects, maternal effects, and genotype-by-environment interactions, we used a half-sibling split-family breeding experiment-raising half of the offspring of a family in the presence of their mother and the other half without their mother present. Larvae reared with their mother present were on average heavier and developed faster, although some of the differences in development decreased or were eliminated by the adult stage. These results suggest that presence or absence of post-hatching maternal care plays an important role in phenotype expression early in life, whereas later the phenotype of the offspring is determined mainly by the genotype and/or unshared environmental effects. Our study also permitted us to examine the differences in genetic effects between the two care environments. Heritabilities, maternal/common environment effect, and most genetic correlations did not differ between the care treatments. Genetic analyses revealed substantial additive genetic effects for development time but small effects for measures of body mass. Maternal plus common environment effects were high for measures of mass but low for development time, suggesting that indirect genetic effects of maternal and/or common environment are less important for the evolution of development time than for mass. Estimates of genetic correlations revealed a trade-off between the duration of the two development stages after the offspring left the carrion. There was also a negative genetic correlation between the time spent on carrion and the mass at 72 h, when mothers usually stop feeding. The analysis of genotype-by-environment interactions indicates substantial variation among maternal families in response to care. Presence or absence of parental care may therefore contribute to the additive genetic variance through its interaction with the maternal component of the additive genetic variance. The presence of this interaction further suggests that parents may vary in care strategies, with some parents dispersing after preparation of the carrion and some parents staying with the larvae. This interaction may help maintain genetic variation in growth, development time, and parental care behavior. Additional work is needed, however, to quantify indirect genetic effects and genetic variation in parental care behavior itself.     

Non-genomic transmission of paternal behaviour between fathers and sons in the monogamous and biparental California mouse

Maternal behaviour has profound, long-lasting implications for the health and well-being of developing offspring. In the monogamous California mouse (Peromyscus californicus), care by both parents is critical for offspring survival. We tested the hypothesis that similar to maternal care in rodents, paternal huddling and grooming (HG) behaviour can be transmitted to future generations via behavioural mechanisms. In California mice, testosterone maintains paternal HG behaviour. In the present study, we randomly assigned a group of male California mice to castration or sham-operated conditions and allowed them to raise their offspring normally. Adult sons of these males were paired with a female, and they were observed interacting with their own offspring. We found that like their fathers, the sons of castrated males huddled and groomed their young at lower levels than the sons of sham-operated fathers. The sons of castrates also retrieved pups more frequently. When both parents were present, the sons of castrates also showed a trend towards engaging in less exploratory behaviour. These data support the hypothesis that paternal behaviour, like maternal behaviour, can be transferred to future generations via epigenetic mechanisms and suggest that in a biparental species both parents contribute to offspring behavioural development.     

Sex differences in parental care: Gametic investment,sexual selection,and social environment

Male and female parents often provide different type and amount of care to their offspring. Three major drivers have been proposed to explain parental sex roles: (1) differential gametic investment by males and females that precipitates into sex difference in care, (2) different intensity of sexual selection acting on males and females, and (3) biased social environment that facilitates the more common sex to provide more care. Here, we provide the most comprehensive assessment of these hypotheses using detailed parental care data from 792 bird species covering 126 families. We found no evidence for the gametic investment hypothesis: neither gamete sizes nor gamete production by males relative to females was related to sex difference in parental care. However, sexual selection correlated with parental sex roles, because the male share in care relative to female decreased with both extra‐pair paternity and frequency of male polygamy. Parental sex roles were also related to social environment, because male parental care increased with male‐biased adult sex ratios (ASRs). Taken together, our results are consistent with recent theories suggesting that gametic investment is not tied to parental sex roles, and highlight the importance of both sexual selection and ASR in influencing parental sex roles.     

The effect of maternal and paternal environments on seed characters in the herbaceous plant Campanula Americana (Campanulaceae)

Maternal environments typically influence the phenotype of their offspring. However, the effect of the paternal environment or the potential for joint effects of both parental environments on offspring characters is poorly understood. Two populations of Campanula americana, a woodland herb with a variable life history, were used to determine the influence of maternal and paternal light and nutrient environments on offspring seed characters. Families were grown in the greenhouse in three levels of light or three levels of nutrients. Crosses were conducted within each environmental gradient to produce seeds with all combinations of maternal and paternal environments. On average, increasing maternal nutrient and light levels increased seed mass and decreased percentage germination. The paternal environment affected seed mass, germination time, and percentage germination. However, the influence of the paternal environment varied across maternal environments, suggesting that paternal environmental effects should be evaluated in the context of maternal environments. Significant interactions between family and the parental environments for offspring characters suggest that parental environmental effects are genetically variable. In C. americana, the timing of germination determines life history. Therefore parental environmental effects on germination timing, and genetic variation in those parental effects, suggest that parental environments may influence life history evolution in this system.     

Paternal Effects on Offspring Fitness Reflect Father’s Social Environment

In many species, males influence phenotypic traits in their offspring through non-genetic paternal effects. Such effects can represent a form of paternal investment, and males may benefit by adjusting the effects depending on environmental parameters, such as operational sex ratio, so as to maximize offspring fitness. In the neriid fly Telostylinus angusticollis, fathers reared on a nutrient-rich larval diet produce larger offspring, independent of the rearing environment of the offspring. Here we asked whether this paternal effect was influenced by the social environment to which fathers were exposed. We found significant interactions of the effects of paternal larval diet quality and social environment (same-sex vs. mixed-sex groups) on offspring fitness-related traits. Fathers reared on a nutrient-rich diet produced larger male offspring when housed in mixed-sex groups. However, fathers reared on a nutrient-rich diet produced more viable offspring (or more viable sperm) when housed in same-sex groups prior to mating. These results suggest that fitness-enhancing paternal effects can trade off, consistent with parental investment theory on the offspring size-number trade-off, which suggests that these traits represent alternative investment options and parents are selected to optimize the balance based on a range of environmental variables. This is the first study to show that males can facultatively modulate paternal effects based on the social environment.