What happens to offspring when parents are inbred,old or had a poor start in life? Evidence for sex‐specific parental effects

Parental effects on offspring performance have been attributed to many factors such as parental age, size and condition. However, we know little about how these different parental characteristics interact to determine parental effects, or the extent to which their effect on offspring depends on either the sex of the parent or that of the offspring. Here we experimentally tested for effects of variation in parents’ early diet and inbreeding levels, as well as effects of parental age, and for potential interactive effects of these three factors on key aspects of offspring development in the mosquitofish (Gambusia holbrooki). Older mothers produced offspring that were significantly smaller at birth. This negative effect of maternal age on offspring size was still evident at maturation as older mothers had smaller daughters, but not smaller sons. The daughters of older mothers did, however, reach maturity sooner. Paternal age did not affect offspring body size, but it had a complex effect on their sons’ relative genital size. When initially raised on a food‐restricted diet, older fathers sired sons with relatively smaller genitalia, but when fathers were initially raised on a control diet their sons had relatively larger genitalia. The inbreeding status of mothers and fathers had no significant effects on any of the measured offspring traits. Our results indicate that the manifestation of parental effects can be complex. It can vary with both parent and offspring sex; can change over an offspring's life; and is sometimes evident as an interaction between different parental traits. Understanding this complexity will be important to predict the role of parental effects in adaptation.     

Maternal inheritance and rapid evolution of sexual size dimorphism: passive effects or active strategies?

Adaptive evolution is often strongly influenced by maternal inheritance that transfers the parental strategies across generations. The consequences of maternal effects for the offspring generation depend on the between-generation similarity in environments and on the evolved sensitivity of the offspring's ontogeny to maternal effects. When these factors differ between sons and daughters, maternal effects can influence the evolution of sexual dimorphism. The establishment of house finch populations across western Montana during the last 30 years was accompanied by rapid evolutionary change in sexual size dimorphism. Here I show that traits that changed the most across generations were most influenced by maternal effects in males but not females. Maternal effects differentially affected sons' and daughters' survival; greater maternal effects were commonly associated with higher survival of sons, especially when maternal and offspring environments were similar. Stronger maternal effects extended preselection phenotypic variance in morphological traits of males, thereby producing some locally adaptive phenotypes and lessening juvenile mortality. Thus, the observed sex-specific maternal effects and their contribution to the evolution of sexual size dimorphism are likely a passive consequence of the distinct sensitivity of sons and daughters to maternal adaptations to breeding in ecologically distinct parts of the house finch's expanding range.     

Manipulating developmental stress reveals sex-specific effects of egg size on offspring phenotype

The general lack of experimental evidence for strong, positive effects of egg size on offspring phenotype has led to suggestions that avian egg size is a neutral trait. To better understand the functional significance of intra-specific variation in egg size as a determinant of offspring fitness within a life-history (sex-specific life-history strategies) and an environmental (poor rearing conditions) context, we experimentally increased developmental stress (via maternal feather-clipping) in the sexually size-dimorphic European starling (Sturnus vulgaris) and measured phenotypic traits in offspring across multiple biological scales. As predicted by life-history theory, sons and daughters had different responses when faced with developmental stress and variation in egg size. In response to developmental stress, small egg size in normally faster-growing sons was associated with catch-up growth prior to attaining larger adult size, resulting in a reduction in developmental stability. Daughters apparently avoided this developmental instability by reducing growth rate and eventual adult body mass and size. Interestingly, large egg size provided offspring with greater developmental flexibility under poor growth conditions. Large-egg sons and daughters avoided the reduction in developmental stability, and daughters also showed enhanced escape performance during flight trials. Furthermore, large egg size resulted in elevated immune responses for both sexes under developmental stress. These findings show that there can be significant, but complex, context-specific effects of egg size on offspring phenotype at least up to fledging, but these can only be demonstrated by appreciating variation in the quality of the offspring environment and life histories. Results are therefore consistent with egg size playing a significant role in shaping the phenotypic outcome of offspring in species that show even greater intra-specific variation in egg size than starlings.     

Sex-specific effects of the in ovo environment on early-life phenotypes in eiders

Maternal effects affect offspring phenotype and fitness. However, the roles of offspring sex-specific sensitivity to maternal glucocorticoids and sex-biased maternal investment remain unclear. It is also uncertain whether telomere length (a marker associated with lifespan) depends on early growth in a sex-specific manner. We assessed whether maternal traits including corticosterone (CORT; the main avian glucocorticoid) and in ovo growth rate are sex-specifically related to offspring CORT exposure, relative telomere length (RTL) and body condition in eiders (Somateria mollissima). We measured feather CORT (fCORT), RTL and body condition of newly hatched ducklings, and growth rate in ovo was expressed as tarsus length at hatching per incubation duration. Maternal traits included baseline plasma CORT, RTL, body condition and breeding experience. We found that fCORT was negatively associated with growth rate in daughters, while it showed a positive association in sons. Lower offspring fCORT was associated with higher maternal baseline plasma CORT, and fCORT was higher in larger clutches and in those hatching later. The RTL of daughters was negatively associated with maternal RTL, whereas that of males was nearly independent of maternal RTL. Higher fCORT in ovo was associated with longer RTL at hatching in both sexes. Duckling body condition was mainly explained by egg weight, and sons had a slightly lower body condition. Our correlational results suggest that maternal effects may have heterogeneous and even diametrically opposed effects between the sexes during early development. Our findings also challenge the view that prenatal CORT exposure is invariably associated with shorter telomeres.     

The maternal social environment shapes offspring growth,physiology, and behavioural phenotype in guinea pigs

Background

Prenatal conditions influence offspring development in many species. In mammals, the effects of social density have traditionally been considered a detrimental form of maternal stress. Now their potential adaptive significance is receiving greater attention.Sex-specific effects of maternal social instability on offspring in guinea pigs (Cavia aperea f. porcellus) have been interpreted as adaptations to high social densities, while the effects of low social density are unknown. Hence, we compared morphological, behavioural and physiological development between offspring born to mothers housed either individually or in groups during the second half of pregnancy.

Results

Females housed individually and females housed in groups gave birth to litters of similar size and sex-ratios, and there were no differences in birth weight. Sons of individually-housed mothers grew faster than their sisters, whereas daughters ofgroup-housed females grew faster than their brothers, primarily due to an effect on growth of daughters. There were few effects on offspring behaviour. Baseline cortisol levels in saliva of pups on day 1 and day 7 were not affected, but we saw a blunted cortisol response to social separation on day 7 in sons of individually-housed females and daughters of group-housed females. The effects were consistent across two replicate experiments.

Conclusions

The observed effects only partially support the adaptive hypothesis. Increased growth of daughters may be adaptive under high densities due to increasedfemale competition, but it is unclear why growth of sons is not increased under low social densities when males face less competition from older, dominant males. The differences in growth may be causally linked to sex-specific effects on cortisol response, although individual cortisol response and growth were not correlated, and various other mechanisms are possible. The observed sex-specific effects on early development are intriguing, yet the potential adaptive benefits and physiological mechanisms require further study.

     

Bigger mothers are better mothers: disentangling size-related prenatal and postnatal maternal effects

Despite a vast literature on the factors controlling adult size, few studies have investigated how maternal size affects offspring size independent of direct genetic effects, thereby separating prenatal from postnatal influences. I used a novel experimental design that combined a cross-fostering approach with phenotypic manipulation of maternal body size that allowed me to disentangle prenatal and postnatal maternal effects. Using the burying beetle Nicrophorus vespilloides as model organism, I found that a mother''s body size affected egg size as well as the quality of postnatal maternal care, with larger mothers producing larger eggs and raising larger offspring than smaller females. However, with respect to the relative importance of prenatal and postnatal maternal effects on offspring growth, only the postnatal effects were important in determining offspring body size. Thus, prenatal effects can be offset by the quality of postnatal maternal care. This finding has implications for the coevolution of prenatal and postnatal maternal effects as they arise as a consequence of maternal body size. In general, my study provides evidence that there can be transgenerational phenotypic plasticity, with maternal size determining offspring size leading to a resemblance between mothers and their offspring above and beyond any direct genetic effects.     

Sex allocation according to multiple sexually dimorphic traits of both parents in the barn swallow (Hirundo rustica)

Parents should differentially invest in sons or daughters depending on the sex‐specific fitness returns from male and female offspring. In species with sexually selected heritable male characters, highly ornamented fathers should overproduce sons, which will be more sexually attractive than sons of less ornamented fathers. Because of genetic correlations between the sexes, females that express traits which are under selection in males should also overproduce sons. However, sex allocation strategies may consist in reaction norms leading to spatiotemporal variation in the association between offspring sex ratio (SR) and parental phenotype. We analysed offspring SR in barn swallows (Hirundo rustica) over 8 years in relation to two sexually dimorphic traits: tail length and melanin‐based ventral plumage coloration. The proportion of sons increased with maternal plumage darkness and paternal tail length, consistently with sexual dimorphism in these traits. The size of the effect of these parental traits on SR was large compared to other studies of offspring SR in birds. Barn swallows thus manipulate offspring SR to overproduce ‘sexy sons’ and potentially to mitigate the costs of intralocus sexually antagonistic selection. Interannual variation in the relationships between offspring SR and parental traits was observed which may suggest phenotypic plasticity in sex allocation and provides a proximate explanation for inconsistent results of studies of sex allocation in relation to sexual ornamentation in birds.     

Larger female fish contribute disproportionately more to self-replenishment

While chance events, oceanography and selective pressures inject stochasticity into the replenishment of marine populations with dispersing life stages, some determinism may arise as a result of characteristics of breeding individuals. It is well known that larger females have higher fecundity, and recent laboratory studies have shown that maternal traits such as age and size can be positively associated with offspring growth, size and survival. Whether such fecundity and maternal effects translate into higher recruitment in marine populations remains largely unanswered. We studied a population of Amphiprion chrysopterus (orange-fin anemonefish) in Moorea, French Polynesia, to test whether maternal size influenced the degree of self-recruitment on the island through body size-fecundity and/or additional size-related maternal effects of offspring. We non-lethally sampled 378 adult and young juveniles at Moorea, and, through parentage analysis, identified the mothers of 27 self-recruits (SRs) out of 101 recruits sampled. We also identified the sites occupied by each mother of an SR and, taking into account variation in maternal size among sites, we found that females that produced SRs were significantly larger than those that did not (approx. 7% greater total length, approx. 20% greater biomass). Our analyses further reveal that the contribution of larger females to self-recruitment was significantly greater than expected on the basis of the relationship between body size and fecundity, indicating that there were important maternal effects of female size on traits of their offspring. These results show, for the first time in a natural population, that larger female fish contribute more to local replenishment (self-recruitment) and, more importantly, that size-specific fecundity alone could not explain the disparity.     

Sex-specific paternal age effects on offspring quality in Drosophila melanogaster

Advanced paternal age has been repeatedly shown to modulate offspring quality via male- and/or female-driven processes, and there are theoretical reasons to expect that some of these effects can be sex-specific. For example, sex allocation theory predicts that, when mated with low-condition males, mothers should invest more in their daughters compared to their sons. This is because male fitness is generally more condition-dependent and more variable than female fitness, which makes it less risky to invest in female offspring. Here, we explore whether paternal age can affect the quality and quantity of offspring in a sex-specific way using Drosophila melanogaster as a model organism. In order to understand the contribution of male-driven processes on paternal age effects, we also measured the seminal vesicle size of young and older males and explored its relationship with reproductive success and offspring quality. Older males had lower competitive reproductive success, as expected, but there was no difference between the offspring sex ratio of young and older males. However, we found that paternal age caused an increase in offspring quality (i.e., offspring weight), and that this increase was more marked in daughters than sons. We discuss different male- and female-driven processes that may explain such sex-specific paternal age effects.     

The Influence of Maternal Quality on Brood Sex Allocation in the Small Carpenter Bee,Ceratina calcarata

In the twig‐nesting carpenter bee, Ceratina calcarata, body size is an important component of maternal quality, smaller mothers producing significantly fewer and smaller offspring than larger mothers. As mothers precisely control the sex and size of each offspring, smaller mothers might compensate by preferentially allocating their investment towards sons. We investigated whether variation in maternal quality leads to variation in sex allocation patterns. At the population level, the numerical sex ratio was 57% male‐biased (1.31 M/F), but the investment between the sexes was balanced (1.02 M/F), because females are 38% larger than males (1.28 F/M). Maternal body size explained both sex allocation pattern and size variation among offspring: larger mothers invested more in individual progeny and produced more female offspring than smaller mothers. Maternal investment in offspring of both sexes decreased throughout the season, probably as a result of increasing maternal wear and age. The exception to this pattern was the curious production of dwarf females in the first two brood cell positions. We suggest that the sex ratio distribution reflects the maternal body size distribution and a constraint on small mothers to produce small broods. This leads to male‐biased allocation by small females, to which large mothers respond by biasing their allocation towards daughters.     

Where do all the maternal effects go? Variation in offspring body size through ontogeny in the live-bearing fish Poecilia parae

Maternal effects are an important source of adaptive variation, but little is known about how they vary throughout ontogeny. We estimate the contribution of maternal effects, sire genetic and environmental variation to offspring body size from birth until 1 year of age in the live-bearing fish Poecilia parae. In both the sexes, maternal effects on body size were initially high in juveniles, and then declined to zero at sexual maturity. In sons, this was accompanied by a sharp rise in sire genetic variance, consistent with the expression of Y-linked loci affecting male size. In daughters, all variance components decreased with time, consistent with compensatory growth. There were significant negative among-dam correlations between early body size and the timing of sexual maturity in both sons and daughters. However, there was no relationship between early life maternal effects and adult longevity, suggesting that maternal effects, although important early in life, may not always influence late life-history traits.     

Relationships of vervet mothers with sons and daughters from one through three years of age

Social relationships between mothers and juvenile offspring were examined in captive, socially-living vervet monkeys (Cercopithecus aethiops sabaeus) to assess the effects of offspring age and sex, and the mother's dominance rank on behavioural interactions. The results indicate that both high-and low-ranking mothers approach and groom their daughters more than they approach and groom their sons. The frequency of both aggressive behaviour toward offspring and support of offspring in agonistic encounters with other group members is influenced by the mother's dominance rank, but not by offsprin sex. Compared to sons, daughters (particularly daughters of high-ranking females) approach and groom their mothers more often, and support their mothers more often in intra-group aggression. The results are discussed in terms of several predictions from parental investment theory and the concept of mutualism.     

Transgenerational effects of nutrition are different for sons and daughters

Food shortage is an important selective factor shaping animal life‐history trajectories. Yet, despite its role, many aspects of the interaction between parental and offspring food environments remain unclear. In this study, we measured developmental plasticity in response to food availability over two generations and tested the relative contribution of paternal and maternal food availability to the performance of offspring reared under matched and mismatched food environments. We applied a cross‐generational split‐brood design using the springtail Orchesella cincta, which is found in the litter layer of temperate forests. The results show adverse effects of food limitation on several life‐history traits and reproductive performance of both parental sexes. Food conditions of both parents contributed to the offspring phenotypic variation, providing evidence for transgenerational effects of diet. Parental diet influenced sons’ age at maturity and daughters’ weight at maturity. Specifically, being born to food‐restricted parents allowed offspring to alleviate the adverse effects of food limitation, without reducing their performance under well‐fed conditions. Thus, parents raised on a poor diet primed their offspring for a more efficient resource use. However, a mismatch between maternal and offspring food environments generated sex‐specific adverse effects: female offspring born to well‐fed mothers showed a decreased flexibility to deal with low‐food conditions. Notably, these maternal effects of food availability were not observed in the sons. Finally, we found that the relationship between age and size at maturity differed between males and females and showed that offspring life‐history strategies in O. cincta are primed differently by the parents.     

Low serum vitamin A mothers breastfeed daughters more often than sons in drought-ridden northern Kenya: a test of the Trivers–Willard hypothesis

The Trivers–Willard hypothesis predicts that natural selection should favor unequal parental investment between daughters and sons based upon maternal condition and offspring reproductive potential. Specifically, it predicts that mothers in good condition should increase investment toward sons, while mothers in poor condition should favor daughters. Previous tests of the hypothesis in human populations overwhelmingly focused on economic resources as maternal condition indicators. We test the Trivers–Willard hypothesis using maternal nutrition—energy and vitamin A status representing macro- and micronutrition, respectively—as the indicator for maternal condition, with breastfeeding frequency recalls serving as the indicator for parental investment. Data from exclusively breastfeeding mothers (n=83) in drought-ridden Ariaal agropastoral villages of northern Kenya were used to test the hypothesis that mothers in poor condition will breastfeed daughters more frequently than sons. Poor condition was defined as having a body mass index <18.5 or serum retinol (vitamin A) concentration <1.05 µmol/l. A linear regression model was applied using breastfeeding frequency as the dependent variable and respective maternal condition, infant's sex, and the maternal condition–infant's sex interaction as the predictors, controlling for covariates. Results supported the hypothesis only in the vitamin A model which predicts that low-vitamin-A mothers breastfeed daughters significantly more frequently than sons (11 vs. 6 times/day), while vitamin-A-sufficient mothers breastfeed daughters and sons equivalently (9 times). These results indicate that maternal nutritional status, particularly micronutrient status, can contribute to the investigation of the evolutionary hypothesis of sex-biased parental investment.     

Big mothers invest more in daughters – reversed sex allocation in a weakly polygynous mammal

How mothers allocate resources to offspring is central to understanding life history strategies. High quality mothers are predicted to favour investment in sons over daughters when to do so increases inclusive fitness. This is the case in ungulates with polygynous mating systems, where reproductive success is more variable among males than females, but information is scarce on sex allocation in less polygynous species. Here, for the weakly dimorphic roe deer, we show that as maternal capacity to invest increases, mothers increase allocation to daughters more than to sons, so that relative allocation to daughters increases markedly with increasing maternal quality. This cannot be explained by a between sex difference in growth priority, hence we conclude that this is evidence for active maternal discrimination. Further, we demonstrate that condition differences between offspring persist to adulthood. For high quality mothers of weakly polygynous species, daughters may be more valuable than sons.     

Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches

Yolk androgens affect offspring hatching, begging, growth and survival in many bird species. If these effects are sex-specific, yolk androgen deposition may constitute a mechanism for differential investment in male and female offspring. We tested this hypothesis in zebra finches. In this species, females increase yolk-testosterone levels and produce male-biased sex ratios when paired to more attractive males. We therefore predicted that especially sons benefit from elevated yolk androgens. Eggs were injected with testosterone or sesame oil (controls) after 2 days of incubation. Testosterone had no clear effect on sex-specific embryonic mortality and changed the pattern of early nestling mortality independent of offspring sex. Testosterone-treated eggs took longer to hatch than control eggs. Control males begged significantly longer than females during the first days after hatching and grew significantly faster. These sex differences were reduced in offspring from testosterone-treated eggs due to prolonged begging durations of daughters, enhanced growth of daughters and reduced growth of sons. The results show that variation in maternal testosterone can play an important role in avian sex allocation due to its sex-specific effects on offspring begging and growth.     

Sex-specific fitness returns are too weak to select for non-random patterns of sex allocation in a viviparous snake

When environmental conditions exert sex-specific selection on offspring, mothers should benefit from biasing their sex allocation towards the sex with the highest fitness in a given environment. Yet, studies show mixed support for such adaptive strategies in vertebrates, which may be due to mechanistic constraints and/or weak selection on facultative sex allocation. In an attempt to disentangle these alternatives, we quantified sex-specific fitness returns and sex allocation (sex ratio and sex-specific mass at birth) according to maternal factors (body size, age, birth date, and litter size), habitat, and year in a viviparous snake with genotypic sex determination. We used data on 106 litters from 19 years of field survey in two nearby habitats occupied by the meadow viper Vipera ursinii ursinii in south-eastern France. Maternal reproductive investment and habitat quality had no differential effects on the growth and survival of sons and daughters. Sex ratio at birth was balanced despite a slight female-biased mortality before birth. No sexual mass dimorphism between offspring was evident. Sex allocation was almost random apart for a trend towards more male-biased litters as females grew older, which could be explained by an inbreeding avoidance strategy. Thus, a weak selection for facultative sex allocation seems sufficient to explain the almost equal sex allocation in the meadow viper.     

Manipulating rearing conditions reveals developmental sensitivity in the smaller sex of a passerine bird, the European starling Sturnus vulgaris

Traditionally, studies of sexually size-dimorphic birds and mammals report that the larger sex is more sensitive to adverse environmental conditions during ontogeny. However, recent studies in avian species that exhibit moderate size-dimorphism indicate that the smaller sex may be more sensitive to poor rearing conditions. To better understand sex-specific sensitivity in a passerine exhibiting moderate size-dimorphism, we examined growth, cell-mediated immunity (CMI) and survival of European starling Sturnus vulgaris nestlings following an experimental reduction of maternal rearing ability (via a feather-clipping manipulation). Contrary to conventional theory, daughters showed reduced growth in both body mass and measures of structural size in response to the maternal treatment. In contrast, sons showed no reductions in any of these traits in relation to the treatment. No sex-specific differences in nestling CMI were found for either group, although CMI of nestlings raised by manipulated mothers were higher than those of control nestlings. Finally, fledging sex ratios did not change from those at hatching indicating that neither sex appeared differentially sensitive to the maternal treatment in terms of mortality. These results reveal that variation in the quality of the rearing environment can have significant effects on the smaller sex of a passerine exhibiting moderate dimorphism and as such support recent studies of species with small-moderate sexual size-dimorphism. Combined results suggest that sex-specific effects of environmental variation on nestling development may be both context- (i.e., brood size, resource level, hatching order) and temporally- (when during development they occur) specific. Furthermore, more studies are needed that examine multiple traits at several developmental stages and then follow the sexes over the longer-term to examine potential effects on fitness.     

Maternal effects influence the sexual behavior of sons and daughters in the zebra finch

Individual differences in sexual behavior have received much attention by evolutionary biologists, but relatively little is known about the proximate causes of this variation. We studied the quantitative genetics of male and female sexual behavior of captive zebra finches and found surprisingly strong maternal effects (differing between individual mothers) on the aggressiveness and song rate of sons and on the daughters' mating preferences for these male traits. We also found that daughters differed in their choosiness during mate-choice experiments depending on whether they originated from eggs produced early or late within the laying sequence of a clutch. Because this effect of laying order occurred independently of hatching order in cross-fostered broods, it must have been caused by consistent within-mother variation in maternal effects transmitted through the egg. Our findings raise the question whether these maternal effects might represent strategic programming of offspring behavior in response to the environment experienced by mothers or whether they are merely nonadaptive byproducts of developmental processes.     

Maternal investment in relation to sex ratio and offspring number in a small mammal – a case for Trivers and Willard theory?

1.  Optimal parental sex allocation depends on the balance between the costs of investing into sons vs. daughters and the benefits calculated as fitness returns. The outcome of this equation varies with the life history of the species, as well as the state of the individual and the quality of the environment.
2.  We studied maternal allocation and subsequent fecundity costs of bank voles, Myodes glareolus , by manipulating both the postnatal sex ratio (all-male/all-female litters) and the quality of rearing environment (through manipulation of litter size by −2/+2 pups) of their offspring in a laboratory setting.
3.  We found that mothers clearly biased their allocation to female rather than male offspring regardless of their own body condition. Male pups had a significantly lower growth rate than female pups, so that at weaning, males from enlarged litters were the smallest. Mothers produced more milk for female litters and also defended them more intensively than male offspring.
4.  The results agree with the predictions based on the bank vole life history: there will be selection for greater investment in daughters rather than sons, as a larger size seems to be more influencial for female reproductive success in this species. Our finding could be a general rule in highly polygynous, but weakly dimorphic small mammals where females are territorial.
5.  The results disagree with the narrow sense Trivers & Willard hypothesis, which states that in polygynous mammals that show higher variation in male than in female reproductive success, high-quality mothers are expected to invest more in sons than in daughters.