Testing hypotheses for maternal effects in Daphnia magna

Maternal effects are widely observed, but their adaptive nature remains difficult to describe and interpret. We investigated adaptive maternal effects in a clone of the crustacean Daphnia magna, experimentally varying both maternal age and maternal food and subsequently varying food available to offspring. We had two main predictions: that offspring in a food environment matched to their mothers should fare better than offspring in unmatched environments, and that offspring of older mothers would fare better in low food environments. We detected numerous maternal effects, for example offspring of poorly fed mothers were large, whereas offspring of older mothers were both large and showed an earlier age at first reproduction. However, these maternal effects did not clearly translate into the predicted differences in reproduction. Thus, our predictions about adaptive maternal effects in response to food variation were not met in this genotype of Daphnia magna.     

Context-dependent sex allocation: constraints on the expression and evolution of maternal effects

Despite decades of research, whether vertebrates can and do adaptively adjust the sex ratio of their offspring is still highly debated. However, this may have resulted from the failure of empirical tests to identify large and predictable fitness returns to females from strategic adjustment. Here, we test the effect of diet quality and maternal condition on facultative sex ratio adjustment in the color polymorphic Gouldian finch (Erythrura gouldiae), a species that exhibits extreme maternal allocation in response to severe and predictable (genetically-determined) fitness costs. On high-quality diets, females produced a relatively equal sex ratio, but over-produced sons in poor dietary conditions. Despite the lack of sexual size dimorphism, nutritionally stressed foster sons were healthier, grew faster, and were more likely to survive than daughters. Although these findings are in line with predictions from sex allocation theory, the extent of adjustment is considerably lower than previously reported for this species. Females therefore have strong facultative control over sex allocation, but the extent of adjustment is likely determined by the relative magnitude of fitness gains and the ability to reliably predict sex-specific benefits from environmental (vs. genetic) variables. These findings may help explain the often inconsistent, weak, or inconclusive empirical evidence for adaptive sex ratio adjustment in vertebrates.     

Mothers adjust egg size to helper number in a cooperatively breeding cichlid

Mothers should adjust the size of propagules to the selectiveforces to which these offspring will be exposed. Usually, alarger propagule size is favored when young are exposed to highmortality risk or conspecific competition. Here we test 2 predictionson how egg size should vary with these selective agents. Whenoffspring are cared for by parents and/or alloparents, protectionmay reduce the predation risk to young, which may allow mothersto invest less per single offspring. In the cooperatively breedingcichlid Neolamprologus pulcher, brood care helpers protect groupoffspring and reduce the latters' mortality rate. Therefore,females are expected to reduce their investment per egg whenmore helpers are present. In a first experiment, we tested thisprediction by manipulating the helper number. In N. pulcher,helpers compete for dispersal opportunities with similar-sizedindividuals of neighboring groups. If the expected future competitionpressure on young is high, females should increase their investmentper offspring to give them a head start. In a second experiment,we tested whether females produce larger eggs when perceivedneighbor density is high. Females indeed reduced egg size withincreasing helper number. However, we did not detect an effectof local density on egg size, although females took longer toproduce the next clutch when local density was high. We arguethat females can use the energy saved by adjusting egg sizeto reduced predation risk to enhance future reproductive output.Adaptive adjustment of offspring size to helper number may bean important, as yet unrecognized, strategy of cooperative breeders.     

Reproductive development and maternal effects in the pine weevil Hylobius abietis

1. In a laboratory study of maturation feeding of female pine weevil Hylobius abietis on current and 1‐year‐old stem bark of transplants of Scots and Corsican pine, Norway and Sitka spruce, Douglas fir, and hybrid larch, the length of the pre‐oviposition period was influenced by the species on which weevils fed. The shortest pre‐oviposition period was on hybrid larch (11.8 days) and the longest on Douglas fir (15.5 days). 2. The species on which weevils fed also affected fecundity but there was evidence of a species–year interaction. Over a period of 36 days, most eggs were laid by weevils feeding on current stem of Norway spruce and Corsican and Scots pine and fewest on current stem of Sitka spruce. 3. Significant maternal effects on egg size were observed both in relation to female size and conifer species. The largest eggs were laid on Corsican pine and the smallest on Douglas fir, with no evidence of a trade‐off between number of eggs laid and their size. 4. There was a positive relationship between egg and larval size and between larval size and survival on logs of four conifer species. Residual resistance mechanisms in the bark of recently cut stumps and larval competition are discussed briefly in relation to the importance of the observed maternal effects on weevil population dynamics.     

Factors affecting offspring survival and development in a cooperative bird: social, maternal and environmental effects

1. In many noncooperative vertebrates, maternal effects commonly influence offspring survival and development. In cooperative vertebrates, where multiple adults help to raise young from a single brood, social effects may reduce or replace maternal effects on offspring. 2. Factors affecting offspring survival and development at different stages (fledging, nutritional independence and adulthood) were tested in the cooperatively breeding Arabian babbler to determine the relative importance of social, maternal and environmental factors at each stage. An influence of maternal effects was found during the nestling stage only. 3. Social factors affected the survival and development of young at all stages. The amount of food received from helpers influenced post-fledging weight gain, development of foraging skills, and survival to reproductive age. Environmental effects were also important, with groups occupying high-quality territories more likely to produce young that survived to maturity. 4. The strong influence of helper contributions on the survival and development of young at all stages from hatching to maturity suggests social factors may have important long-term effects on offspring fitness in cooperative societies. Traditional measures of offspring survival in cooperative birds, which commonly measure survival to fledging age only, may underestimate the significant benefit of helper contributions on the survival and development of young.     

Size delays female senescence in a medium sized marsupial: The effects of maternal traits on annual fecundity in the northern brown bandicoot (Isoodon macrourus)

The degree to which females allocate resources between current reproduction, future fecundity and survival is a central theme in life history theory. We investigated two hypotheses proposed to explain patterns of reproductive investment, terminal investment and senescence, by examining the effects of maternal traits (age and maternal mass) on annual fecundity in female northern brown bandicoots, Isoodon macrourus (Marsupialia: Peramelidae). We found that annual fecundity in females declined in their final year of reproduction, indicating reproductive senescence. Maternal mass significantly influenced the rate of senescence and, in turn, a female's lifetime reproductive output. Mass had little effect on fecundity in 1st and 2nd year females, but a positive relationship with fecundity in 3rd year females. This meant that heavy, 3rd year females did not suffer the decline in fecundity shown in light 3rd year females. For 1st year females, mass and leg length increased between their first and second reproductive seasons, indicating a temporary shift, from the allocation of resources to reproduction, to increasing condition or structural size post their first breeding event. There were no net changes to body mass in subsequent years. We suggest that this year of post‐reproductive growth has important consequences for senescent effects on reproduction. Overall, results provided support for the effects of senescence on annual fecundity. Our findings were not consistent with the terminal investment hypothesis; reproductive output did not increase in females' final reproductive season despite a rapid decline in survival. However, this notion cannot be entirely dismissed; other measures of reproductive performance not examined here (e.g. offspring mass) may have provided an indication that females did increase their effort at the end of their lifespan. This study highlights the difficulty of measuring reproductive costs and the importance of understanding the combined effects of specific characteristics of an individual when interpreting reproductive strategies in iteroparous organisms.     

Variation among populations of Diodia teres (Rubiaceae) in environmental maternal effects

Previous studies have quantified variation in environmental maternal effects (EME) within populations, but these effects could differ among populations as well. In this study we grew clonal replicates of individuals from three populations of the annual plant Diodia teres in their native and non-native environments. Our goal was to estimate the effects of maternal environment and maternal population on seed and seedling traits. Seeds that were produced in this field study were then planted in two soil types to quantify effects of the offspring environment on seedling traits. There was substantial variation among populations for seed weight. We found population variation for EME, and maternal environment by offspring environment interactions. We conclude that variation among populations in EME may be an unrecognized component of local adaptation, and that attempts to control maternal effects by statistically accounting for variation in seed weight may be ineffective.     

Sex-related effects of maternal egg investment on offspring in relation to carotenoid availability in the great tit

1. Maternal carotenoids in the egg yolk have been hypothesized to promote maturation of the immune system and protect against free radical damages. Depending on availability, mothers may thus influence offspring quality by depositing variable amounts of carotenoids into the eggs. Sex allocation theory predicts that in good quality environments, females should invest into offspring of the sex that will provide larger fitness return, generally males. 2. In a field experiment we tested whether female great tits bias their investment towards males when carotenoid availability is increased, and whether male offspring of carotenoid-supplemented mothers show higher body condition. We partially cross-fostered hatchlings to disentangle maternal effects from post-hatching effects, and manipulated hen flea Ceratophyllus gallinae infestation to investigate the relationship between carotenoid availability and resistance to ectoparasites. 3. As predicted, we found that carotenoid-supplemented mothers produced males that were heavier than their sisters at hatching, while the reverse was true for control mothers. This suggests that carotenoid availability during egg production affects male and female hatchlings differentially, possibly via a differential allocation to male and female eggs. 4. A main effect of maternal supplementation became visible 14 days after hatching when nestlings hatched from eggs laid by carotenoid-supplemented mothers had gained significantly more mass than control nestlings. Independently of the carotenoid treatment, fleas impaired mass gain of nestlings during the first 9 days in large broods only and reduced tarsus length of male nestlings at an age of 14 days, suggesting a cost to mount a defence against parasites. 5. Overall, our results suggest that pre-laying availability of carotenoids affects nestling condition in a sex-specific way with potentially longer-lasting effects on offspring fitness.     

Multiple pathways of maternal effects in black-headed gull eggs: constraint and adaptive compensatory adjustment

We investigated in the black-headed gull whether female deposition of antioxidants and immunoglobulins (enhancing early immune function), and testosterone (suppressing immune function and increasing early competitive skills) correlate suggesting that evolution has favoured the mutual adjustment of different pathways for maternal effects. We also took egg mass, the position of the egg in the laying sequence and offspring sex into account, as these affect offspring survival. Yolk antioxidant and immunoglobulin concentrations decreased across the laying order, while yolk testosterone concentrations increased. This may substantially handicap the immune defence of last-hatched chicks. The decrease in antioxidant levels was greater when mothers had a low body mass and when the increase in testosterone concentrations was relatively large. This suggests that female black-headed gulls are constrained in the deposition of antioxidants in last-laid eggs and compensate for this by enhanced testosterone deposition. The latter may be adaptive since it re-allocates the chick's investment from costly immune function to growth and competitive skills, necessary to overcome the consequences of hatching late from an egg of reduced quality.     

Estimates of (co)variance components due to direct and maternal effects for body weights in Jamunapari goats

Estimates of (co)variance components were obtained for weights at birth, weaning and at 6, 9 and 12 months of age in Jamunapari goats maintained at the Central Institute for Research on Goats, Makhdoom, Mathura, India, over a period of 23 years (1982 to 2004). Records of 4301 kids descended from 204 sires and 1233 does were used in the study. Analyses were carried out by restricted maximum likelihood (REML), fitting an animal model and ignoring or including maternal genetic or permanent environmental effects. Six different animal models were fitted for all traits. The best model was chosen after testing the improvement of the log-likelihood values. Direct heritability estimates were inflated substantially for all traits when maternal effects were ignored. Heritability estimates for weights at birth, weaning and at 6, 9 and 12 months of age were 0.12, 0.18, 0.13, 0.17 and 0.21, respectively. Maternal heritability of body weight declined from 0.19 at birth to 0.08 at weaning and was near zero and not significant thereafter. Estimates of the fraction of variance due to maternal permanent environmental effects were 0.09, 0.13 and 0.10 for body weights at weaning, 6 months and 9 months of age, respectively. Results suggest that maternal additive effects were important only in the early stages of growth, whereas a permanent environmental maternal effect existed from weaning to 9 months of age. These results indicate that modest rates of genetic progress appear possible for all weights.     

Females allocate differentially to offspring size and number in response to male effects on female and offspring fitness

Female investment in offspring size and number has been observed to vary with the phenotype of their mate across diverse taxa. Recent theory motivated by these intriguing empirical patterns predicted both positive (differential allocation) and negative (reproductive compensation) effects of mating with a preferred male on female investment. These predictions, however, focused on total reproductive effort and did not distinguish between a response in offspring size and clutch size. Here, we model how specific paternal effects on fitness affect maternal allocation to offspring size and number. The specific mechanism by which males affect the fitness of females or their offspring determines whether and how females allocated differentially. Offspring size is predicted to increase when males benefit offspring survival, but decrease when males increase offspring growth rate. Clutch size is predicted to increase when males contribute to female resources (e.g. with a nuptial gift) and when males increase offspring growth rate. The predicted direction and magnitude of female responses vary with female age, but only when per-offspring paternal benefits decline with clutch size. We conclude that considering specific paternal effects on fitness in the context of maternal life-history trade-offs can help explain mixed empirical patterns of differential allocation and reproductive compensation.     

Intergenerational effects of maternal birth season on offspring size in rural Gambia

Environmental conditions experienced in early life can influence an individual's growth and long-term health, and potentially also that of their offspring. However, such developmental effects on intergenerational outcomes have rarely been studied. Here we investigate intergenerational effects of early environment in humans using survey- and clinic-based data from rural Gambia, a population experiencing substantial seasonal stress that influences foetal growth and has long-term effects on first-generation survival. Using Fourier regression to model seasonality, we test whether (i) parental birth season has intergenerational consequences for offspring in utero growth (1982 neonates, born 1976-2009) and (ii) whether such effects have been reduced by improvements to population health in recent decades. Contrary to our predictions, we show effects of maternal birth season on offspring birth weight and head circumference only in recent maternal cohorts born after 1975. Offspring birth weight varied according to maternal birth season from 2.85 to 3.03 kg among women born during 1975-1984 and from 2.84 to 3.41 kg among those born after 1984, but the seasonality effect reversed between these cohorts. These results were not mediated by differences in maternal age or parity. Equivalent patterns were observed for offspring head circumference (statistically significant) and length (not significant), but not for ponderal index. No relationships were found between paternal birth season and offspring neonatal anthropometrics. Our results indicate that even in rural populations living under conditions of relative affluence, brief variation in environmental conditions during maternal early life may exert long-term intergenerational effects on offspring.     

Sex-specific sibling interactions and offspring fitness in vertebrates: patterns and implications for maternal sex ratios

Vertebrate sex ratios are notorious for their lack of fit to theoretical models, both with respect to the direction and the magnitude of the sex ratio adjustment. The reasons for this are likely to be linked to simplifying assumptions regarding vertebrate life histories. More specifically, if the sex ratio adjustment itself influences offspring fitness, due to sex-specific interactions among offspring, this could affect optimal sex ratios. A review of the literature suggests that sex-specific sibling interactions in vertebrates result from three major causes: (i) sex asymmetries in competitive ability, for example due to sexual dimorphism, (ii) sex-specific cooperation or helping, and (iii) sex asymmetries in non-competitive interactions, for example steroid leakage between fetuses. Incorporating sex-specific sibling interactions into a sex ratio model shows that they will affect maternal sex ratio strategies and, under some conditions, can repress other selection pressures for sex ratio adjustment. Furthermore, sex-specific interactions could also explain patterns of within-brood sex ratio (e.g. in relation to laying order). Failure to take sex-specific sibling interactions into account could partly explain the lack of sex ratio adjustment in accordance with theoretical expectations in vertebrates, and differences among taxa in sex-specific sibling interactions generate predictions for comparative and experimental studies.     

When mothers make sons sexy: maternal effects contribute to the increased sexual attractiveness of extra-pair offspring

Quality differences between offspring sired by the social and by an extra-pair partner are usually assumed to have a genetic basis, reflecting genetic benefits of female extra-pair mate choice. In the zebra finch (Taeniopygia guttata), we identified a colour ornament that is under sexual selection and appears to have a heritable basis. Hence, by engaging in extra-pair copulations with highly ornamented males, females could, in theory, obtain genes for increased offspring attractiveness. Indeed, sons sired by extra-pair partners had larger ornaments, seemingly supporting the genetic benefit hypothesis. Yet, when comparing ornament size of the social and extra-pair partners, there was no difference. Hence, the observed differences most likely had an environmental basis, mediated, for example, via differential maternal investment of resources into the eggs fertilized by extra-pair and social partners. Such maternal effects may (at least partly) be mediated by egg size, which we found to be associated with mean ornament expression in sons. Our results are consistent with the idea that maternal effects can shape sexual selection by altering the genotype-phenotype relationship for ornamentation. They also caution against automatically attributing greater offspring attractiveness or viability to an extra-pair mate's superior genetic quality, as without controlling for differential maternal investment we may significantly overestimate the role of genetic benefits in the evolution of extra-pair mating behaviour.     

A test of three hypotheses for ovariole number determination in the grasshopper Romalea microptera

Ovariole number in insects determines potential fecundity and can be influenced by genes, environmental conditions during development and parental effects. In the present study, three hypotheses are tested for ovariole number determination in the grasshopper Romalea microptera (Beauvois), which exhibits both intra‐ and interpopulation variation in ovariole number. In hypothesis 1, variation in ovariole number is a result of genetic variation. In hypothesis 2, ovariole number is influenced by nutrition during development. In hypothesis 3, ovariole number is influenced by maternal nutritional status. Females from four treatments are compared: low‐food, high‐food, daughters of low‐food, and daughters of high‐food. There is a relationship between parent and offspring ovariole number despite different environments, supporting hypothesis 1. Also, ovariole numbers are slightly, but significantly lower in individuals fed a low‐food diet compared with a high‐food diet, supporting hypothesis 2. Hypothesis 3 is not supported: starved and well‐fed females produce eggs of similar mass, as well as offspring with similar numbers of ovarioles, suggesting that the nutritional status of mothers does not influence offspring mass or offspring ovariole number. The results imply that genetic variation and developmental conditions determine ovariole number in this species but maternal environment does not. These results conflict with previous studies of ovariole determination in grasshoppers and locusts.     

Polyandry restores female fertility and paternal effects diminished by inbreeding in Hippodamia convergens

1. The fertility restoration hypothesis posits that polyandry can evolve when female fertility is reduced by matings with related males, but restored by matings with unrelated ones. 2. Using a promiscuous ladybird, this hypothesis was tested by mating mature, virgin females twice with sib and non‐sib males in all four permutations and observing female fertility. The development of progeny from the first and 10th clutches was also followed to test for differences in paternal effects. 3. Mating treatment did not affect fecundity, but egg viability was reduced by sib matings, and restored by non‐sib matings, regardless of mating sequence. In addition, negative paternal effects of sib matings on progeny (lower survival) were compensated by non‐sib matings. 4. The survival of offspring in first clutches was sensitive to the paternal mating sequence and was higher if a sibling male was preceded by a non‐sib male, compared with the reverse, consistent with a time lag in response to male epigenetic signals. Offspring survival did not differ between these two treatments in the 10th clutch, suggesting a blending of paternal effects over time. 5. The results are indicative of interactions between the paternal effects contributed by different males, and between paternal and maternal effects, the latter causing faster development in later clutches. 6. Thus, the reproductive benefits of polyandry for H. convergens females are potentially both genetic and epigenetic, as both egg fertility and beneficial paternal effects were diminished by sib matings, but restored by matings with unrelated males.     

Manipulation of male attractiveness induces rapid changes in avian maternal yolk androgen deposition

Avian eggs contain maternal androgens that may adjust offspringdevelopment to environmental conditions. We review evidenceand functional explanations for the relationship between androgenconcentrations in avian eggs and male attractiveness. Experimentalstudies in captive birds show generally positive relationships,but results from correlational and experimental field studiesare less consistent, perhaps because they lack a within-femaledesign to control for confounding between-female variation.We analyzed the effect of male attractiveness on yolk levelsof maternal androgens in a wild bird, using a correlationaland experimental approach with a within-female design. We manipulatedthe sexually selected UV coloration of the crown feathers ofmale blue tits (Cyanistes caeruleus) after their female hadlaid the second egg and measured the subsequent effect on androgenconcentrations (testosterone and androstenedione) in the fifth,seventh, and ninth eggs relative to that in the second egg.Levels of testosterone, but not androstenedione, in eggs 5 and7 were higher for control (attractive) than for UV-reduced (unattractive)males. This effect disappeared in the ninth egg, coincidingwith the recovery of UV coloration after manipulation. Thissuggests that females are capable of rapid adjustments of testosteronedeposition in response to changes in their mate's ornamentalplumage. However, androgen concentrations in the second eggand pretreatment male crown coloration were not correlated.Possibly, the combination of relatively small variation in UVcoloration before treatment and the influence of unknown confoundingvariables in the correlative approach resulted in insufficientstatistical power to detect such a correlation.