Differential effects of offspring and maternal inbreeding on egg laying and offspring performance in the burying beetle Nicrophorus vespilloides

We investigate the effect of offspring and maternal inbreeding on maternal and offspring traits associated with early offspring fitness in the burying beetle Nicrophorus vespilloides. We conducted two experiments. In the first experiment, we manipulated maternal inbreeding only (keeping offspring outbred) by generating mothers that were outbred, moderately inbred or highly inbred. Meanwhile, in the second experiment, we manipulated offspring inbreeding only (keeping females outbred) by generating offspring that were outbred, moderately inbred or highly inbred. In both experiments, we monitored subsequent effects on breeding success (number of larvae), maternal traits (clutch size, delay until laying, laying skew, laying spread and egg size) and offspring traits (hatching success, larval survival, duration of larval development and average larval mass). Maternal inbreeding reduced breeding success, and this effect was mediated through lower hatching success and greater larval mortality. Furthermore, inbred mothers produced clutches where egg laying was less skewed towards the early part of laying than outbred females. This reduction in the skew in egg laying is beneficial for larval survival, suggesting that inbred females adjusted their laying patterns facultatively, thereby partially compensating for the detrimental effects of maternal inbreeding on offspring. Finally, we found evidence of a nonlinear effect of offspring inbreeding coefficient on number of larvae dispersing. Offspring inbreeding affected larval survival and larval development time but also unexpectedly affected maternal traits (clutch size and delay until laying), suggesting that females adjust clutch size and the delay until laying in response to being related to their mate.     

All eggs are made equal: meta‐analysis of egg sexual size dimorphism in birds

Sex‐biased resource allocation in avian eggs has gained increasing interest. The adaptive explanations of such allocation are often related to life‐history strategies of the studied species. In some species, egg sexual size dimorphism (SSD) was suggested to promote future size differences between adults of each sex. In other species, egg SSD was invoked as an adaptive means by which a mother balances sex‐specific nestling mortality. According to the first scenario, mothers should produce bigger eggs for the bigger sex, thus across species, adult SSD should be a significant positive predictor of egg SSD. Under the second scenario, mothers should produce bigger eggs for the smaller sex. If different species use contrasting strategies, then a universal expectation is that there should be a significant relationship between the magnitude of adult SSD and the magnitude of egg SSD, irrespective of the direction of those differences. Our aim was to examine whether the direction of egg SSD is predicted by the direction of adult SSD or whether degree of egg SSD is related to degree of adult SSD. To answer that question, we performed meta‐analysis of 63 studies, which included information on egg SSD of 65 effect sizes from 51 avian species. We found that across species, adult SSD does not predict egg SSD. More importantly, the observed variation in effect sizes in our data set was largely explained by sampling error (variance). Although adult SSD is undoubtedly a prominent feature of birds, there is little evidence for egg SSD across avian species.     

Error management theory and the adaptive significance of transgenerational maternal‐stress effects on offspring phenotype

It is well established that circulating maternal stress hormones (glucocorticoids, GCs) can alter offspring phenotype. There is also a growing body of empirical work, within ecology and evolution, indicating that maternal GCs link the environment experienced by the mother during gestation with changes in offspring phenotype. These changes are considered to be adaptive if the maternal environment matches the offspring's environment and maladaptive if it does not. While these ideas are conceptually sound, we lack a testable framework that can be used to investigate the fitness costs and benefits of altered offspring phenotypes across relevant future environments. We present error management theory as the foundation for a framework that can be used to assess the adaptive potential of maternal stress hormones on offspring phenotype across relevant postnatal scenarios. To encourage rigorous testing of our framework, we provide field‐testable hypotheses regarding the potential adaptive role of maternal stress across a diverse array of taxa and life histories, as well as suggestions regarding how our framework might provide insight into past, present, and future research. This perspective provides an informed lens through which to design and interpret experiments on the effects of maternal stress, provides a framework for predicting and testing variation in maternal stress across and within taxa, and also highlights how rapid environmental change that induces maternal stress may lead to evolutionary traps.     

Effects of male genetic contribution and paternal investment to egg and hatchling size in the cricket,Gryllus firmus

Egg provisions represent the complete energy supply of oviparous organisms from fertilization until hatching, and egg size is generally correlated with initial offspring size and a suite of other early fitness related traits. Since egg size is determined by the mother, little attention has been given to potential sources of paternal effects on either egg size or initial offspring size. This study considers two processes by which the sire can affect the egg size and/or initial body size of his offspring, in the multiply mated cricket, Gryllus firmus. The first is a paternal genetic effect, whereby differences in offspring genotype result in differences in the efficiency of metabolising available resources. The second is a paternal environmental effect, whereby the quality or size of paternal investment varies among male phenotypes and this is correlated with the size of eggs the females subsequently produce. Using a one-locus two-allele recessive mutation for pale eye colour as a marker, a mating experiment was designed which enabled the discrimination between eggs fertilized by two males mated simultaneously to a single female. The results of this experiment suggest that sire effects on egg and initial body size occur through both processes. Eggs fertilised by the two males were significantly different at day ten of development, suggesting that the genetic contribution of the sire is affecting embryonic body size. Further, a negative correlation was found between the head size of the pale eyed male and the size of all the eggs that the female laid, suggesting an effect of male size of the amount of nutrients the female receives from her mates. The results of this study suggest that paternal effects may be both more common and more profound than previously thought, and that studies examining early fitness traits that are correlated to egg size or initial body size, in oviparous animals, should consider the possibility and importance of the paternal contribution.     

Seasonal variation in sex ratio and sexual egg dimorphism favouring daughters in first clutches of the spotless starling

We investigated possible pre‐hatching mechanisms of sex‐differential investment by females that may contribute to offspring sex‐ratio adjustment enhancing the fitness return from reproductive effort in the spotless starling (Sturnus unicolor). We found a seasonal shift in sex ratio from daughters to sons as the season advances. Furthermore, the probability of breeding at 1‐year old and recruitment into the breeding population in daughters is associated with laying date but not with mass at fledging. The reverse is true for males which rarely bred at 1‐year old. We also found that eggs containing female embryos are significantly heavier than those containing males in spite of the slight sexual dimorphism in favour of males. This suggests maternal control of provisioning, favouring daughters that may balance sibling mortality and competition with their brothers. Our results on seasonal variation in sex ratio and differential egg provisioning are consistent with an adaptive tactic in which mothers increase their reproductive return by enhancing the probability that daughters survive and breed in their first year of life.     

Parent–offspring conflict and selection on egg size in turtles

The trade‐off between offspring size and number can present a conflict between parents and their offspring. Because egg size is constrained by clutch size, the optimal egg size for offspring fitness may not always be equivalent to that which maximizes parental fitness. We evaluated selection on egg size in three turtle species (Apalone mutica, Chelydra serpentina and Chrysemys picta) to determine if optimal egg sizes differ between offspring and their mothers. Although hatching success was generally greater for larger eggs, the strength and form of selection varied. In most cases, the egg size that maximized offspring fitness was greater than that which maximized maternal fitness. Consistent with optimality theory, mean egg sizes in the populations were more similar to the egg sizes that maximized maternal fitness, rather than offspring fitness. These results provide evidence that selection has maximized maternal fitness to achieve an optimal balance between egg size and number.     

Egg size and offspring quality: a meta‐analysis in birds

Parents affect offspring fitness by propagule size and quality, selection of oviposition site, quality of incubation, feeding of dependent young, and their defence against predators and parasites. Despite many case studies on each of these topics, this knowledge has not been rigorously integrated into individual parental care traits for any taxon. Consequently, we lack a comprehensive, quantitative assessment of how parental care modifies offspring phenotypes. This meta‐analysis of 283 studies with 1805 correlations between egg size and offspring quality in birds is intended to fill this gap. The large sample size enabled testing of how the magnitude of the relationship between egg size and offspring quality depends on a number of variables. Egg size was positively related to nearly all studied offspring traits across all stages of the offspring life cycle. Not surprisingly, the relationship was strongest at hatching but persisted until the post‐fledging stage. Morphological traits were the most closely related to egg size but significant relationships were also found with hatching success, chick survival, and growth rate. Non‐significant effect sizes were found for egg fertility, chick immunity, behaviour, and life‐history or sexual traits. Effect size did not depend on whether chicks were raised by their natural parents or were cross‐fostered to other territories. Effect size did not depend on species‐specific traits such as developmental mode, clutch size, and relative size of the egg, but was larger if tested in captive compared to wild populations and between rather than within broods. In sum, published studies support the view that egg size affects juvenile survival. There are very few studies that tested the relationship between egg size and the fecundity component of offspring fitness, and no studies on offspring survival as adults or on global fitness. More data are also needed for the relationships between egg size and offspring behavioural and physiological traits. It remains to be established whether the relationship between egg size and offspring performance depends on the quality of the offspring environment. Positive effect sizes found in this study are likely to be driven by a causal effect of egg size on offspring quality. However, more studies that control for potential confounding effects of parental post‐hatching care, genes, and egg composition are needed to establish firmly this causal link.     

Energetics of reproduction: consequences of divergent selection on egg size, food limitation, and female age for egg composition and reproductive effort in a butterfly

Using lines artificially selected on egg size and being subjected to a restricted and an unrestricted feeding treatment, we examined the relationships between egg size, egg number, egg composition, and reproductive investment in the butterfly Bicyclus anynana . Despite a successful manipulation of egg size, correlated responses to selection in larval time, pupal mass, pupal time, longevity, fecundity, or the amount of energy allocated to reproduction were virtually absent. Thus, there was no indication for an evolutionary link between offspring size and reproductive investment. Egg composition, in contrast, was affected by selection, with larger eggs containing relatively more lipid and water, but less protein and energy compared to smaller eggs. Hence, females producing large eggs did not have to sacrifice fecundity due to adjustments in egg composition. Food limitation per se caused only minor changes in egg composition, and there was no general reduction in egg provisioning with female age. The latter was restricted to food-limited females, whereas egg quality remained remarkably similar throughout the females' life in control groups. We conclude that neglecting changes in biochemical egg composition, depending on genetic background, food availability, and female age, may introduce substantial error when estimating reproductive effort, and may ultimately lead to invalid conclusions.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 403–418.     

The causes and consequences of variation in offspring size: a case study using Daphnia

Offspring size can have large and direct fitness implications, but we still do not have a complete understanding of what causes offspring size to vary. Daphnia (water fleas) generally produce fewer and larger offspring when food is limited. Here, we use a mathematical model to show that this could be explained by either: (1) an advantage of producing larger eggs when food is limited; or (2) a lower boundary on egg volume (below which eggs do not have sufficient resources to be viable), that is similar in volume to the evolutionarily stable egg volume predicted by standard clutch size models. We tested the first possibilities experimentally by placing offspring from mothers kept at two food treatments (high and low - leading to relatively small and large eggs respectively) into two food treatments (same as maternal treatments, in a fully factorial design) and measuring their fitness (reproduction, age at maturity, and size at maturity). We also tested survival under starvation conditions of offspring produced from mothers at low and high food treatments. We found that (larger) offspring produced by low-food mothers actually had lower fitness as they took longer to reproduce, regardless of their current food treatment. Additionally, we found no survival advantage to being born of a food-stressed mother. Consequently, our results do not support the hypothesis that there is an advantage to producing larger eggs when food is limited. In contrast, data from the literature support the importance of a lower boundary on egg size.     

Experimental litter size reduction reveals costs of gestation and delayed effects on offspring in a viviparous lizard

Experimental studies have often been employed to study costs of reproduction, but rarely to study costs of gestation. Disentangling the relative importance of each stage of the reproductive cycle should help to assess the costs and benefits of different reproductive strategies. To that end, we experimentally reduced litter size during gestation in a viviparous lizard. We measured physiological and behavioural parameters during gestation and shortly after parturition, as well as survival and growth of females and their offspring. This study showed four major results. First, the experimental litter size reduction did not significantly affect the cellular immune response, the metabolism and the survival of adult females. Second, females with reduced litter size decreased their basking time. Third, these females also had an increased postpartum body condition. As postpartum body condition is positively related to future reproduction, this result indicates a gestation cost. Fourth, even though offspring from experimentally reduced litters had similar weight and size at birth as other offspring, their growth rate after birth was significantly increased. This shows the existence of a maternal effect during gestation with delayed consequences. This experimental study demonstrates that there are some costs to gestation, but it also suggests that some classical trade-offs associated with reproduction may not be explained by gestation costs.     

Of mammals and milk: how maternal stress affects nursing offspring

1. A large body of research shows that maternal stress during an offspring’s early life can impact its phenotype in both the short and long term. In the Vertebrata, most research has been focused on maternal stress during the prenatal period. However, the postnatal period is particularly important in mammals because maternal milk provides a conduit by which maternal hormones secreted in response to stressors (glucocorticoids, GCs) can reach offspring. Moreover, lactation outlasts gestation in many species.
2. Though GCs were first detected in milk over 40 years ago, few studies have explored how they affect nursing offspring, and no reviews have been written on how maternal stress affects nursing offspring in the natural world.
3. We discuss the evolution of milk and highlight its importance in each of the three mammalian lineages: monotremes (subclass Monotremata), marsupials (infraclass Marsupialia), and eutherians (infraclass Placentalia). Most research on the effects of milk GCs on offspring has been focused on eutherians, but monotremes and marsupials rely on their mothers’ milk for a proportionally longer period of time, and so research on these taxa may yield more insight.
4. We show that GCs are important for milk production, both during an individual nursing bout and over the entire lactation period, and review evidence of GCs moving from maternal blood to milk, and eventually to nursing offspring. We examine evidence from rodents and primates of associations between GC levels in lactating females (either blood or milk) and offspring behaviour and growth rates. We discuss ways that maternal stress may impact these offspring phenotypes outside of milk GCs, such as changes to: (1) milk output, (2) other milk constituents (e.g. macronutrients, growth factors, cytokines), and (3) maternal care behaviour.
5. Critical to understanding the fitness impacts of elevated maternal GC levels during lactation is to place this within the context of the natural environment. Species-specific traits and natural histories will help us to understand why such maternal stress produces different offspring phenotypes that equip them to cope with and succeed in the environment they are about to enter.

     

The effect of egg size and habitat on starling nestling growth and survival

In spite of the fact that hatchling size and energy reserves in birds are affected by egg size, many studies have failed to find an effect of egg size on offspring fitness. One possibility is that this is because they have been performed in areas with high food availability and that effects of egg size on offspring fitness are most apparent in areas of low food availability. To investigate this, egg size,␣offspring mass and survival of European starlings (Sturnus vulgaris) were measured in an agricultural landscape with a low but variable amount of pasture, the preferred foraging habitat of parent starlings. Offspring mass was related to egg size, but egg size explained a declining proportion of the variation in nestling mean mass as nestlings grew older. Offspring survival during the early, but not during the late nestling period was related to egg size. Throughout the nestling␣period, survival was related to the mass of the nestlings. It is suggested that the effect of egg size on␣offspring survival is through the effect of egg size on offspring mass, this effect declining as offspring grow older. Offspring survival during the early part of the nestling period was related to egg size when availability of pasture was low, but not when it was high. However, the interaction was not significant. Selection for␣larger egg size is discussed in relation to the structuring␣of starling populations into sources and sinks. Received: 22 September 1997 / Accepted: 22 January 1998     

Social and breeding status are associated with the expression of GnIH

Discoveries of how social behavior can influence the plasticity of gonadotropin-releasing hormone (GnRH) have revolutionized the field of behavioral neuroendocrinology by providing new insights into the neural mechanisms controlling behavior. In 2000, the neuropeptide gonadotropin inhibitory hormone (GnIH) was discovered and is changing the way we view how the brain mediates reproduction and associated behaviors. GnIH acts as a reproductive 'pause button', momentarily inhibiting the activity of the reproductive system. However, how GnIH fluctuates naturally in response to social environment is unknown. We examine how the outcome of competition for limited resources needed for reproduction is associated with GnIH. We experimentally manipulated nesting opportunities for pairs of European starlings (Sturnus vulgaris) and examined brain GnIH mRNA and peptide content, as well as GnRH content and plasma testosterone and corticosterone. By limiting the number of nest boxes per enclosure and thus the number of social pairing and nesting opportunities, we observed that birds which outcompeted others for nest boxes ('winners') had significantly fewer numbers of GnIH peptide-producing cells than those without nest boxes ('losers') and this relationship changed with breeding stage. GnRH content, testosterone and corticosterone did not vary with nest box ownership. Thus, while birds appeared reproductively capable across treatments, our data indicate that GnIH may serve as a modulator of reproductive behaviors in response to social environment. Additionally, we provide some evidence of the adaptive value of this mechanism.     

Influence of egg size differences within egg clutches on larval parameters in nine libellulid species (Odonata)

Abstract.  1. In libellulids, egg size differs between species and populations. There are also size differences within egg clutches of individual females.
2. Past experiments suggest that there are two different types of egg clutches in libellulids. Egg size decreases significantly during oviposition in species that perform non-contact guarding during oviposition. In contrast, in species ovipositing in tandem, egg size is randomly distributed.
3. This study deals with the possible consequences of egg size variation within the different egg clutch types. The study examined whether there is a correlation between egg development time, offspring sex or larval size and egg size.
4. The current experiments were conducted in Namibia and Germany. Five non-contact guarding and four tandem guarding libellulid species were used.
5. In some species larger eggs needed more time to develop, in some species no correlation between egg size and egg development time could be found, whereas in other species larger eggs developed faster.
6. The sex ratio was biased towards females in Leucorrhinia dubia and in Sympetrum striolatum and egg size was not associated with gender.
7. In both egg clutch types larger eggs resulted in larger larvae. In this study, evidence was found that the effects of egg size diminished with progressing larval development under good conditions. However, it is possible that the effects may have a greater influence under harsh circumstances.     

Post-hatching parental care masks the effects of egg size on offspring fitness: a removal experiment on burying beetles

Parents can increase the fitness of their offspring by allocating nutrients to eggs and/or providing care for eggs and offspring. Although we have a good understanding of the adaptive significance of both egg size and parental care, remarkably little is known about the co-evolution of these two mechanisms for increasing offspring fitness. Here, we report a parental removal experiment on the burying beetle Nicrophorus vespilloides in which we test whether post-hatching parental care masks the effect of egg size on offspring fitness. As predicted, we found that the parent's presence or absence had a strong main effect on larval body mass, whereas there was no detectable effect of egg size. Furthermore, egg size had a strong and positive effect on offspring body mass in the parent's absence, whereas it had no effect on offspring body mass in the parent's presence. These results support the suggestion that the stronger effect of post-hatching parental care on offspring growth masks the weaker effect of egg size. We found no correlation between the number and size of eggs. However, there was a negative correlation between larval body mass and brood size in the parent's presence, but not in its absence. These findings suggest that the trade-off between number and size of offspring is shifted from the egg stage towards the end of the parental care period and that post-hatching parental care somehow moderates this trade-off.     

Sex-specific effects of maternal immunization on yolk antibody transfer and offspring performance in zebra finches

Trans-generational antibody transfer constitutes an important mechanism by which mothers may enhance offspring resistance to pathogens. Thus, differential antibody deposition may potentially allow a female to differentiate offspring performance. Here, we examined whether maternal immunization with sheep red blood cells (SRBC) prior to egg laying affects sex-specific yolk antibody transfer and sex-specific offspring performance in zebra finches (Taeniopygia guttata). We showed that immunized mothers deposit anti-SRBC antibodies into the eggs depending on embryo sex and laying order, and that maternal exposure to SRBC positively affects the body size of female, but not male offspring. This is the first study reporting sex-specific consequences of maternal immunization on offspring performance, and suggests that antibody transfer may constitute an adaptive mechanism of maternal favouritism.     

Sex allocation in yellow-legged gulls (Larus michahellis) depends on nutritional constraints on production of large last eggs

Male and female offspring can differ in their susceptibility to pre-natal (e.g. egg quality) and post-natal (e.g. sib–sib competition) conditions, and parents can therefore increase their individual fitness by adjusting these maternal effects according to offspring sex. In birds, egg mass and laying/hatching order are the main determinants of offspring viability, but these effects can act differently on each sex. In a previous study, relatively large last-laid (c-)eggs of yellow-legged gulls (Larus michahellis) were more likely to carry a female embryo. This suggests compensatory allocation of maternal resources to daughters from c-eggs, which suffer reduced viability. In the present study, we supplemented yellow-legged gulls with food during the laying period to experimentally test whether their nutritional conditions were responsible for the observed covariation between c-egg sex and mass. As predicted, food supplementation enhanced female c-eggs'' mass more than that of male c-eggs. Thus, this experiment indicates that mothers strategically allocated their resources to c-eggs, possibly in order to compensate for the larger susceptibility of daughters to hatching (and laying) order. The results also suggested that mothers decided on resource allocation depending on the sex of already ovulated c-eggs, rather than ovulating ova of either sex depending on food availability.     

Variation in body size in the giant rhinoceros beetle Trypoxylus dichotomus is mediated by maternal effects on egg size

1. The egg size of insects can vary depending on maternal body size or resource status, and it may influence offspring body size by determining initial resource level. 2. The giant rhinoceros beetle Trypoxylus dichotomus exhibits considerable variation in body size, some of which is attributed to the variation in larval food (humus) quality, although a substantial amount of variation in body size remains unexplained. In the present study, changes in the egg size and offspring body size in response to several maternal variables were examined (i.e. body size, age, and, nutritional status). 3. Nutritional intake of the females during the adult stage did not affect the egg size. Larvae hatched from small eggs partially recovered from the initial disadvantage during their ontogenetic processes by increasing growth rate (i.e. compensatory growth); however, there was still a positive relationship between egg size and pupal body size. 4. Older females produced small eggs, but because of compensatory growth, the pupae were no longer small. By contrast, due to a lack of compensatory growth, small females produced small eggs as well as small pupae. 5. These results suggest that maternal body size affects offspring body size through effects on egg size. This transgenerational effect may account for some of the variation in adult body size of T. dichotomus.