Effects of maternal diet on offspring fitness in the bird cherry‐oat aphid

1. Maternal and offspring diet effects on life‐history traits of the bird cherry‐oat aphid Rhopalosiphum padi were tested on three wheat varieties. Using nine reciprocal combinations of wheat varieties, the effects of previous experience (maternal diet effect) on the aphid's response to resistant and susceptible varieties (offspring diet effect) were tested. Batis was susceptible, and Xiaoyan22 and Ww2730 were both resistant, but with different mechanisms. 2. Aphids produced the most alatae in the treatments with the most resistant maternal diet variety Xiaoyan22. The fecundity (F) and intrinsic rate of increase (r_m) of these alatae were at their greatest in the most resistant offspring diet variety, but these traits were not influenced in the apterae. 3. There were significant interactions in the alatae production and apterae life‐history traits, such as r_m, development time, weight gain, and mean relative growth rate, between the maternal and offspring diet varieties. The interactions in apterae responses between varieties, some of which were reciprocal, indicated phenotypic plasticity in these parthenogenetic aphids. 4. Rhopalosiphum padi produced more alatae on the most resistant variety; the alatae would disperse and were more fecund. The growth responses of the apterae showed phenotypic plasticity to the different combinations of maternal and offspring diet varieties. The phenotypic plasticity would allow R. padi to better utilise the variable environments represented by the small wheat plots of different varieties in China.     

Altitudinal divergence in maternal thermoregulatory behaviour may be driven by differences in selection on offspring survival in a viviparous lizard

Plastic responses to temperature during embryonic development are common in ectotherms, but their evolutionary relevance is poorly understood. Using a combination of field and laboratory approaches, we demonstrate altitudinal divergence in the strength of effects of maternal thermal opportunity on offspring birth date and body mass in a live-bearing lizard (Niveoscincus ocellatus). Poor thermal opportunity decreased birth weight at low altitudes where selection on body mass was negligible. In contrast, there was no effect of maternal thermal opportunity on body mass at high altitudes where natural selection favored heavy offspring. The weaker effect of poor maternal thermal opportunity on offspring development at high altitude was accompanied by a more active thermoregulation and higher body temperature in highland females. This may suggest that passive effects of temperature on embryonic development have resulted in evolution of adaptive behavioral compensation for poor thermal opportunity at high altitudes, but that direct effects of maternal thermal environment are maintained at low altitudes because they are not selected against. More generally, we suggest that phenotypic effects of maternal thermal opportunity or incubation temperature in reptiles will most commonly reflect weak selection for canalization or selection on maternal strategies rather than adaptive plasticity to match postnatal environments.     

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

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

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.

     

Chronic maternal stress affects growth, behaviour and hypothalamo-pituitary-adrenal function in juvenile offspring

Maternal stress during pregnancy, particularly that combined with low socioeconomic status (SES), has been linked to an increased risk for impaired behavioural and emotional development and affective disorders in children. In animal models, acute periods of prenatal stress have profound effects on hypothalamo-pituitary-adrenal (HPA) function and behaviour. However, few studies have determined the impact of chronic exposure to stress in animal models. The objective of this study was to determine the effects of chronic maternal stress (CMS) during the 2nd half of pregnancy and nursing on growth, locomotor behaviour and HPA axis function in juvenile guinea pig offspring. Pregnant guinea pigs were exposed to a random combination of variable stressors every other day over the 2nd half of gestation and from postnatal day (pnd) 1 until weaning (pnd25). CMS mothers displayed increased basal salivary cortisol levels in the later stages of pregnancy compared to control mothers (p < 0.05). The male offspring of CMS mothers had a lower bodyweight, which was maintained to weaning (p < 0.01). In open-field testing, CMS male offspring showed a decrease in activity compared to controls (p < 0.05). There was no effect of CMS on bodyweight or activity in female offspring. In contrast, both male and female offspring born to CMS mothers displayed increased (p < 0.05) basal salivary cortisol at pnd25, but a blunted adrenocortical response to exposure to the novel open-field enclosure. In conclusion, CMS leads to modification of growth trajectory, locomotor activity and adrenocortical responses to stress in juvenile offspring. Further, males appear considerably more vulnerable to these effects than females.     

Drought affects the coordination of belowground and aboveground resource‐related traits in Solidago canadensis in China

Quantifying patterns of variation and coordination of plant functional traits can help to understand the mechanisms underlying both invasiveness and adaptation of plants. Little is known about the coordinated variations of performance and functional traits of different organs in invasive plants, especially in response to their adaptation to environmental stressors. To identify the responses of the invasive species Solidago canadensis to drought, 180 individuals were randomly collected from 15 populations and 212 ramets were replanted in a greenhouse to investigate both the response and coordination between root and leaf functional traits. Drought significantly decreased plant growth and most of the root and leaf functional traits, that is, root length, surface area, volume and leaf size, number, and mass fraction, except for the root length ratio and root mass fraction. Phenotypic plasticity was higher in root traits than in leaf traits in response to drought, and populations did not differ significantly. The plasticity of most root functional traits, that is, root length (RL), root surface area (RSA), root volume (RV), and root mass fraction (RMF), were significantly positively correlated with biomass between control and drought. However, the opposite was found for leaf functional traits, that is, specific leaf area (SLA), leaf area ratio (LAR), and leaf mass fraction (LMF). Drought enhanced the relationship between root and leaf, that is, 26 pairwise root–leaf traits were significantly correlated under drought, while only 15 pairwise root–leaf traits were significantly correlated under control conditions. Significant correlations were found between biomass and all measured functional traits except for leaf size. RV, root length ratio, RMF, total area of leaves, and LMF responded differently to water availability. These responses enable S. canadensis to cope with drought conditions and may help to explain the reason of the vast ecological amplitude of this species.     

Epigenetic regulation of trophic morphology through feeding behaviour in Arctic charr, Salvelinus alpinus

Several models of speciation suggest that in species that are phenotypically plastic, selection can act on phenotypic variation that is environmentally induced in the earliest stages of divergence. One trait that could be subject to this process is foraging behaviour, where discrete foraging strategies are common. One species which is highly plastic in the expression of phenotype, the Arctic charr, Salvelinus alpinus (L.), is characterized by discrete variation in the anatomy of the head and mouthparts. These traits have been shown to have a functional significance, but the expression of which is thought to be at least partly phenotypically plastic. Here we test the hypothesis that foraging behaviour may regulate the anatomy of the head and mouthparts in Arctic charr. In a dyad experiment, size‐matched pairs of fish from a mixed family group were fed a diet of either Mysis (a hard‐bodied shrimp) or Chironomid larvae. Nine morphometric measures of head dimensions that describe wild trophic morphs were measured at the start of the experiment and 24 weeks later. Principal component scores of size‐corrected morphometric measures showed highly significant differences between fish exposed to the two diets. Univariate ANOVA analysis of the head morphometric variables showed that fish fed on Chironomids developed longer, wider jaws, longer heads and a larger eye for a given body length than did those fish fed upon Mysis. We conclude that foraging anatomy in Arctic charr is phenotypically plastic and that variation in foraging behaviour that results in feeding specialization in the wild could induce variation in head anatomy. This in turn could reinforce foraging specialization. Very rapid epigenetic divergence into distinct feeding morphs (as demonstrated here) would allow selection to act at more than one mode and thus could promote rapid evolutionary divergence, initially prior to genetic segregation, in species which are highly plastic. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 78 , 43–49.     

Developmental temperature affects the expression of ejaculatory traits and the outcome of sperm competition in Callosobruchus maculatus

The outcome of post‐copulatory sexual selection is determined by a complex set of interactions between the primary reproductive traits of two or more males and their interactions with the reproductive traits of the female. Recently, a number of studies have shown the primary reproductive traits of both males and females express phenotypic plasticity in response to the thermal environment experienced during ontogeny. However, how plasticity in these traits affects the dynamics of sperm competition remains largely unknown. Here, we demonstrate plasticity in testes size, sperm size and sperm number in response to developmental temperature in the bruchid beetle Callosobruchus maculatus. Males reared at the highest temperature eclosed at the smallest body size and had the smallest absolute and relative testes size. Males reared at both the high‐ and low‐temperature extremes produced both fewer and smaller sperm than males reared at intermediate temperatures. In the absence of sperm competition, developmental temperature had no effect on male fertility. However, under conditions of sperm competition, males reared at either temperature extreme were less competitive in terms of sperm offence (P₂), whereas those reared at the lowest temperature were less competitive in terms of sperm defence (P₁). This suggests the developmental pathways that regulate the phenotypic expression of these ejaculatory traits are subject to both natural and sexual selection: natural selection in the pre‐ejaculatory environment and sexual selection in the post‐ejaculatory environment. In nature, thermal heterogeneity during development is commonplace. Therefore, we suggest the interplay between ecology and development represents an important, yet hitherto underestimated component of male fitness via post‐copulatory sexual selection.     

Environmental and not maternal effects determine variation in offspring phenotypes in a passerine bird

Maternal and environmental effects can profoundly influence offspring phenotypes, independent of genetic effects. Within avian broods, both the asymmetric post‐hatching environment created by hatching asynchrony and the differential maternal investment through the laying sequence have important consequences for individual nestlings in terms of the allocation of resources to body structures with different contributions to fitness. The purpose of this study was to evaluate the relative importance of post‐hatching environmental and maternal effects in generating variation in offspring phenotypes. First, an observational study showed that within blue tit, Cyanistes caeruleus, broods, late‐hatched nestlings allocated resources to tarsus development, maintained mass gain and head‐bill growth and directed resources away from the development of fourth primary feathers. Second, a hatching order manipulation experiment resulted in nestlings from first‐laid eggs hatching last, thereby allowing comparison with both late and early‐hatched nestlings. Experimental nestlings had growth patterns which were closer to late‐hatched nestlings, suggesting that within‐brood growth patterns are determined by post‐hatching environmental effects. Therefore, we conclude that post‐hatching environmental effects play an important role in generating variation in offspring phenotypes.     

Change in maternal environment induced by cross-fostering alters genetic and epigenetic effects on complex traits in mice

The interaction between maternally provided environment and offspring genotype is a major determinant of offspring development and fitness in many organisms. Recent research has demonstrated that not only genetic effects, but also epigenetic effects may be subject to modifications by the maternal environment. Genomic imprinting resulting in parent-of-origin-dependent gene expression is among the best studied of epigenetic effects. However, very little is known about the degree to which genomic imprinting effects can be modulated by the maternally provided environment, which has important implications for phenotypic plasticity. In this study, we investigated this unresolved question using a cross-fostering design in which mouse pups were nursed by either their own or an unrelated mother. We scanned the entire genome to search for quantitative trait loci whose effects depend on cross-fostering and detected 10 of such loci. Of the 10 loci, 4 showed imprinting by cross-foster interactions. In most cases, the interaction effect was due to the presence of an effect in either cross-fostered or non-cross-fostered animals. Our results demonstrate that genomic imprinting effects may often be modified by the maternal environment and that such interactions can impact key fitness-related traits suggesting a greater plasticity of genomic imprinting than previously assumed.     

Structural complexity in the hatchery rearing environment affects activity,resting metabolic rate and post-release behaviour in brown trout Salmo trutta

The effects of structural enrichment in the hatchery rearing environment of brown trout Salmo trutta was linked to post-release performance. Enrichment resulted in reduced swimming activity scored in an open field test and reduced movement in a natural river after release. Also, enrichment increased resting metabolic rates, which correlated positively with overwinter growth.     

Individual plastic responses by males to rivals reveal mismatches between behaviour and fitness outcomes

Plasticity in behaviour is of fundamental significance when environments are variable. Such plasticity is particularly important in the context of rapid changes in the socio-sexual environment. Males can exhibit adaptive plastic responses to variation in the overall level of reproductive competition. However, the extent of behavioural flexibility within individuals, and the degree to which rapidly changing plastic responses map onto fitness are unknown. We addressed this by determining the behaviour and fitness profiles of individual Drosophila melanogaster males subjected to up to three episodes of exposure to rivals or no rivals, in all combinations. Behaviour (mating duration) was remarkably sensitive to the level of competition and fully reversible, suggesting that substantial costs arise from the incorrect expression of even highly flexible behaviour. However, changes in mating duration matched fitness outcomes (offspring number) only in scenarios in which males experienced zero then high competition. Following the removal of competition, mating duration, but not offspring production, decreased to below control levels. This indicates that the benefit of increasing reproductive investment when encountering rivals may exceed that of decreasing investment when rivals disappear. Such asymmetric fitness benefits and mismatches with behavioural responses are expected to exert strong selection on the evolution of plasticity.     

Quantitative genetics of oviposition behaviour and interactions among oviposition traits in the sand cricket

We performed a quantitative genetic study of oviposition behaviours and oviposition traits in the sand cricket Gryllus firmus. Egg survival in crickets depends on the depth at which they are inserted into the soil with the ovipositor. We examined whether egg depth depends on ovipositor length alone, or on both morphological and behavioural traits associated with oviposition. Heritability estimates were high (h² >0.5) for ovipositor length and small (h²=0.2) for oviposition behaviours. Negative genetic correlations between ovipositor length and some behavioural traits (digging depth and the behavioural component of egg depth) indicated compensation between oviposition traits on egg depth. Because of behavioural compensation, females with different ovipositor lengths subject to stabilizing selection on egg depth could have equal fitnesses. Females laid their eggs deeper, and their eggs were marginally more evenly distributed in dry than in wet sand. This suggests adaptive phenotypic plasticity in laying behaviour, but may also result from physical constraints of the substrate on the insertion of the ovipositor. The absence of significant between-family variation in oviposition traits in response to sand moisture indicates low evolutionary potential for phenotypic plasticity in oviposition traits according to soil moisture. In highly unpredictable environments, females could spread the risk of desiccation by laying eggs at different depths independently of environmental conditions (bet hedging). Our results show significant additive genetic influences on the ability of a female to spread risks as measured by genetic variation in egg distribution, suggesting that a bet-hedging strategy of egg laying has the potential to evolve in this population. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Canalisation in the wild: effects of developmental conditions on physiological traits are inversely linked to their association with fitness

Ecological conditions affect fitness, but mechanisms causing such effects are not well known, while evolved responses to environmental variation may depend on the underlying mechanisms. Consequences of environmental conditions vary strongly between traits, but a framework to interpret such variation is lacking. We propose that variation in trait response may be explained by differential canalisation, with traits with larger fitness effects showing weaker responses to environmental perturbations due to preferential resource allocation to such traits. We tested the canalisation hypothesis using brood size manipulation in wild jackdaw nestlings in which we measured eight physiological traits (mainly oxidative stress markers), and two feather traits. For each trait, we estimated manipulation response and association with fitness (over‐winter survival). As predicted, a strong negative correlation emerged between manipulation response and association with fitness (r =?0.76). We discuss the consequences of differential trait canalisation for the study of mechanisms mediating environmental effects on fitness.     

Fitness consequences of maternal and grandmaternal effects

Transgenerational effects are broader than only parental relationships. Despite mounting evidence that multigenerational effects alter phenotypic and life‐history traits, our understanding of how they combine to determine fitness is not well developed because of the added complexity necessary to study them. Here, we derive a quantitative genetic model of adaptation to an extraordinary new environment by an additive genetic component, phenotypic plasticity, maternal and grandmaternal effects. We show how, at equilibrium, negative maternal and negative grandmaternal effects maximize expected population mean fitness. We define negative transgenerational effects as those that have a negative effect on trait expression in the subsequent generation, that is, they slow, or potentially reverse, the expected evolutionary dynamic. When maternal effects are positive, negative grandmaternal effects are preferred. As expected under Mendelian inheritance, the grandmaternal effects have a lower impact on fitness than the maternal effects, but this dual inheritance model predicts a more complex relationship between maternal and grandmaternal effects to constrain phenotypic variance and so maximize expected population mean fitness in the offspring.