Variation In Offspring Phenotypes Research Articles

Effect of maternal ammonia stress on population dynamics of the rotifer Brachionus calyciflorus offspring.

Maternal effects play important roles in phenotypic variations among individuals and are thus considered to regulate population performance in responses to environmental stress. High ammonia levels are known to suppress population growth of the rotifer Brachionus calyciflorus. However, it remains unclear whether maternal environmental ammonia stress influences the offspring phenotypic variation and, if so, how it affects the offspring population dynamics in the rotifer. The present work examined variations in life history, morphology, feeding and digestive activities of B. calyciflorus offspring affected by maternal ammonia stress and the effect of the above variations on offspring population dynamics. We observed increased fitness in the offspring population affected by the cumulative maternal effect. There was a trade-off between offspring (F1) survival and reproductive investment under maternal (F0) ammonia stress. Population growth of the offspring possibly increased via decreasing body size and posterolateral spine length while enhancing cellulase activity. Moreover, the absence of the posterolateral spine of the rotifer was a sensitive response to maternal ammonia stress. These findings underscore maternal environmental stress as an important source of phenotypic variations and highlight these multiple responses work together to affect population dynamics.

DNA Methylation Profiles Suggest Intergenerational Transfer of Maternal Effects.

The view of maternal effects (nongenetic maternal environmental influence on offspring phenotype) has changed from one of distracting complications in evolutionary genetics to an important evolutionary mechanism for improving offspring fitness. Recent studies have shown that maternal effects act as an adaptive mechanism to prepare offspring for stressful environments. Although research into the magnitude of maternal effects is abundant, the molecular mechanisms of maternal influences on offspring phenotypic variation are not fully understood. Despite recent work identifying DNA methylation as a potential mechanism of nongenetic inheritance, currently proposed links between DNA methylation and parental effects are indirect and primarily involve genomic imprinting. We combined a factorial breeding design and gene-targeted sequencing methods to assess inheritance of methylation during early life stages at 14 genes involved in growth, development, metabolism, stress response, and immune function of Chinook salmon (Oncorhynchus tshawytscha). We found little evidence for additive or nonadditive genetic effects acting on methylation levels during early development; however, we detected significant maternal effects. Consistent with conventional maternal effect data, maternal effects on methylation declined through development and were replaced with nonadditive effects when offspring began exogenous feeding. We mapped methylation at individual CpG sites across the selected candidate genes to test for variation in site-specific methylation profiles and found significant maternal effects at selected CpG sites that also declined with development stage. While intergenerational inheritance of methylated DNA is controversial, we show that CpG-specific methylation may function as an underlying molecular mechanism for maternal effects, with important implications for offspring fitness.

Maternal investment in last-laid eggs does not compensate for hatching asynchrony in a seabird.

Maternal and environmental effects can have profound effects on offspring performance by generating variation in offspring phenotypes, independent of genetic effects. Within avian broods, differential maternal investment of resources across the laying sequence is thought to be an adaptive strategy to modulate competitive hierarchies induced by hatching asynchrony. In this study, we evaluated the relative importance of maternally derived within-clutch variation and the asymmetric post-hatching environment for growth and survival of common tern (Sterna hirundo) siblings. We experimentally manipulated hatching order, resulting in chicks from last-laid eggs hatching first and vice versa. Although both initial age and size asymmetries were larger within experimental than control broods, the early survival of last-hatched chicks was similar between groups. Initial positive effects of egg size disappeared as siblings approached fledging. Ultimately at fledging, both within-brood growth and cumulative survival patterns were similar between experimental and control broods, suggesting that the effects of systematic variation of egg constituents (e.g., maternally derived yolk hormones) and egg size are too subtle and largely overwhelmed by the effects of hatching asynchrony. Therefore, we conclude that variation in offspring phenotypes is pre-dominantly determined by the social environment experienced post-hatching. Maternal effects may further fine-tune phenotypic variation in response to varying environmental conditions, but this needs to be tested through empirical studies in which multiple maternal effects are measured simultaneously under different environmental conditions.

Chaperones, Canalization, and Evolution of Animal Forms.

Over half a century ago, British developmental biologist Conrad Hal Waddington proposed the idea of canalization, that is, homeostasis in development. Since the breakthrough that was made by Rutherford and Lindquist (1998), who proposed a role of Hsp90 in developmental buffering, chaperones have gained much attention in the study of canalization. However, recent studies have revealed that a number of other molecules are also potentially involved in canalization. Here, I introduce the emerging role of DnaJ chaperones in canalization. I also discuss how the expression levels of such buffering molecules can be altered, thereby altering organismal development. Since developmental robustness is maternally inherited in various organisms, I propose that dynamic bet hedging, an increase in within-clutch variation in offspring phenotypes that is caused by unpredictable environmental challenges to the mothers, plays a key role in altering the expression levels of buffering molecules. Investigating dynamic bet hedging at the molecular level and how it impacts upon morphological phenotypes will help our understanding of the molecular mechanisms of canalization and evolutionary processes.

Maternal Trophic Status and Offpsring Phenotype in a Marine Invertebrate

Offspring size variation in relation to maternal size and season is characteristic of a range of species living in seasonal environments. Little is known about the proximate mechanisms explaining the links between maternally driven variation in offspring phenotypes, for instance when mothers have different diets depending on their size or the season. Here, we use stable isotopes techniques to quantify size dependent and seasonal variations in diet in mothers of shrimp Palaemon serratus and explore possible links between maternal diet and phenotype of embryos and freshly hatched larvae. We found that larger females, which occur more frequently in winter, produce larvae with higher carbon and nitrogen content as well as higher percent carbon, than smaller mothers collected in winter. In addition, isotopic composition suggest that larger mothers collected in winter, were feeding at a higher trophic level, or on an enriched prey pool compared with smaller mothers collected in summer. Overall, there seems to be a strong association between offspring size and maternal diet, mediated by maternal size and/or season.

Age-related parental care in a long-lived bird: implications for offspring development

In long-lived species, behaviour is expected to vary across the lifespan, first improving with maturation and experience and then declining with senescence, but measurement is rare, particularly during old age. Measuring nest defence intensity in 255 known-age blue-footed boobies (Sula nebouxii) of 19 age classes confirmed the inverted-U pattern: intensity of nest defence increased in young males and females until roughly 11–12 years and declined progressively afterwards. We discuss the processes that may generate this distinctive pattern. Regardless of the underlying processes, this study establishes the existence of age-related variation in parental care in a long-lived species. Natural variation in natal conditions has recently been shown to have long-term impacts on development, so this study raises the question whether age-related changes in parental care generate systematic variation in offspring phenotypes. In theory, age-related change in parental care can result in differences among offspring produced at different ages. However, parental behaviour has never been measured over the whole age-span of any long-lived species because of the difficulty of sampling very old animals in the field. We measured intensity of nest defence over the age-span and confirmed that blue-footed boobies exhibit an age-related quadratic pattern in this parental behaviour: defence intensity increases in early life and declines progressively afterwards. Our results imply that similar-shaped patterns may exist in other components of parental care, such as feeding and social interaction, potentially affecting the long-term development of offspring.

Offspring development and life‐history variation in a water flea depends upon clone‐specific integration of genetic, non‐genetic and environmental cues

Summary Theory predicts that offspring developmental strategies involve the integration of genetic, non‐genetic and environmental ‘cues’. But it is unclear how cue integration is achieved during development, and whether this pattern is general or genotype specific. In order to test this, we manipulated the maternal and offspring environments of three genetically distinct clones of the water flea Daphnia magna taken from different populations. We then quantified the effect that the genotype, maternal environment and the offspring environment had on the development and life histories of the three different clones. Mothers responded to the same maternal environments in different ways, resulting in clone‐specific maternal effects on neonate size. Offspring responses to maternal cues varied according to the trait in question and were also clone specific. The integration of these maternal effects during development was highly context dependent in two clones but more consistent across environments in the third. Genetic, non‐genetic and environmental cues contributed to offspring phenotypic variation in all three clones, but there was no general pattern linking traits to specific cues. In fact, two clones used different combinations of cues at different points in development to achieve similar phenotypic outcomes. Reaction norms for the age and size at which maturation was initiated differed among genotypes, between maternal environments and across current environments. Developmental transitions such as the decision to mature may thus play an important role in determining patterns of cue integration. Considering multiple traits during development demonstrated that variation in the integration of genetic, non‐genetic and environmental cues was an important determinant of life‐history variation among D. magna genotypes. This variation is likely to influence phenotypic evolution. A lay summary is available for this article.

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.

A comparative perspective on epigenetics

Ever since Watson and Crick signed off their 1953 Nature paper with the closing line, ‘It has not escaped our notice that the specific pairing we have postulated immediately suggests a possible copying mechanism for the genetic material’, we have lived in an age of genes and genomes. And before

Sex-specific traits in Common Tern Sterna hirundo chicks: associations with rearing environment, parental factors and survival

Offspring phenotypic variation has important consequences for the future survival, reproductive success and individual fitness of nestlings, but the sex-specific reproductive value and fitness returns for parents of this variation have only rarely been explored. We analysed twelve phenotypic traits of nestling Common Terns (Sterna hirundo) in relation to their sex, age and hatching date, and explored whether sexual differences in these traits were associated with the rearing environment and survival. In addition, we studied sex-specific differences in offspring phenotype related to parental factors, since the existence of sexual dimorphism may reflect differential parental investment. Bill–head length and mediated immune response varied in relation to offspring sex, with males showing larger values than females. Immune response was also affected by environmental (year), rearing (competition over 14 days old) and parental (clutch size) factors. None of the morphological, serological and immunological variables were associated with chick mortality, but female nestlings that did not survive had suffered longer periods of within-brood competition. Although some parental traits influenced offspring phenotype, sexual differences among nestlings did not vary in relation to parental age, mass or arrival date, which may imply that there is no great difference in cost between raising sons and raising daughters, and thus no adjustment of parental effort in relation to nestling sex. However, the evidence that immune response was higher for sons in larger clutches that were raised with siblings indicates a difference in the developmental strategies for sons and daughters, which may be related to their reproductive value. These results therefore provide evidence of certain pathways for parental sex allocation that may differentially affect sons and daughters.

Maternal and additive genetic effects contribute to variation in offspring traits in a lizard

Evolutionary responses to selection require that traits have a heritable basis, yet maternal effects (the effect of a mother's phenotype on her offspring's phenotype) can have profound effects on evolutionary processes. It is therefore essential to understand how maternal effects contribute to phenotypic variation in offspring traits and test key assumptions of additive genetic variance in evolutionary models. We measured 5 traits linked to fitness in lizards (endurance, sprint speed, snout-vent length [SVL], mass, and growth rate) and estimated the contribution of additive genetic and maternal effects in explaining variation in these traits in the Eastern water skink (Eulamprus quoyii). We estimated parentage using 6 microsatellite DNA loci from lizards taking part in a mating experiment in large seminatural enclosures and used animal models to partition variance into additive genetic and maternal effects. We found that only endurance was significantly heritable (h(2) = 0.37, 95% credible interval = 0.18-0.50), whereas all other traits were either strongly influenced by maternal effects (mass, sprint speed, SVL, and captive growth rate) or were influenced by environmental variability (wild growth rate). Our study disentangles the relative contributions of additive genetic and maternal effects in contributing to variation in offspring phenotypes and suggests that little additive genetic variance exists for traits often assumed to be heritable. Although the heritability of phenotypic traits is essential in evolutionary models, our results also highlight the important role maternal effects have in explaining variation in phenotypes.

The influence of parental effects on transcriptomic landscape during early development in brook charr (Salvelinus fontinalis, Mitchill)

Parental effects represent an important source of variation in offspring phenotypes. Depending on the specific mechanisms involved, parental effects may be caused to different degrees by either the maternal or the paternal parent, and these effects may in turn act at different stages of development. To detect parental effects acting on gene transcription regulation and length phenotype during ontogeny, the transcriptomic profiles of two reciprocal hybrids from Laval × Rupert and Laval × Domestic populations of brook charr were compared at hatching, yolk sac resorption and 15 weeks after exogenous feeding. Using a salmonid cDNA microarray, our results show that parental effects modulated gene expression among reciprocal hybrids only at the yolk sac resorption stage. In addition, Laval × Domestic and Laval × Rupert reciprocal hybrids differed in the magnitude of theses parental effects, with 199 and 630 differentially expressed transcripts, respectively. This corresponds to a maximum of 18.5% of the analyzed transcripts. These transcripts are functionally related to cell cycle, nucleic acid metabolism and intracellular protein traffic, which is consistent with observed differences associated with embryonic development and growth differences in other fish species. Our results thus illustrate how parental effects on patterns of gene transcription seem dependent on the genetic architecture of the parents. In addition, in absence of transcriptional differences, non-transcript deposits in the yolk sac could contribute to the observed length differences among the reciprocal hybrids before yolk sac resorption.

Egg testosterone affects wattle color and trait covariation in the ring-necked pheasant

Transfer of maternal hormones to the eggs is a major source of offspring phenotypic variation. The developmental and organizational effects of egg hormones can extend into adulthood and affect behavioral and morphological traits involved in sexual and reproductive behavior, with important consequences for offspring fitness. In this study, we injected testosterone (T) in egg albumen of captive ring-necked pheasant (Phasianus colchicus) eggs. We then assessed the consequences for chick growth, cell-mediated immunity, and multiple male secondary sexual traits at maturity by comparison with a control group. We also compared the covariation between traits in the two experimental groups. We found that control males had redder wattles than males from T-injected eggs, suggesting that attractiveness and reproductive success of the offspring might vary depending on maternal transfer of T to the eggs. T treatment also modified the covariation between cell-mediated immunity and wattle coloration and between the area of the wattle and the expression of another secondary sexual trait, the ear tufts. These effects are likely to translate into fitness differences among the offspring if mate acquisition depends on the simultaneous expression of several traits that are differentially affected by the same maternal contribution. Maternal effects mediated by egg hormones might affect the fitness of the offspring not only by directional modification of phenotypic traits, but also by facilitating or inhibiting their covariation. This suggests the possibility that female choice based on the relative expression of multiple secondary sexual traits exerts a pressure on how maternal transfer of androgens contributes to developmental programs.

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.

Climate and geographic trends in hatch delay of the treehole mosquito, Aedes triseriatus Say (Diptera: Culicidae)

Eggs of Aedes triseriatus mosquitoes are stimulated to hatch when inundated with water, but only a small fraction of eggs from the same batch will hatch for any given stimulus. Similar hatching or germination patterns are observed in desert plants, copepods, rotifers, insects, and many other species. Bet hedging theory suggests that parents stagger offspring emergence into vulnerable life history stages in order to avoid catastrophic reproductive failures. For Ae. triseriatus, a treehole breeding mosquito, immediate hatching of an entire clutch leaves all of the parent's progeny vulnerable to extinction in the event of a severe drought. Natural selection has likely favored parents that pursued a bet hedging strategy where the risk of reproductive failure is distributed over time. Considering treehole mosquitoes, bet hedging theory could be used to predict that hatch delay would be positively correlated with the likelihood of drought. To test this prediction, we collected Ae. triseriatus from habitats that varied widely in mean annual precipitation and exposed them to several hatch stimuli in the laboratory. Here we report that, as predicted, Ae. triseriatus eggs from high precipitation regions showed less hatch delay than areas of low precipitation. This strategy probably allows Ae. triseriatus to cope with the wide variety of climatic conditions that it faces in its extensive geographical range.

The effects of incubation temperature on the morphology and composition of Australian Brush-turkey (Alectura lathami) chicks

Environmental heterogeneity during embryonic development generates an important source of variation in offspring phenotypes and can influence the evolution of life histories. The effects of incubation temperature on offspring phenotypes in reptiles has been well documented but remains relatively unexplored in birds as their embryos typically develop over a narrow range of temperatures. Megapode birds (Order Galliformes; Family Megapodiidae) are unique in that their embryos tolerate and develop over a wide range of incubation temperatures, yet little is known of the effect that temperature has on hatchling morphology and composition. Australian Brush-turkey eggs collected on the day of laying were incubated in the laboratory under constant temperatures of 32, 34 and 36 degrees C until hatching in order to determine the influence of temperature on hatchling mass, size and composition. The dry mass of the yolk-free body and residual yolk of hatchlings were temperature dependent, such that higher temperatures produced chicks of lesser yolk-free body mass and greater residual yolk mass than chicks incubated at lower temperatures. However the overall size (linear dimensions) and lipid, protein and ash content of chicks were independent of temperature.

Maternal influences on offspring phenotypes and sex ratios in a multi-clutching lizard with environmental sex determination

Maternal and environmental factors are important sources of phenotypic variation because both factors influence offspring traits in ways that impact offspring and maternal fitness. The present study explored the effects of maternal factors (maternal body size, egg size, yolk-steroid allocation, and oviposition-site choice) and seasonally-variable environmental factors on offspring phenotypes and sex ratios in a multi-clutching lizard with environmental sex determination (Amphibolurus muricatus). Maternal identity had strong effects on offspring morphology, but the nature of maternal effects differed among successive clutches produced by females throughout the reproductive season (i.e. maternal identity by environment interactions). The among-female and among-clutch variation in offspring traits (including sex ratios) was not mediated through maternal body size, egg size, or variation in yolk steroid hormones. This lack of nongenetic maternal effects suggests that phenotypic variation may be generated by gene by environment interactions. These results demonstrate a significant genetic component to variation in offspring phenotypes, including sex ratios, even in species with environmental sex determination. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95, 256–266.

THE COST OF REPRODUCTION INDUCED BY BODY SIZE AT BIRTH AND BREEDING DENSITY

Body size at birth has implications for the quality of individuals throughout their life. Although large body size is generally considered an advantage, the relationship between body size at birth and long-term fitness is often complicated. Under spatial or temporal variation in environmental conditions, such as the seasonally changing densities of Fennoscandian vole populations, selection should favor variation in offspring phenotypes, as different qualities may be beneficial in different conditions. We performed an experiment in which a novel hormonal manipulation method was used to increase phenotypic variance in body size at birth in the bank vole (Myodes glareolus). The effects of body size on the future fitness of young males and females were then studied at varying population densities in outdoor enclosures. Our results show that small body size at birth and high breeding density increase the survival costs of reproduction. However, there was no interaction between the effects of body size and density on survival, which suggests that the fitness effects of body size were strong enough to persist under environmental variation. Moreover, litter size and the probability of breeding were more sensitive to variation in breeding density than offspring size. Therefore, it is unlikely that individual fitness could be optimized by adjusting offspring body size to the prevailing population density through adaptive maternal effects. Our results highlight the significance of the costs of reproduction in the evolution of life-history traits, and give strong experimental support for the long-term fitness effects of body size at birth.

Early maternal, genetic and environmental components of antioxidant protection, morphology and immunity of yellow-legged gull (Larus michahellis) chicks

Maternal effects mediated by egg quality are important sources of offspring phenotypic variation and can influence the course of evolutionary processes. Mothers allocate to the eggs diverse antioxidants that protect the embryo from oxidative stress. In the yellow-legged gull (Larus michahellis), yolk antioxidant capacity varied markedly among clutches and declined considerably with egg laying date. Analysis of bioptic yolk samples from clutches that were subsequently partially cross-fostered revealed a positive effect of yolk antioxidant capacity on embryonic development and chick growth, but not on immunity and begging behaviour, while controlling for parentage and common environment effects. Chick plasma antioxidant capacity varied according to rearing environment, after statistically partitioning out maternal influences mediated by egg quality. Thus, the results of this study indicate that egg antioxidants are important mediators of maternal effects also in wild bird populations, especially during the critical early post-hatching phase.

IMPACT OF NEST-SITE SELECTION ON NEST SUCCESS AND NEST TEMPERATURE IN NATURAL AND DISTURBED HABITATS

Nest-site selection behavior is a maternal effect that contributes to offspring survival and variation in offspring phenotypes that are subject to natural selection. We investigated nest-site selection and its consequences in the snapping turtle, Chelydra serpentina, in northwestern Illinois. We evaluated nest-site selection at both the microhabitat and habitat patch levels. Turtles selected nest sites with shorter vegetation, more open sand, and fewer cacti than random locations. These microhabitat characteristics described sandy patches where both nest density and success were higher compared to grassy patches in 1999. We subsequently investigated nest-site selection within two discrete subdivisions of the study area that varied in the degree of human disturbance to determine if nesting behavior, nest success, or nest temperatures were affected. The tendency to nest in sandy patches was much stronger at the natural site due to habitat modifications at the residential site that have blurred the distinction between sandy and grassy patches. Additionally, the residential site had a high density of nests within 5 m of houses and a fence (both areas with disturbed habitat similar to sandy patches), compared to the overall density. Thus, nest success associated with sandy patches may be compromised at the residential site; an ecological trap may result in lower nest success in areas with preferred microhabitat characteristics. Despite a similar basis for nest-site selection in terms of microhabitat characteristics at both sites, nest temperatures were correlated with microhabitat characteristics used to select nest sites only at the natural site. Nest temperatures at the residential site were instead correlated only with the percentage overstory vegetation cover and therefore averaged 2°C lower than at the natural site, a temperature difference that influenced offspring sex. The higher percentage overstory vegetation cover at the residential site was due to human alterations of the habitat, and may serve to extend the ecological trap biasing the sex ratio of this population. This study illustrates the importance of (1) nest-site selection as a substantive maternal effect, (2) understanding habitat use during crucial life-history events, and (3) the potential for human disturbance to modify offspring phenotypes and negatively impact nest success despite adaptive nesting behavior.