Parental environmental effects on life history traits in Arabidopsis thaliana (Brassicaceae)

Environmentally induced maternal effects on offspring phenotype are well known in plants. When genotypes or maternal lineages are replicated and raised in different environmental conditions, the phenotype of their offspring often depends on the environment in which the parents developed. However, the degree to which such maternal effects are maintained over subsequent generations has not been documented in many taxa. Here we report the results of a study designed to assess the effects of parental environment on vegetative and reproductive traits, using glasshouse-raised maternal lines sampled from natural populations of Arabidopsis thaliana . Replicates of five highly selfed lines from each of four wild populations were cultivated in two abiotic environments in the glasshouse, and the quality and performance of seeds derived from these two environments were examined over two generations. We found that offspring phenotype was strongly influenced by parental environment, but because the parental environments differed with respect to the time of seed harvest, it was not possible to distinguish clearly between parental environmental effects and the possible (but unlikely) effects of seed age on offspring phenotype. We observed a rapid decline in the expression of ancestral environmental effects, and no main environmental effects on progeny phenotype persisted in the second generation. The mechanism of transmission of environmental effects did not appear to be associated with the quantity or quality of reserves in the seeds, suggesting that environmental effects may be transmitted across subsequent generations via some mechanism that generates environment-specific gene expression.     

Parental condition affects early life-history of a coral reef fish

Parents can exert a range of non-genetic effects on the growth and survival of their offspring. In particular, parents may modify the size or condition of their offspring depending on the amount of energy they have available for reproduction. In this study, the body condition of breeding pairs of the coral reef fish Acanthochromis polyacanthus was experimentally manipulated to test the effects of parental condition on reproductive output and offspring life history traits. Parents in good condition commenced breeding earlier, had higher reproductive output, and their eggs exhibited increased survival during embryogenesis, compared to parents in poorer condition. Increased reproductive output was attained through more reproductive bouts over the breeding season that contained both a greater number and an increased size of eggs. The offspring from parents in good condition were larger at hatching, with larger yolk reserves and increased survival on endogenous reserves. Larger size is expected to provide benefits to offspring through reduced susceptibility to size-selective mortality. The range of offspring characteristics modified by parental condition could result in a greater proportion of offspring from good condition parents recruiting to the population.     

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.     

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

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

COMPLEX INTERACTIONS BETWEEN PATERNAL AND MATERNAL EFFECTS: PARENTAL EXPERIENCE AND AGE AT REPRODUCTION AFFECT FECUNDITY AND OFFSPRING PERFORMANCE IN A BUTTERFLY

Parental effects can greatly affect offspring performance and are thus expected to impact population dynamics and evolutionary trajectories. Most studies have focused on maternal effects, whereas fathers are also likely to influence offspring phenotype, for instance when males transfer nutrients to females during mating. Moreover, although the separate effects of maternal age and the environment have been documented as a source of parental effects in many species, their combined effects have not been investigated. In the present study, we analyzed the combined effects of maternal and paternal age at reproduction and a mobility treatment in stressful conditions on offspring performance in the butterfly Pieris brassicae. Both paternal and maternal effects affected progeny traits but always via interactions between age and mobility treatment. Moreover, parental effects shifted from male effects expressed at the larval stage to maternal effects at the adult stage. Indeed, egg survival until adult emergence significantly decreased with father age at mating only for fathers having experienced the mobility treatment, whereas offspring adult life span decreased with increasing mother age at laying only for females that did not experience the mobility treatment. Overall, our results demonstrate that both parents’ phenotypes influence offspring performance through nongenetic effects, their relative contribution varying over the course of progeny's life.     

Parental effects in Plantago lanceolata L. III. Measuring parental temperature effects in the field

To determine the evolutionary importance of parental environmental effects in natural populations, we must begin to measure the magnitude of these effects in the field. For this reason, we conducted a combined growth chamber-field experiment to measure parental temperature effects in Plantago lanceolata. We grew in the field offspring of controlled crosses of chamber-grown parents subjected to six temperature treatments. Each treatment was characterized by a unique combination of maternal prezygotic (prior to fertilization), paternal prezygotic, and postzygotic (during fertilization and seed set) temperatures. Offspring were followed for three years to measure the effects of treatment on several life-history traits and population growth rate, our estimate of fitness. Parental treatment influenced germination, growth, and reproduction of newborns, but not survival or reproduction of offspring at least one year old. High postzygotic temperature significantly increased germination and leaf area at 17 weeks by approximately 35% and 2%, respectively. Probability of flowering and spike production in the newborn age class showed significant parental genotype x parental treatment interactions. High postzygotic temperature increased offspring fitness by approximately 50%. The strongest contributors to fitness were germination and probability of flowering and spike production of newborns. A comparison of our data with previously collected data for chambergrown offspring shows that the influence of parental environment on offspring phenotype is weaker but still biologically meaningful in the field. The results provide evidence that parental environment influences offspring fitness in natural populations of P. lanceolata and does so by affecting the life-history traits most strongly contributing to fitness. The data suggest that from the perspective of offspring fitness, natural selection favors parents that flower later in the flowering season in the North Carolina Piedmont when it is warmer. Genotypic-specific differences in response of offspring reproductive traits to parental environment suggest that parental environmental effects can influence the rate of evolutionary change in P. lanceolata.     

Transgenerational interactions involving parental age and immune status affect female reproductive success in Drosophila melanogaster

It is well established that the parental phenotype can influence offspring phenotypic expression, independent of the effects of the offspring''s own genotype. Nonetheless, the evolutionary implications of such parental effects remain unclear, partly because previous studies have generally overlooked the potential for interactions between parental sources of non-genetic variance to influence patterns of offspring phenotypic expression. We tested for such interactions, subjecting male and female Drosophila melanogaster of two different age classes to an immune activation challenge or a control treatment. Flies were then crossed in all age and immune status combinations, and the reproductive success of their immune- and control-treated daughters measured. We found that daughters produced by two younger parents exhibited reduced reproductive success relative to those of other parental age combinations. Furthermore, immune-challenged daughters exhibited higher reproductive success when produced by immune-challenged relative to control-treated mothers, a pattern consistent with transgenerational immune priming. Finally, a complex interplay between paternal age and parental immune statuses influenced daughter''s reproductive success. These findings demonstrate the dynamic nature of age- and immune-mediated parental effects, traceable to both parents, and regulated by interactions between parents and between parents and offspring.     

Transgenerational effects of parental larval diet on offspring development time, adult body size and pathogen resistance in Drosophila melanogaster

Environmental conditions experienced by parents are increasingly recognized to affect offspring performance. We set out to investigate the effect of parental larval diet on offspring development time, adult body size and adult resistance to the bacterium Serratia marcescens in Drosophila melanogaster. Flies for the parental generation were raised on either poor or standard diet and then mated in the four possible sex-by-parental diet crosses. Females that were raised on poor food produced larger offspring than females that were raised on standard food. Furthermore, male progeny sired by fathers that were raised on poor food were larger than male progeny sired by males raised on standard food. Development times were shortest for offspring whose one parent (mother or the father) was raised on standard and the other parent on poor food and longest for offspring whose parents both were raised on poor food. No evidence for transgenerational effects of parental diet on offspring disease resistance was found. Although paternal effects have been previously demonstrated in D. melanogaster, no earlier studies have investigated male-mediated transgenerational effects of diet in this species. The results highlight the importance of not only considering the relative contribution each parental sex has on progeny performance but also the combined effects that the two sexes may have on offspring performance.     

Position in the laying order has sex-specific consequences for reproductive success in adult black-headed gulls

Mothers who produce multiple offspring within one reproductive attempt often allocate resources differentially; some maternally derived substances are preferentially allocated to last-produced offspring and others to first-produced offspring. The combined effect of these different allocation regimes on the overall fitness of offspring produced early or late in the sequence is not well understood, partly because production order is often coupled with birth order, making it difficult-to-separate effects of pre-natal maternal allocation from those of post-natal social environments. In addition, very little is known about the influence of laying order on fitness in later life. In this study, we used a semi-natural captive colony of black-headed gulls to test whether an offspring's position in the laying order affected its early-life survival and later-life reproductive success, independent of its hatching order. Later-laid eggs were less likely to hatch, but among those that did, survival to adulthood was greater than that of first-laid eggs. In adulthood, the laying order of females did not affect their likelihood of breeding in the colony, but male offspring hatched from last-laid eggs were significantly less likely to gain a breeding position than earlier-laid males. In contrast, later-laid female parents hatched lower proportions of their clutches than first-laid females, but hatching success was unrelated to the laying order of male parents. Our results indicate that gull mothers induce complex and sex-specific effects on both the early survival of their offspring and on long-term reproductive success through laying order effects among eggs of the same breeding attempt.     

The consequences of parental age for development,body mass and resistance to stress in the red flour beetle

The performance of most animals deteriorates with age. Motivated by the inconsistency in the literature regarding the effect of parental age on offspring traits and performance, we studied how parental age affects offspring development time, body mass, and starvation and cold tolerance in the red flour beetle (Tribolium castaneum). Offspring of old parents pupated later and at a higher body mass, and there was a general positive correlation between body mass and starvation tolerance. Despite their higher body mass, offspring of old parents tolerated starvation less well than those of young parents, emphasizing the impaired performance of the former. However, parental age did not affect offspring thermal tolerance and offspring of old parents were not more sensitive to cold shock than those of young parents. We also examined how ageing affects body mass and cold tolerance in the parental generations. By contrast to the effect of ontogeny on thermal tolerance, which is better known, change in thermal tolerance with age is seldom studied and can take different shapes. Old beetles were more sensitive to cold shock than younger beetles. Similar to cold tolerance, body mass decreased with age. In summary, older beetles reflect a worse physiological condition than younger ones. Ageing leads to impaired cold tolerance, lower body mass, lower number of offspring reaching adulthood, and deteriorated performance of the offspring, expressed as a lower starvation tolerance and a longer development time of the offspring. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 305–314.     

Selection for increased brood size in historical human populations

Human twinning rates are considered to either reflect the direct fitness effects of twinning in variable environments, or to be a maladaptive by-product of selection for other maternal reproductive traits (e.g., polyovulation). We used historical data (1710-1890) of Sami populations from Northern Scandinavia to contrast these alternative hypotheses. We found that women who produced twins started their reproduction younger, ceased it later, had higher lifetime fecundity, raised more offspring to adulthood, and had higher fitness (individual lambda) than mothers of singletons in all populations studied. For example, an average of 1.2 offspring survived to adulthood from a twin delivery, irrespective of its sex ratio, whereas only 0.8 offspring survived to adulthood from a singleton delivery. Only if mothers started reproduction at very late age (> 37 yr), or had a very long reproductive life span (> 20 yr), was it more beneficial to produce only singletons. These findings suggest that twin deliveries among Sami could not be explained as a maladaptive by-product of selection for other maternal reproductive traits. In contrast, our results suggest that twinning was under natural selection, although the strength of selection was likely to have been context dependent.     

Transgenerational plasticity in Silene vulgaris in response to three types of stress

• The environment experienced by plants can influence the phenotype of their offspring. Such transgenerational plasticity can be adaptive when it results in higher fitness of the offspring under conditions correlated with those experienced by the mother plant. However, it has rarely been tested if such anticipatory parental effects may be induced with different environments.
• We grew clonal replicates of Silene vulgaris under control conditions and three types of stress (nutrient deficiency, copper addition and drought), which are known from natural populations of the species. We then subjected offspring from differently treated mother plants to each of the different stress treatments to analyse the influence of maternal and offspring environment on performance and several functional traits.
• Current stress treatments strongly influenced biomass and functional traits of the plants, mostly in line with responses predicted by the theory of functional equilibrium. Plant performance was also influenced by maternal stress treatments, and some effects independent of initial size differences remained until harvest. In particular, stressed mothers produced offspring of higher fitness than control plants. However, there was no evidence for treatment‐specific adaptive transgenerational plasticity, as offspring from a mother plant that had grown in a specific environment did not grow better in that environment than other plants.
• Our results indicate that the maternal environment may affect offspring traits and performance, but also that this transgenerational plasticity is not necessarily adaptive.

     

What are the benefits of parental care? The importance of parental effects on developmental rate

The evolution of parental care is beneficial if it facilitates offspring performance traits that are ultimately tied to offspring fitness. While this may seem self‐evident, the benefits of parental care have received relatively little theoretical exploration. Here, we develop a theoretical model that elucidates how parental care can affect offspring performance and which aspects of offspring performance (e.g., survival, development) are likely to be influenced by care. We begin by summarizing four general types of parental care benefits. Care can be beneficial if parents (1) increase offspring survival during the stage in which parents and offspring are associated, (2) improve offspring quality in a way that leads to increased offspring survival and/or reproduction in the future when parents are no longer associated with offspring, and/or (3) directly increase offspring reproductive success when parents and offspring remain associated into adulthood. We additionally suggest that parental control over offspring developmental rate might represent a substantial, yet underappreciated, benefit of care. We hypothesize that parents adjust the amount of time offspring spend in life‐history stages in response to expected offspring mortality, which in turn might increase overall offspring survival, and ultimately, fitness of parents and offspring. Using a theoretical evolutionary framework, we show that parental control over offspring developmental rate can represent a significant, or even the sole, benefit of care. Considering this benefit influences our general understanding of the evolution of care, as parental control over offspring developmental rate can increase the range of life‐history conditions (e.g., egg and juvenile mortalities) under which care can evolve.     

The effect of maternal and paternal immune challenge on offspring immunity and reproduction in a cricket

Trans‐generational immune priming is the transmission of enhanced immunity to offspring following a parental immune challenge. Although within‐generation increased investment into immunity demonstrates clear costs on reproductive investment in a number of taxa, the potential for immune priming to impact on offspring reproductive investment has not been thoroughly investigated. We explored the reproductive costs of immune priming in a field cricket, Teleogryllus oceanicus. To assess the relative importance of maternal and paternal immune status, mothers and fathers were immune‐challenged with live bacteria or a control solution and assigned to one of four treatments in which one parent, neither or both parents were immune‐challenged. Families of offspring were reared to adulthood under a food‐restricted diet, and approximately 10 offspring in each family were assayed for two measures of immunocompetence. We additionally quantified offspring reproductive investment using sperm viability for males and ovary mass for females. We demonstrate that parental immune challenge has significant consequences for the immunocompetence and, in turn, reproductive investment of their male offspring. A complex interaction between maternal and paternal immune status increased the antibacterial immune response of male offspring. This increased immune response was associated with a reduction in son's sperm viability, implicating a trans‐generational resource trade‐off between investment into immunocompetence and reproduction. Our data also show that these costs are sexually dimorphic, as daughters did not demonstrate a similar increase in immunity, despite showing a reduction in ovary mass.     

Paternal Effects on Offspring Fitness Reflect Father’s Social Environment

In many species, males influence phenotypic traits in their offspring through non-genetic paternal effects. Such effects can represent a form of paternal investment, and males may benefit by adjusting the effects depending on environmental parameters, such as operational sex ratio, so as to maximize offspring fitness. In the neriid fly Telostylinus angusticollis, fathers reared on a nutrient-rich larval diet produce larger offspring, independent of the rearing environment of the offspring. Here we asked whether this paternal effect was influenced by the social environment to which fathers were exposed. We found significant interactions of the effects of paternal larval diet quality and social environment (same-sex vs. mixed-sex groups) on offspring fitness-related traits. Fathers reared on a nutrient-rich diet produced larger male offspring when housed in mixed-sex groups. However, fathers reared on a nutrient-rich diet produced more viable offspring (or more viable sperm) when housed in same-sex groups prior to mating. These results suggest that fitness-enhancing paternal effects can trade off, consistent with parental investment theory on the offspring size-number trade-off, which suggests that these traits represent alternative investment options and parents are selected to optimize the balance based on a range of environmental variables. This is the first study to show that males can facultatively modulate paternal effects based on the social environment.     

Parental age and lifespan influence offspring recruitment: a long-term study in a seabird

Recent studies of wild populations provide compelling evidence that survival and reproduction decrease with age because of senescence, a decline in functional capacities at old ages. However, in the wild, little is known about effects of parental senescence on offspring quality. We used data from a 21-year study to examine the role of parental age on offspring probability of recruitment in a long-lived bird, the blue-footed booby (Sula nebouxii). Offspring probability of recruiting into the breeding population varied over the life of parents and effects age were similar in mothers and fathers. Offspring recruitment was high when parents were roughly 6-12 years old and low before and after then. Effects of parental age on offspring recruitment varied with lifespan (parental age at last reproduction) and previous breeding experience. Offspring recruitment from young and old parents with long reproductive lifespans was greater than that of offspring from parents with short lifespans at young and old ages. For parents with little previous breeding experience recruitment of offspring decreased with their hatch date, but experienced parents were no similarly affected. We found evidence of terminal effects on offspring recruitment in young parents but not in older parents, suggesting that senescence is more likely a gradual process of deterioration than a process of terminal illness. Failure to recruit probably reflects mortality during the first years after independence but also during the fledgling transition to full independence. Our results show effects of parental age and quality on offspring viability in a long-lived wild vertebrate and support the idea that wild populations are composed of individuals of different quality, and that this individual heterogeneity can influence the dynamics of age-structured populations.     

Effects of parental and own early developmental conditions on the phenotype in zebra finches (Taeniopygia guttata)

The performance of an individual can be critically influenced by its experience early in life as well as trans-generationally by the conditions experienced by its parents. However, it remains unclear whether or not the early experience of parents and offspring interact with each other and adapt offspring when the parental and own early environmental conditions match. Here, zebra finches (Taeniopygia guttata) that had experienced either early low or high nutritional conditions raised their offspring under either matched or mismatched nutritional conditions. Parental and offspring early conditions both separately affected the offspring’s adult phenotype, but early conditions experienced by parents and offspring did not interact as predicted. Offspring that grew up under conditions matching those their parents had experienced did not do better than those that grew up in a mismatched environment. Thus, transgenerational effects remain a lifelong burden to the offspring acting in addition to the offspring’s own early life experience. The lack of evidence for adaptive programming to matching environmental conditions may result from non-predictive environments under natural conditions in such opportunistic breeders.     

Maternal effects are long‐lasting and influence female offspring's reproductive strategy in the swordtail fish Xiphophorus multilineatus

The adaptive benefits of maternal investment into individual offspring (inherited environmental effects) will be shaped by selection on mothers as well as their offspring, often across variable environments. We examined how a mother's nutritional environment interacted with her offspring's nutritional and social environment in Xiphophorus multilineatus, a live‐bearing fish. Fry from mothers reared on two different nutritional diets (HQ = high quality and LQ = low quality) were all reared on a LQ diet in addition to being split between two social treatments: exposed to a large adult male during development and not exposed. Mothers raised on a HQ diet produce offspring that were not only initially larger (at 14 days of age), but grew faster, and were larger at sexual maturity. Male offspring from mothers raised on both diets responded to the exposure to courter males by growing faster; however, the response of their sisters varied with mother's diet; females from HQ diet mothers reduced growth if exposed to a courter male, whereas females from LQ diet mothers increased growth. Therefore, we detected variation in maternal investment depending on female size and diet, and the effects of this variation on offspring were long‐lasting and sex specific. Our results support the maternal stress hypothesis, with selection on mothers to reduce investment in low‐quality environments. In addition, the interaction we detected between the mother's nutritional environment and the female offspring's social environment suggests that female offspring adopted different reproductive strategies depending on maternal investment.     

Dispersal distance is influenced by parental and grand-parental density

Non-genetic transmission of information across generations, so-called parental effects, can have significant impacts on offspring morphology, physiology, behaviour and life-history traits. In previous experimental work using the two-spotted spider mite Tetranychus urticae Koch, we demonstrated that dispersal distances increase with local density and levels of genetic relatedness. We here show that manipulation of parental and grand-parental density has a significant effect on offspring dispersal distance, of the same order of magnitude as manipulation of offspring density. We demonstrate that offspring exposed to the same density disperse further if they were born to parents exposed to higher density compared with parents exposed to low density. Offspring dispersal distance also increases when grand-parents were exposed to higher density, except for offspring exposed to low densities, which disperse at shorter distances whatever the grand-parental density. We also show that offspring from mothers exposed to higher densities were overall larger, which suggests that parents in high densities invest more in individual offspring, enabling them to disperse further. We propose that our findings should be included in models investigating the spread rate of invasive species or when predicting the success of conservation measures of species attempting to track changing climates.     

Control of parental investment changes plastically over time with residual reproductive value

Evolutionary conflict between parents and offspring over parental resource investment is a significant selective force on the traits of both parents and offspring. Empirical studies have shown that for some species, the amount of parental investment is controlled by the parents, whereas in other species, it is controlled by the offspring. The main difference between these two strategies is the residual reproductive value of the parents or opportunities for future reproduction. Therefore, this could explain the patterns of control of parental investment at the species level. However, the residual reproductive value of the parents will change during their lifetime; therefore, parental influence on the amount of investment can be expected to change plastically. Here, we investigated control of parental investment when parents were young and had a high residual reproductive value, compared to when they were old and had a low residual reproductive value using a cross‐fostering experiment in the burying beetle Nicrophorus quadripunctatus. We found that parents exert greater control over parental investment when they are young, but parental control is weakened as the parents age. Our results demonstrate that control of parental investment is not fixed, but changes plastically during the parent's lifetime.