Parental conflict does not necessarily lead to the evolution of imprinting

For some genes, the epigenetic state (whether they are expressed) depends on whether the gene is inherited through the mother or the father. Such imprinting, or parent-specific gene expression (PSGE), occurs in mammals, including humans, and higher plants. The theory that PSGE solves genetic conflict between mother and father is widely accepted. We argue, however, that the conditions for PSGE to evolve are restricted. With respect to seed size, PSGE can only evolve when the developing offspring has a strong effect on its own resource acquisition. When seed size is close to the optimum for the maternal parent, there is no internal conflict in the offspring because maternally and paternally derived genes both favour increased seed size. Although the literature generally suggests that the maternal parent controls seed size, a number of observations suggest an additional role for the paternal parent. Here, we critically evaluate these studies and suggest a rigorous methodology for establishing paternal effects on seed size, which can be applied to the model species Arabidopsis thaliana.     

Maternal control of nutrient allocation in plant seeds by genomic imprinting

Imprinted genes are commonly expressed in mammalian placentas and in plant seed endosperms, where they exhibit preferential uniparental allelic expression. In mammals, imprinted genes directly regulate placental function and nutrient distribution from mother to fetus; however, none of the >60 imprinted genes thus far reported in plants have been demonstrated to play an equivalent role in regulating the flow of resources to the embryo. Here we show that imprinted Maternally expressed gene1 (Meg1) in maize is both necessary and sufficient for the establishment and differentiation of the endosperm nutrient transfer cells located at the mother:seed interface. Consistent with these findings, Meg1 also regulates maternal nutrient uptake, sucrose partitioning, and seed biomass yield. In addition, we generated an imprinted and nonimprinted synthetic Meg1 ((syn)Meg1) dosage series whereby increased dosage and absence of imprinting both resulted in an unequal investment of maternal resources into the endosperm. These findings highlight dosage regulation by genomic imprinting as being critical for maintaining a balanced distribution of maternal nutrients to filial tissues in plants, as in mammals. However, unlike in mammals, Meg1 is a maternally expressed imprinted gene that surprisingly acts to promote rather than restrict nutrient allocation to the offspring.     

Genetic evidence for a Janzen-Connell recruitment pattern in reproductive offspring of Pinus halepensis trees

Effective seed dispersal, combining both dispersal and postdispersal (establishment) processes, determines population dynamics and colonization ability in plants. According to the Janzen-Connell (JC) model, high mortality near the mother plant shifts the offspring establishment distribution farther away from the mother plant relative to the seed dispersal distribution. Yet, extending this prediction to the distribution of mature (reproductive) offspring remains a challenge for long-living plants. To address this challenge, we selected an isolated natural Aleppo pine (Pinus halepensis) population in Mt. Pithulim (Israel), which expanded from five ancestor trees in the beginning of the 20th century into ～2000 trees today. Using nine microsatellite markers, we assigned parents to trees established during the early stages of population expansion. To elucidate the effect of the distance from the mother plant on postdispersal survival, we compared the effective seed dispersal kernel, based on the distribution of mother-offspring distances, with the seed dispersal kernel, based on simulations of a mechanistic wind dispersal model. We found that the mode of the effective dispersal kernel is shifted farther away than the mode of the seed dispersal kernel, reflecting increased survival with increasing distance from the mother plant. The parentage analysis demonstrated a highly skewed reproductive success and a strong directionality in effective dispersal corresponding to the wind regime. We thus provide compelling evidence that JC effects act also on offspring that become reproductive and persist as adults for many decades, a key requirement in assessing the role of postdispersal processes in shaping population and community dynamics.     

Paternal effects on seed mass in Arabidopsis thaliana

Who is in control of seed size, and do some fathers sire bigger seeds than others? We used isogenic male-sterile genotypes of the Arabidopsis thaliana accessions Col and Ler. By fertilising flowers side-by-side with either pollen from the same accession ('self-pollination') or pollen from another accession (outcrossing), we compared, on the same mother plant, seed set of flowers that were very similar in resource status. Some paternal genotypes had a significant effect on seed mass, with the most extreme father siring seeds 15.3% heavier than seeds resulting from 'self-pollination'. There was no correlation between seed mass of paternal parents and the seeds they sired. We discuss the evolution of seed size as a tug-of-war between parent and offspring.     

Maternal environmental effects on the phenotypic responses of the twining vine Ipomoea purpurea to support availability

The presence of physical support elicits a number of morphological changes in the shoot of the common morning glory Ipomoea purpurea , including a shortening of internodes and petioles and a thickening of the main stem. Working with experimentally supported and non-supported plants of I . purpurea , I tested the existence of maternal environmental effects of physical support in this twining vine. I evaluated whether the offspring of supported plants differed from the offspring of non-supported plants in a number of morphological and reproductive characters. Stem diameter was the only shoot trait that showed a significant effect of the maternal environment (support). The stems of the progeny of supported mother plants were thicker than the stems of the progeny of non-supported mother plants. This was true for both supported and non-supported progeny. Stem diameter, however, was not significantly related to plant fitness (seed number) in supported or non-supported progeny plants. The maternal environment did not affect the magnitude of the phenotypic responses to support of shoot traits in the progeny plants. There were no maternal environmental effects of physical support on the proportion of flowering plants at week 10 in both non-supported and supported progeny. Likewise, the presence of physical support in the maternal environment did not affect reproductive traits (seed number, seed size, percentage of reproductive biomass) in supported and non-supported progeny plants. Finally, the relationship between seed size and seed number was affected by the maternal support environment. The progeny of supported mother plants showed a significantly negative association (trade-off) between seed size and number, whereas such a trade-off was not observed in the progeny of non-supported plants. This was true for both supported and non-supported progeny.     

Facultative apomixis and hybridization in arctic Potentilla section Niveae (Rosaceae) from Svalbard

The degree of sexual seed set and the ability to cross were investigated in three taxa of Potentilla section Niveae ( P. chamissonis , P. insularis and P. nivea ) from the Svalbard Archipelago. Emasculated and bagged flowers had little or no seed set, while 71% of the emasculated, bagged and pollinated flowers had some. The taxa are interpreted as pseudogamous apomicts. Parental plants and offspring were subjected to isozyme analysis. Most of the offspring were clones of the mother plant, but 1.7% had bands from the pollen donor. The sexual offspring were all produced by mother plants of P. insularis , which is interpreted as a facultative apomict. Surprisingly, crosses between different taxa gave higher seed to ovule ratios and numbers of sexually produced offspring than crosses within taxa. Some of the sexually produced hybrid offspring had the same kind of hairs on the petioles as their mother taxon, showing that hybrids may not be intermediate in hair characters, which are considered important in the delimitation of these taxa. The results of the present study indicate very close relationships among the investigated plants.  © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society , 2003, 142 , 373−381.     

Why do large mothers produce large offspring? Theory and a test

To explain the general tendency of large mothers to produce large offspring, we developed two models in which either the rate at which each single offspring extracts resources from the mother or the rate at which the mother supplies resources to all the offspring is limited (terminal- or upper-stream-limitation on resource transport, respectively). We also reanalyzed the data of Erythronium japonicum to test the models. The terminal-stream-limitation model predicted that the optimal offspring size that maximizes the fitness of the mother increases with an increase in the maximum rate of resource extraction by each single offspring. Thus, large mothers produce large offspring if the maximum resource extraction rate is high in those mothers. The upper-stream-limitation model predicted that the optimal offspring size decreases with an increase in the maximum rate of resource supply by the mother to all the offspring. In E. japonicum, the maximum growth rate of a seed was independent of the number of seeds of a plant, suggesting that the resource extraction rate is limited at the individual seed level. The maximum growth rate was high in large plants and had a strong positive effect on final seed mass. Thus, the results were consistent with the terminal-stream-limitation model.     

Seed traits,seed‐reserve utilization and offspring performance across pre‐industrial to future CO2 concentrations in a Mediterranean community

Atmospheric CO₂ enrichment can affect plants directly via impacts on their performance, and indirectly, by environment‐specific traits passed down from the mother plant to the offspring. Such maternal effects can significantly alter plant species composition, especially in annual ecosystems where the entire community is recruited from seeds each year. This study assessed impacts of future, high CO₂ (440 and 600 ppm) and pre‐industrial, low CO₂ (280 ppm) on seed traits and offspring performance in three plant functional groups (grasses, legumes, forbs) comprising 17 annual species of a semi‐arid Mediterranean community. In grasses, seed size and seed‐reserve utilization as expressed by root elongation tended to be higher at high than at low maternal CO₂, but total seed protein concentration and protein pool decreased with increasing maternal CO₂. The response of seed size to high CO₂ increased with increasing leaf‐mass fraction in grasses, and decreased with decreasing concentration of leaf non‐structural carbohydrates in legumes. Offspring development was studied at ambient CO₂, and showed reduced emergence success of high‐CO₂ progeny compared with low‐CO₂ progeny in forbs. Total biomass was lower in high‐CO₂ than in low‐CO₂ offspring across all functional groups. The biomass response to high maternal CO₂ in legume offspring correlated inversely with seed size, resulting in up to 25% lower biomass in large‐seeded species. Under the scenario of maternal effects combined with projected changes in biomass and seed production under direct exposure to high CO₂, legumes might gain and forbs and grasses might lose from future CO₂ enrichment. Most changes in seed traits and offspring performance were greater between pre‐industrial and near‐future CO₂ than between near‐ and remote‐future CO₂ concentrations. Hence, maternal effects of increasing CO₂ may contribute to current changes in plant productivity and species composition, and they need to be considered when predicting impacts of global change on plant communities.     

Parent-of-origin effects on seed development in Arabidopsis thaliana require DNA methylation

Some genes in mammals and flowering plants are subject to parental imprinting, a process by which differential epigenetic marks are imposed on male and female gametes so that one set of alleles is silenced on chromosomes contributed by the mother while another is silenced on paternal chromosomes. Therefore, each genome contributes a different set of active alleles to the offspring, which develop abnormally if the parental genome balance is disturbed. In Arabidopsis, seeds inheriting extra maternal genomes show distinctive phenotypes such as low weight and inhibition of mitosis in the endosperm, while extra paternal genomes result in reciprocal phenotypes such as high weight and endosperm overproliferation. DNA methylation is known to be an essential component of the parental imprinting mechanism in mammals, but there is less evidence for this in plants. For the present study, seed development was examined in crosses using a transgenic Arabidopsis line with reduced DNA methylation. Crosses between hypomethylated and wild-type diploid plants produced similar seed phenotypes to crosses between plants with normal methylation but different ploidies. This is consistent with a model in which hypomethylation of one parental genome prevents silencing of alleles that would normally be active only when inherited from the other parent - thus phenocopying the effects of extra genomes. These results suggest an important role for methylation in parent-of-origin effects, and by inference parental imprinting, in plants. The phenotype of biparentally hypomethylated seeds is less extreme than the reciprocal phenotypes of uniparentally hypomethylated seeds. The observation that development is less severely affected if gametes of both sexes (rather than just one) are 'neutralized' with respect to parent-of-origin effects supports the hypothesis that parental imprinting is not necessary to regulate development.     

A simple method for detection of imprinting effects based on case-parents trios

Using data from families in which marker genotypes are known for the father, the mother and the affected offspring, a simple statistic for testing for imprinting effects is developed. The statistic considers whether the expected number of families in which the father carries more copies of a particular marker allele than the mother is equal to the expected number of families in which the mother carries more copies of the allele than the father. The proposed parent-of-origin effects test statistic (POET) is shown to be normally distributed and can be employed to test for imprinting in situations where the marker locus need not be a disease susceptibility locus and where the female and male recombination fractions are sex-specific. A simulation study is conducted to characterize the power of the POET and other properties, and its results show that it is appropriate to employ the POET.     

Assessment of spatial discordance of primary and effective seed dispersal of European beech (Fagus sylvatica L.) by ecological and genetic methods

Spatial discordance between primary and effective dispersal in plant populations indicates that postdispersal processes erase the seed rain signal in recruitment patterns. Five different models were used to test the spatial concordance of the primary and effective dispersal patterns in a European beech (Fagus sylvatica) population from central Spain. An ecological method was based on classical inverse modelling (SSS), using the number of seed/seedlings as input data. Genetic models were based on direct kernel fitting of mother‐to‐offspring distances estimated by a parentage analysis or were spatially explicit models based on the genotype frequencies of offspring (competing sources model and Moran‐Clark's Model). A fully integrated mixed model was based on inverse modelling, but used the number of genotypes as input data (gene shadow model). The potential sources of error and limitations of each seed dispersal estimation method are discussed. The mean dispersal distances for seeds and saplings estimated with these five methods were higher than those obtained by previous estimations for European beech forests. All the methods show strong discordance between primary and effective dispersal kernel parameters, and for dispersal directionality. While seed rain was released mostly under the canopy, saplings were established far from mother trees. This discordant pattern may be the result of the action of secondary dispersal by animals or density‐dependent effects; that is, the Janzen‐Connell effect.     

Parental effects modulate seed longevity: exploring parental and offspring phenotypes to elucidate pre-zygotic environmental influences

? Seed longevity, which is essential for germplasm conservation and survival of many land plant species, can vary considerably within species and cultivars. Here, we explore the relationship between parental and offspring phenotypes to elucidate how pre-zygotic environment affects seed longevity. ? Plants of the wild species Plantago cunninghamii were exposed to wet or dry soil within a warm or cool glasshouse until flowering and then moved to a common environment. Seeds subsequently produced were collected at maturity, and longevity was assessed by controlled ageing at 45°C, 60% relative humidity. Multivariate analysis was used to examine relationships between the parental and offspring phenotypes. ? The pre-zygotic environment resulted in a highly plastic parental response which was passed on to offspring seeds and changed their longevity (p(50)) by more than a factor of 2. Seed longevity is a function of the seed population's distribution of deaths in time (σ) and quality (K(i)); σ was associated with plant size, and K(i) with reproductive plant traits. ? The pre-zygotic growth environment modulated seed longevity via a parental effect. Reproductive performance and seed quality (K(i)) were highly correlated with each other and unrelated to the maternal plant phenotype. Hence seed quality may be associated with the paternal plant response to the environment.     

Bigger is not always better: conflicting selective pressures on seed size in Quercus ilex

Most theoretical treatments of the evolutionary ecology of offspring size assume a simple and direct effect of investment per offspring on offspring fitness. In this paper I experimentally determine the relationship between seed mass and several main fitness components of the oak Quercus ilex, to estimate phenotypic selection acting on seed mass during the early life cycle and to discover any potential selective conflicts occurring between different stages from dispersal to establishment. I found a positive effect of acorn size on most fitness components related to seedling establishment. Large size increased germination rate and seedling survival, accelerated germination timing, and enhanced seedling growth. Nevertheless, there was also a direct negative effect of acorn size on survival to predation, because large acorns were highly preferred by the main postdispersal seed predators at the study site, wild boars and wood mice. Because of the low probability of escape from predation, the fitness of large acorns estimated on this component was significantly lower than the fitness of smaller acorns. Therefore, seed size affected fitness in two different ways, yielding opposing and conflicting selective forces. These findings suggest that the general assumption that offspring fitness is a fixed positive function of seed size needs to be reconsidered for some systems. The existence of conflicting selection might explain the occurrence of an optimal seed size in some plant species without invoking a seed number-size trade-off.     

Seed size and plant strategy across the whole life cycle

We compiled information from the international literature to quantify the relationships between seed mass and survival through each of the hazards plants face between seed production and maturity. We found that small-seeded species were more abundant in the seed rain than large-seeded species. However, this numerical advantage was lost by seedling emergence. The disadvantage of small-seeded species probably results from size-selective post-dispersal seed predation, or the longer time small-seeded species spend in the soil before germination. Seedlings from large-seeded species have higher survival through a given amount of time as seedlings. However, this advantage seems to be countered by the greater time taken for large-seeded species to reach reproductive maturity: our data suggested no relationship, or perhaps a weak negative relationship, between seed size and survival from seedling emergence through to adulthood. A previous compilation showed that the inverse relationship between seed mass and the number of seeds produced per unit canopy area per year is countered by positive relationships between seed mass, plant size and plant longevity. Taken together, these data show that our old understanding of a species' seed mass as the result of a trade–off between producing a few large offspring, each with high survival probability, versus producing many small offspring each with a lower chance of successfully establishing was incomplete. It seems more likely that seed size evolves as part of a spectrum of life history traits, including plant size, plant longevity, juvenile survival rate and time to reproduction.     

Nature of size–number trade–off: test of the terminal-stream-limitation model for seed production of Cardiocrium cordatum

We tested the prediction of the terminal-stream-limitation model using Cardiocrium cordatum . This model predicts that the total offspring mass increases with offspring number, whereas it decreases with offspring size, because the loss of resources via maintenance respiration decreases with offspring number but increases with offspring size. We traced the growth curve of seeds and harvested seeds when they matured. The maximum gross growth rate of a seed had a strong positive effect on final seed dry mass, whereas the respiration cost had a strong negative effect on such mass. The total seed mass produced by a plant decreased with (or was independent of) an increase in the mean seed dry mass of the plant, whereas it increased with an increase in the number of seeds produced by the plant. An increase in seed number resulted in a decrease in the loss of resources due to respiration during seed growth, whereas an increase in the mean seed dry mass did not result in a decrease in the loss of resources due to respiration. Thus, we concluded that these results are consistent overall with the prediction of the model and that an increase in seed number rather than an increase in individual seed size is advantageous in terms of resource use efficiency.     

The relationship between individual seed quality and maternal plant body size in crowded herbaceous vegetation

Aims In most natural plant populations, there is a strong right-skewed distribution of body sizes for reproductive plants—i.e. the vast majority are relatively small, suppressed weaklings that manage not just to survive effects of crowding/competition and other hazards but also to produce offspring. Recent research has shown that because of their relatively large numbers, these relatively small resident plants collectively contribute most of the seed offspring production available for the population in the next generation. However, the success of these offspring will depend in part on their quality, e.g. reflected by seed size and resource content. Accordingly, in the present study, we used material from natural populations of herbaceous species to test the null hypothesis that there is no significant relationship between body size variation in resident plants—resulting from between-site variation in the intensity of crowding/competition—and variation in the mass or N content of their individual seeds.Methods Using populations of 56 herbaceous species common in eastern Ontario, total above-ground dry plant mass, mean mass per seed and mean nitrogen (N) content per seed were recorded for a sample of the largest resident plants and also for the smallest reproductive plants growing in local neighbourhoods with the most severe crowding/competition from near neighbours.Important findings Mass per seed was numerically smaller from the smallest resident plants for most study species, but with few exceptions, this was not significantly different (P> 0.05) from mass per seed from the largest resident plants. The results therefore showed no general effect of maternal plant body size on individual seed mass, or N content. This suggests that the reproductive output of the smaller half of the resident plant size distribution within these populations is likely to contribute not just most of the seed production available for the next generation but also seed offspring that are just as likely—on a per individual basis—to achieve seedling/juvenile recruitment success as the seed offspring produced by the largest resident plants. This conflicts with the traditional 'size-advantage' hypothesis for predicting plant fitness under severe competition, and instead supports the recent 'reproductive-economy-advantage' hypothesis, where competitive fitness is promoted by capacity to produce offspring that—despite severe body size suppression imposed by neighbour effects—in turn have capacity to produce grand-offspring.     

Costly Solicitation, Timing of Offspring Conflict, and Resource Allocation in Plants

The theory of parent–offspring conflict is extended toplants that produce many offspring in one reproductive event.The energetic cost of begging signals and the timing of offspringconflict are explicitly taken into account. We find that ifthe indirect costs of increased provisioning of selfish offspringare borne by their brood mates, then offspring are selectedto solicit in so costly a way that a substantial part of parentalinvestment in a brood goes to solicitation rather than offspring'sgrowth and survival. Consequently, offspring conflict oftenresults in smaller seed size than the parental optimum in theabsence of conflict, although each offspring still consumesmore resources than the amount its mother is willing to give.While the optimal sex allocation can be shown to be independentof solicitation and sibling conflict, the overall reproductiveeffort is always lowered by parent–offspring conflict.The timing of offspring conflict during the period of parentalinvestment is demonstrated to be an important factor that influencesthe outcome of parent–offspring conflict. The more resourcesare allocated to individual offspring before the occurrenceof offspring solicitation, the less offspring should solicit,and hence the closer the offspring size to the parental optimum.Copyright 2000 Annals of Botany Company Evolutionarily stable strategy, parent–offspring conflict, parental investment, reproductive resource allocation, seed size, solicitation, timing of offspring conflict     

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.     

Genomic Imprinting of Grb10?: Coadaptation or Conflict?

Mammalian development involves significant interactions between offspring and mother. But is this interaction a carefully coordinated effort by two individuals with a common goal—offspring survival? Or is it an evolutionary battleground (a central idea in our understanding of reproduction). The conflict between parents and offspring extends to an offspring''s genes, where paternally inherited genes favor demanding more from the mother, while maternally inherited genes favor restraint. This “intragenomic conflict” (among genes within a genome) is the dominant evolutionary explanation for “genomic imprinting.” But a new study in PLOS Biology provides support for a different perspective: that imprinting might facilitate coordination between mother and offspring. According to this “coadaptation theory,” paternally inherited genes might be inactivated because maternally inherited genes are adapted to function harmoniously with the mother. As discussed in this article, the growth effects associated with the imprinted gene Grb10 are consistent with this idea, but it remains to be seen just how general the pattern is.     

Influence of mom and dad: quantitative genetic models for maternal effects and genomic imprinting

The expression of an imprinted gene is dependent on the sex of the parent it was inherited from, and as a result reciprocal heterozygotes may display different phenotypes. In contrast, maternal genetic terms arise when the phenotype of an offspring is influenced by the phenotype of its mother beyond the direct inheritance of alleles. Both maternal effects and imprinting may contribute to resemblance between offspring of the same mother. We demonstrate that two standard quantitative genetic models for deriving breeding values, population variances and covariances between relatives, are not equivalent when maternal genetic effects and imprinting are acting. Maternal and imprinting effects introduce both sex-dependent and generation-dependent effects that result in differences in the way additive and dominance effects are defined for the two approaches. We use a simple example to demonstrate that both imprinting and maternal genetic effects add extra terms to covariances between relatives and that model misspecification may over- or underestimate true covariances or lead to extremely variable parameter estimation. Thus, an understanding of various forms of parental effects is essential in correctly estimating quantitative genetic variance components.