The influence of light on paternal plants in Campanula americana (Campanulaceae): pollen characteristics and offspring traits

Offspring trait expression is determined by the combination of parental genes and parental environments. Although maternal environmental effects have been widely characterized, few studies have focused on paternal environmental effects. To determine whether light availability influences pollen and offspring traits in the woodland herb Campanula americana, we reared clones of 12 genotypes in two light levels. In the parental generation we measured pollen number and size. Plants grown under high light produced more pollen grains per flower than those grown under low light. However, the response was genotype specific; some individuals responded little to changes in light availability while others substantially reduced pollen production. As a consequence, paternity ratios may vary between light environments if more pollen is associated with greater siring success. We crossed a subset of these plants to produce the offspring generation. The paternal and maternal light environments influenced offspring seed mass, percentage germination, and days to germination, while only maternal light levels influenced later life traits, such as leaf number and size. Maternal and paternal environmental effects had opposite influences on seed mass, percentage germination and days to germination. Finally, there was no direct relationship between light effects on pollen production and offspring trait expression.     

Maternal effects provide phenotypic adaptation to local environmental conditions

In outcrossing plants, seed dispersal distance is often less than pollen movement. If the scale of environmental heterogeneity within a population is greater than typical seed dispersal distances but less than pollen movement, an individual's environment will be similar to that of its mother but not necessarily its father. Under these conditions, environmental maternal effects may evolve as a source of adaptive plasticity between generations, enhancing offspring fitness in the environment that they are likely to experience. This idea is illustrated using Campanula americana, an herb that grows in understory and light-gap habitats. Estimates of seed dispersal suggest that offspring typically experience the same light environment as their mother. In a field experiment testing the effect of open vs understory maternal light environments, maternal light directly influenced offspring germination rate and season, and indirectly affected germination season by altering maternal flowering time. Results to date indicate that these maternal effects are adaptive; further experimental tests are ongoing. Evaluating maternal environmental effects in an ecological context demonstrates that they may provide phenotypic adaptation to local environmental conditions.     

EFFECTS OF MATERNAL AND PATERNAL ENVIRONMENT AND GENOTYPE ON OFFSPRING PHENOTYPE IN SOLIDAGO ALTISSIMA L.

To predict the possible evolutionary response of a plant species to a new environment, it is necessary to separate genetic from environmental sources of phenotypic variation. In a case study of the invader Solidago altissima, the influences of several kinds of parental effects and of direct inheritance and environment on offspring phenotype were separated. Fifteen genotypes were crossed in three 5 × 5 diallels excluding selfs. Clonal replicates of the parental genotypes were grown in two environments such that each diallel could be made with maternal/paternal plants from sand/sand, sand/soil, soil/sand, and soil/soil. In a first experiment (1989) offspring were raised in the experimental garden and in a second experiment (1990) in the glasshouse. Parent plants growing in sand invested less biomass in inflorescences but produced larger seeds than parent plants growing in soil. In the garden experiment, phenotypic variation among offspring was greatly influenced by environmental heterogeneity. Direct genetic variation (within diallels) was found only for leaf characters and total leaf mass. Germination probability and early seedling mass were significantly affected by phenotypic differences among maternal plants because of genotype ( genetic maternal effects ) and soil environment ( general environmental maternal effects ). Seeds from maternal plants in sand germinated better and produced bigger seedlings than seeds from maternal plants in soil. They also grew taller with time, probably because competition accentuated the initial differences. Height growth and stem mass at harvest (an integrated account of individual growth history) of offspring varied significantly among crosses within parental combinations ( specific environmental maternal effects ). In the glasshouse experiment, the influence of environmental heterogeneity and competition could be kept low. Except for early characters, the influence of direct genetic variation was large but again leaf characters (= basic module morphology) seemed to be under stricter genetic control than did size characters. Genetic maternal effects, general environmental maternal effects, and specific environmental maternal effects dominated in early characters. The maternal effects were exerted both via seed mass and directly on characters of young offspring. Persistent effects of the general paternal environment ( general environmental paternal effects ) were found for leaf length and stem and leaf mass at harvest. They were opposite in direction to the general environmental maternal effects, that is the same genotypes produced “better mothers” in sand but “better fathers” in soil. The general environmental paternal effects must have been due to differences in pollen quality, resulting from pollen selection within the male parent or leading to pre- or postzygotic selection within the female parent. The ranking of crosses according to mean offspring phenotypes was different in the two experiments, suggesting strong interaction of the observed effects with the environment. The correlation structure among characters changed less between experiments than did the pattern of variation of single characters, but under the competitive conditions in the garden plant height seemed to be more directly related to fitness than in the glasshouse. Reduced competition could also explain why maternal effects were less persistent in the glasshouse than in the garden experiment. Evolution via selection of maternal effects would be possible in the study population because these effects are in part due to genetic differences among parents.     

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.     

Links between parental life histories of wild salmon and the telomere lengths of their offspring

The importance of parental contributions to offspring development and subsequent performance is self‐evident at a genomic level; however, parents can also affect offspring fitness by indirect genetic and environmental routes. The life history strategy that an individual adopts will be influenced by both genes and environment; and this may have important consequences for offspring. Recent research has linked telomere dynamics (i.e., telomere length and loss) in early life to future viability and longevity. Moreover, a number of studies have reported a heritable component to telomere length across a range of vertebrates, although the effects of other parental contribution pathways have been far less studied. Using wild Atlantic salmon with different parental life histories in an experimental split‐brood in vitro fertilization mating design and rearing the resulting families under standardized conditions, we show that there can be significant links between parental life history and offspring telomere length (studied at the embryo and fry stage). Maternal life history traits, in particular egg size, were most strongly related to offspring telomere length at the embryonic stage, but then became weaker through development. In contrast, paternal life history traits, such as the father's growth rate in early life, had a greater association in the later stages of offspring development. However, offspring telomere length was not significantly related to either maternal or paternal age at reproduction, nor to paternal sperm telomere length. This study demonstrates both the complexity and the importance of parental factors that can influence telomere length in early life.     

The maternal environment determines the timing of germination in Pinus pinaster

Optimizing the germination timing is crucial for the establishment of new generations. We hypothesized that environmental maternal effects may be relevant in the fine tuning of this trait in a long-lived Mediterranean model tree. We analyzed the influence of maternal genotype, maternal environment and their interaction on the germination success and germination phenology of 8725 Pinus pinaster seeds collected from genotypes clonally replicated in two contrasting environments. Besides maternal genetic effects, the maternal environment significantly affected both the percentage and the timing of germination. Seeds from the more favourable environment germinated 7.5 days earlier and showed higher germination rate (0.93 ± 0.01 vs 0.85 ± 0.03). Seed weight significantly influenced germination time, but seed weight differences between maternal environments were not enough to explain this form of transgenerational plasticity. The effect of the maternal environment varied depending on the genotype, indicating that genetic variation in the sensitivity to the maternal environment in this pine species does exist.     

Maternal warming affects early life stages of an invasive thistle

Maternal environment can influence plant offspring performance. Understanding maternal environmental effects will help to bridge a key gap in the knowledge of plant life cycles, and provide important insights for species’ responses under climate change. Here we show that maternal warming significantly affected the early life stages of an invasive thistle, Carduus nutans. Seeds produced by plants grown in warmed conditions had higher germination percentages and shorter mean germination times than those produced by plants under ambient conditions; this difference was most evident at suboptimal germination temperatures. Subsequent seedling emergence was also faster with maternal warming, with no cost to seedling emergence percentage and seedling growth. Our results suggest that maternal warming may accelerate the life cycle of this species via enhanced early life‐history stages. These maternal effects on offspring performance, together with the positive responses of the maternal generation, may exacerbate invasions of this species under climate change.     

Seed after-ripening and dormancy determine adult life history independently of germination timing

? Seed dormancy can affect life history through its effects on germination time. Here, we investigate its influence on life history beyond the timing of germination. ? We used the response of Arabidopsis thaliana to chilling at the germination and flowering stages to test the following: how seed dormancy affects germination responses to the environment; whether variation in dormancy affects adult phenology independently of germination time; and whether environmental cues experienced by dormant seeds have an effect on adult life history. ? Dormancy conditioned the germination response to low temperatures, such that prolonged periods of chilling induced dormancy in nondormant seeds, but stimulated germination in dormant seeds. The alleviation of dormancy through after-ripening was associated with earlier flowering, independent of germination date. Experimental dormancy manipulations showed that prolonged chilling at the seed stage always induced earlier flowering, regardless of seed dormancy. Surprisingly, this effect of seed chilling on flowering time was observed even when low temperatures did not induce germination. ? In summary, seed dormancy influences flowering time and hence life history independent of its effects on germination timing. We conclude that the seed stage has a pronounced effect on life history, the influence of which goes well beyond the timing of germination.     

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.     

Testing population differentiation in plant species – how important are environmental maternal effects

The maternal environment may contribute to population differentiation in offspring traits if growing conditions of mother plants are different. However, the magnitude of such environmental maternal effects compared with genetic differentiation is often not clear. We tested the importance of environmental maternal effects by comparing population differentiation in parental seed directly collected in the field and in F₁ seed grown under homogeneous conditions. The F₁ seeds were obtained by random crosses within populations. We used five populations in each of four plant species to analyse seed mass and growth chamber germination of both generations at the same time. In two species, we additionally tested offspring performance in the field. We found a significant population differentiation in all species and for nearly all measured traits. Population‐by‐generation interactions indicating environmental maternal effects were significant for germination (three species) and for seed mass (two species) but not for growth and reproduction. The significant interaction was partly due to a reduction of among‐population differentiation from the parental to the F₁ generation that can be explained by a decrease of maternal provisioning effects. However, in some species by trait combinations a change in population ranking and not a decrease of variation was responsible for significant population‐by‐generation interactions indicating environmental maternal effects beyond maternal provisioning. Fitting of seed mass as covariate was not successful in reducing environmental maternal effects on population differentiation in germination. We discuss alternative methods to account for environmental maternal effects in studies on genetic differentiation among populations.     

Do seed mass and family affect germination and juvenile performance in Knautia arvensis? A study using failure-time methods

Germination and seedling establishment are vulnerable stages in the plant life cycle. We investigated how seed mass and family (progeny origin) affect germination and juvenile performance in the grassland herb Knautia arvensis. Seeds were produced by cross-pollination by hand. The fate of 15 individually weighed seeds from each of 15 plants was followed during a 3-month growth chamber experiment. Progeny origin affected germination, both through seed mass and as an independent factor. Two groups of progenies could be distinguished by having rapid or delayed germination. The two groups had similar mean seed masses, but a positive relationship between seed mass and germination rate could be established only among the rapidly germinating progenies. These biologically relevant patterns were revealed because timing of germination was taken into account in the analyses, not only frequencies. Time-to-event data were analysed with failure-time methods, which gave more stable estimates for the relation between germination and seed mass than the commonly applied logistic regression. Progeny origin and seed mass exerted less impact on later characters like juvenile survival, juvenile biomass, and rosette number. These characters were not affected by the timing of germination under the competition-free study conditions. The decrease in the effect of progeny origin from the seed and germination to the juvenile stages suggests that parental effects other than those contributing to the offspring genotype strongly influenced the offspring phenotype at the earliest life stages. Further, the division of progeny germination patterns into two fairly distinct groups indicates that there was a genetic basis for the variation in stratification requirements among parental plants. Field studies are needed to elucidate effects of different timing of germination in the seasonal grasslands that K. arvensis inhabits.     

Effects of germination time on seed morph ratio in a seed-dimorphic species and possible ecological significance

Background and Aims Diaspores of heteromorphic species may germinate at different times due to distinct dormancy-breaking and germination requirements, and this difference can influence life history traits. The primary aim of this study was to determine the effect of germination time of the two seed morphs of Suaeda corniculata subsp. mongolica on life history traits of the offspring.Methods Germinated brown and black seeds were sown on the 20th of each month from April to September in a simulated but near-natural habitat of the species. Phenological and vegetative traits of the maternal plants, and number, size and germination percentage of the offspring were determined.Key Results Germinated seeds sown late in the year produced smaller plants that had a higher proportion of non-dormant brown than dormant black seeds, and these brown seeds were larger than those produced by germinated seeds sown early in the year. The length of the seedling stage for brown seeds was shorter than that for black seeds, and the root/shoot ratio and reproductive allocation of plants from brown seeds were more variable than they were for plants from black seeds. Late-germinating brown seeds produced larger plants than late-germinating black seeds.Conclusions Altering the proportion of the two seed types in response to germination timing can help alleviate the adverse effects of delayed germination. The flexible strategy of a species, such as S. corniculata, that produces different proportions of dimorphic seeds in response to variation in germination timing may favour the maintenance and regeneration of the population in its unpredictable environment.     

Maternal and paternal contributions to the fitness of hybrids between red and white mulberry (Morus, Moraceae)

The fitness of hybrids depends on the genetic disparity between parental taxa and the magnitude of their nuclear and non-nuclear contributions. To estimate the role of non-nuclear effects, we crossed red (R), white (W) and hybrid (H) mulberry in all combinations and compared the magnitude of maternal and paternal effects on offspring fitness (seed set, germination, survival and aboveground biomass) in a greenhouse environment. Variation in offspring fitness was determined largely by the identity of the maternal parent; specifically, progeny with white mothers had the highest cumulative fitness. As fathers, red, white, and hybrid mulberry had no effect on fitness, and maternal × paternal interactions were significant only for survival. Individual cross-types differed significantly for all fitness components except seed set. Offspring from hybrid crosses (W × R, H × R, H × W) often differed from at least one of the within-parent crosses (W × W, R × R) as well as from other hybrid crosses, although their fitness values never exceeded the most fit parent. Reciprocal crosses differed in only two of 15 possible parental combinations: W × H (cumulative fitness) and W × R (aboveground biomass). Overall, the strong asymmetry in magnitude of maternal and paternal effects suggests that fitness of hybrid mulberry is governed largely by non-nuclear, parental effects.     

Parental effects in Lychnis flos-cuculi. I: Seed size,germination and seedling performance in a controlled environment

Selection responses in natural plant populations depend on how the phenotypic variation of traits is composed. The contributions of nuclear genetic, maternal, paternal, environmental and inbreeding effects to variation in time to germination, germination percentage, and seed- and seedling size were studied in a population of Lychnis flos-cuculi. It was found that: (1) Maternal effects predominated in the determination of progeny seed size and germination characteristics; (2) Maternal environment during seed development was less important than maternal genotype; (3) Small but significant variation within maternal families could be observed among individuals sired by different fathers; (4) Additive genetic variance was significant for seedling size 4 weeks after germination. In conclusion, selection shortly after emergence will mainly favour particular maternal genotypes, while selection later in the life cycle may act upon zygotic genotypes. Inbreeding depression was significant, especially for vegetative growth. Consistent differences were found among maternal genotypes in the degree of variation in the time to germination, suggesting that selection could operate to favour polymorphic or uniform germination behaviour.     

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.     

PLEIOTROPY IN THE WILD: THE DORMANCY GENE DOG1 EXERTS CASCADING CONTROL ON LIFE CYCLES

In the wild, organismal life cycles occur within seasonal cycles, so shifts in the timing of developmental transitions can alter the seasonal environment experienced subsequently. Effects of genes that control the timing of prior developmental events can therefore be magnified in the wild because they determine seasonal conditions experienced by subsequent life stages, which can influence subsequent phenotypic expression. We examined such environmentally induced pleiotropy of developmental‐timing genes in a field experiment with Arabidopsis thaliana. When studied in the field under natural seasonal variation, an A. thaliana seed‐dormancy gene, Delay Of Germination 1 (DOG1), was found to influence not only germination, but also flowering time, overall life history, and fitness. Flowering time of the previous generation, in turn, imposed maternal effects that altered germination, the effects of DOG1 alleles, and the direction of natural selection on these alleles. Thus under natural conditions, germination genes act as flowering genes and potentially vice versa. These results illustrate how seasonal environmental variation can alter pleiotropic effects of developmental‐timing genes, such that effects of genes that regulate prior life stages ramify to influence subsequent life stages. In this case, one gene acting at the seed stage impacted the entire life cycle.     

Effects of increased nitrogen deposition and precipitation on seed and seedling production of Potentilla tanacetifolia in a temperate steppe ecosystem

Background

The responses of plant seeds and seedlings to changing atmospheric nitrogen (N) deposition and precipitation regimes determine plant population dynamics and community composition under global change.

Methodology/Principal Findings

In a temperate steppe in northern China, seeds of P. tanacetifolia were collected from a field-based experiment with N addition and increased precipitation to measure changes in their traits (production, mass, germination). Seedlings germinated from those seeds were grown in a greenhouse to examine the effects of improved N and water availability in maternal and offspring environments on seedling growth. Maternal N-addition stimulated seed production, but it suppressed seed mass, germination rate and seedling biomass of P. tanacetifolia. Maternal N-addition also enhanced responses of seedlings to N and water addition in the offspring environment. Maternal increased-precipitation stimulated seed production, but it had no effect on seed mass and germination rate. Maternal increased-precipitation enhanced seedling growth when grown under similar conditions, whereas seedling responses to offspring N- and water-addition were suppressed by maternal increased-precipitation. Both offspring N-addition and increased-precipitation stimulated growth of seedlings germinated from seeds collected from the maternal control environment without either N or water addition. Our observations indicate that both maternal and offspring environments can influence seedling growth of P. tanacetifolia with consequent impacts on the future population dynamics of this species in the study area.

Conclusion/Significance

The findings highlight the importance of the maternal effects on seed and seedling production as well as responses of offspring to changing environmental drivers in mechanistic understanding and projecting of plant population dynamics under global change.     

Early life of fathers affects offspring fitness in a wild rodent

Intergenerational fitness effects on offspring due to the early life of the parent are well studied from the standpoint of the maternal environment, but intergenerational effects owing to the paternal early life environment are often overlooked. Nonetheless, recent laboratory studies in mammals and ecologically relevant studies in invertebrates predict that paternal effects can have a major impact on the offspring's phenotype. These nongenetic, environment‐dependent paternal effects provide a mechanism for fathers to transmit environmental information to their offspring and could allow rapid adaptation. We used the bank vole Myodes glareolus, a wild rodent species with no paternal care, to test the hypothesis that a high population density environment in the early life of fathers can affect traits associated with offspring fitness. We show that the protein content in the diet and/or social environment experienced during the father's early life (prenatal and weaning) influence the phenotype and survival of his offspring and may indicate adaptation to density‐dependent costs. Furthermore, we show that experiencing multiple environmental factors during the paternal early life can lead to a different outcome on the offspring phenotype than stimulated by experience of a single environmental factor, highlighting the need to study developmental experiences in tandem rather than independent of each other.     

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.