Differential costs of reproduction in females and hermaphrodites in a gynodioecious plant

Background and Aims

Plants exhibit a variety of reproductive systems where unisexual (females or males) morphs coexist with hermaphrodites. The maintenance of dimorphic and polymorphic reproductive systems may be problematic. For example, to coexist with hermaphrodites the females of gynodioecious species have to compensate for the lack of male function. In our study species, Geranium sylvaticum, a perennial gynodioecious herb, the relative seed fitness advantage of females varies significantly between years within populations as well as among populations. Differences in reproductive investment between females and hermaphrodites may lead to differences in future survival, growth and reproductive success, i.e. to differential costs of reproduction. Since females of this species produce more seeds, higher costs of reproduction in females than in hermaphrodites were expected. Due to the higher costs of reproduction, the yearly variation in reproductive output of females might be more pronounced than that of hermaphrodites.

Methods

Using supplemental hand-pollination of females and hermaphrodites of G. sylvaticum we examined if increased reproductive output leads to differential costs of reproduction in terms of survival, probability of flowering, and seed production in the following year.

Key Results

Experimentally increased reproductive output had differential effects on the reproduction of females and hermaphrodites. In hermaphrodites, the probability of flowering decreased significantly in the following year, whereas in females the costs were expressed in terms of decreased future seed production.

Conclusions

When combining the probability of flowering and seed production per plant to estimate the multiplicative change in fitness, female plants showed a 56 % and hermaphrodites showed a 39 % decrease in fitness due to experimentally increased reproduction. Therefore, in total, female plants seem to be more sensitive to the cost of reproduction in terms of seed fitness than hermaphrodites.     

Early life expenditure in sexual competition is associated with increased reproductive senescence in male red deer

The evolutionary theories of senescence predict that investment in reproduction in early life should come at the cost of reduced somatic maintenance, and thus earlier or more rapid senescence. There is now growing support for such trade-offs in wild vertebrates, but these exclusively come from females. Here, we test this prediction in male red deer (Cervus elaphus) using detailed longitudinal data collected over a 40-year field study. We show that males which had larger harems and thereby allocated more resources to reproduction during early adulthood experienced higher rates of senescence in both harem size and rut duration. Males that carried antlers with more points during early life did not show more pronounced declines in reproductive traits in later life. Overall, we demonstrate that sexual competition shapes male reproductive senescence in wild red deer populations and provide rare empirical support for the disposable soma theory of ageing in males of polygynous vertebrate species.     

Compensation of seed production after severe injury in the short-lived herb Barbarea vulgaris

A pot experiment with the common ruderal herb Barbarea vulgaris (Brassicaceae) was set up to elucidate to what extent short-lived species sprouting from roots regenerate and compensate for seed production after damage. We tested if sprouting from roots ensures survival after severe aboveground biomass damage, but the number of seeds produced declines with increasing severity of injury, decreasing nutrient availability and progress in the life cycle at the time of injury.Plants of B. vulgaris were cultivated in a 3-year garden experiment at two nutrient levels (high vs. low). During the experiment, two levels of injury severity were applied: high (removal of all aboveground biomass) and low (removal of aboveground biomass leaving basal axillary buds intact). Damage was applied at four life-cycle phases: young rosette, overwintered rosette, flowering plant and fruiting plant. All injured plants survived and resprouted irrespective of life-cycle phase, severity of injury and nutrient availability. Injury significantly affected seed production and also the plants’ life cycle. Plants injured in the second year of their life (overwintered rosette, flowering plant and fruiting plant) postponed reproduction to the third season (in the case of high injury severity) or their seed production was lower than in intact plants (in the case of low injury severity). In plants injured in the first life year, seed production and life cycle were not influenced. Nutrient level only marginally affected resprouting after injury and seed production.The experiment showed that the ability to sprout from roots enables plants to survive a 100% loss of aboveground biomass, and to keep some seed production or even compensate it. The short-lived ruderal species B. vulgaris successfully copes with severe disturbance by resprouting and does not rely only on its seed bank.     

The Effects of Root-knot Nematode Infection and Mi-mediated Nematode Resistance in Tomato on Plant Fitness

The Mi-1.2 resistance gene in tomato (Solanum lycopersicum) confers resistance against several species of root-knot nematodes (Meloidogyne spp.). This study examined the impact of M. javanica on the reproductive fitness of near-isogenic tomato cultivars with and without Mi-1.2 under field and greenhouse conditions. Surprisingly, neither nematode inoculation or host plant resistance impacted the yield of mature fruits in field microplots (inoculum=8,000 eggs/plant), or fruit or seed production in a follow-up greenhouse bioassay conducted with a higher inoculum level (20,000 eggs/plant). However, under heavy nematode pressure (200,000 eggs/plant), greenhouse-grown plants carrying Mi-1.2 had more than ten-fold greater fruit production than susceptible plants and nearly forty-fold greater estimated lifetime seed production, confirming prior reports of the benefits of Mi-1.2. In all cases Mi-mediated resistance significantly reduced nematode reproduction. These results indicated that tomato can utilize tolerance mechanisms to compensate for moderate levels of nematode infection, but that the Mi-1.2 resistance gene confers a dramatic fitness benefit under heavy nematode pressure. No significant cost of resistance was detected in the absence of nematode infection.     

Evidence of a component Allee effect driven by predispersal seed predation in a plant (Pedicularis rex,Orobanchaceae)

A small or sparse population may suffer a reduction in fitness owing to Allee effects. Here, we explored effects of plant density on pollination, reproduction and predation in the alpine herb Pedicularis rex over two years. We did not detect a significant difference in the pollination rate or fecundity (fruit set and the initial seed set) before predation between sparse and dense patches in either year, indicating no pollination-driven Allee effect. However, dense patches experienced significantly fewer attacks by predispersal seed predators in both years, resulting in a significantly decreased realized fecundity (final seed set), suggesting a component Allee effect driven by predispersal seed predation. Predation-driven Allee effects have been predicted by many models and demonstrated for a range of animals, but there is scant evidence for such effects in plants. Our study provides strong evidence of a component Allee effect driven by predation in a plant species.     

Kinship between parents reduces offspring fitness in a natural population of Rhododendron brachycarpum

Background and Aims

A reduction in offspring fitness resulting from mating between neighbours is interpreted as biparental inbreeding depression. However, little is known about the relationship between the parents'' genetic relatedness and biparental inbreeding depression in their progeny in natural populations. This study assesses the effect of kinship between parents on the fitness of their progeny and the extent of spatial genetic structure in a natural population of Rhododendron brachycarpum.

Methods

Kinship coefficients between 11 858 pairs of plants among a natural population of 154 R. brachycarpum plants were estimated a priori using six microsatellite markers. Plants were genotyped, and pairs were selected from among 60 plants to vary the kinship from full-sib to unrelated. After a hand-pollination experiment among the 60 plants, offspring fitness was measured at the stages of seed maturation (i.e. ripening) under natural conditions, and seed germination and seedling survival under greenhouse conditions. In addition, spatial autocorrelation was used to assess the population''s genetic structure.

Key Results

Offspring fitness decreased significantly with increasing kinship between parents. However, the magnitude and timing of this effect differed among the life-cycle stages. Measures of inbreeding depression were 0·891 at seed maturation, 0·122 (but not significant) at seed germination and 0·506 at seedling survival. The local population spatial structure was significant, and the physical distance between parents mediated the level of inbreeding between them.

Conclusions

The level of inbreeding between individuals determines offspring fitness in R. brachycarpum, especially during seed maturation. Genetic relatedness between parents caused inbreeding depression in their progeny. Therefore, biparental inbreeding contributes little to reproduction and instead acts as a selection force that promotes outcrossing, as offspring of more distant (less related) parents survive better.     

The mean and variability of a floral trait have opposing effects on fitness traits

Background and Aims Floral traits are essential for ensuring successful pollination and reproduction in flowering plants. In particular, style and anther positions are key for pollination accuracy and efficiency. Variation in these traits among individuals has been well studied, but less is known about variation within flowers and plants and its effect on pollination and reproductive success.Methods Style deflexion is responsible for herkogamy and important for pollen deposition in Passiflora incarnata. The degree of deflexion may vary among stigmas within flowers as well as among flowers. We measured the variability of style deflexion at both the flower and the plant level. The fitness consequences of the mean and variation of style deflexion were then evaluated under natural pollination by determining their relationship to pollen deposition, seed production and average seed weight using structural equation modelling. In addition, the relationship between style deflexion and self-pollen deposition was estimated in a greenhouse experiment.Key Results We found greater variation in style deflexion within flowers and plants than among plants. Variation of style deflexion at the flower and plant level was positively correlated, suggesting that variability in style deflexion may be a distinct trait in P. incarnata. Lower deflexion and reduced variation in that deflexion increased pollen deposition, which in turn increased seed number. However, lower styles also increased self-pollen deposition. In contrast, higher deflexion and greater variability of that deflexion increased variation in pollen deposition, which resulted in heavier seeds.Conclusions Variability of style deflexion and therefore stigma placement, independent from the mean, appears to be a property of individual P. incarnata plants. The mean and variability of style deflexion in P. incarnata affected seed number and seed weight in contrasting ways, through the quantity and potentially quality of pollen deposition. This antagonistic selection via different fitness components may maintain diverse style phenotypes.     

Global 5-methylcytosine alterations in DNA during ageing of Quercus robur seeds

Background and Aims Epigenetic regulation plays an important role in the management of plant growth, development and response to stress factors, and several reports have indicated that DNA methylation plays a critical role in seed development and viability. This study examines changes in 5-methylcytosine (m⁵C) levels in the DNA of seeds during ageing, a process that has important implications for plant conservation and agriculture.Methods Changes in the global level of m⁵C were measured in mature seeds of oak, Quercus robur. The extent of DNA methylation was measured using a protocol based on two-dimensional thin-layer chromatography. Viability of seeds was determined by germination and seedling emergence tests.Key Results An ageing-related decrease in total m⁵C during storage of recalcitrant seeds was highly and significantly correlated with a decrease in seed viability, as reflected by a reduction in germination (r = 0·8880) and seedling emergence (r = 0·8269).Conclusions The decrease in viability during ageing of Q. robur seeds is highly correlated with a global decline in the amount of m⁵C in genomic DNA, and it is possible that this may represent a typical response to ageing and senescence in recalcitrant seeds. Potential mechanisms that drive changes in genomic DNA methylation during ageing are discussed, together with their implications for seed viability.     

Effect of seed position in spikelet on life history of Eremopyrum distans (Poaceae) from the cold desert of north-west China

Background and Aims

Most studies on seed position-dependent effects have focused on germination characteristics. Our aim was to determine the effects of seed position in the spikelet on differences in timing of germination and on the ecological life history of the grass Eremopyrum distans in its cold desert habitat.

Methods

For seeds in three spikelet positions, morphology, mass and dormancy/germination characteristics were determined in the laboratory, and seeds planted in field plots with and without watering were followed to reproduction to investigate seedling emergence and survival, plant size and seed production.

Key Results

After maturation, of the seeds within the spikelet, basal ones (group 1) are the largest and have the highest proportion with physiological dormancy, while distal ones (group 3) are the smallest and have the highest proportion of non-dormant seeds. A higher percentage of seeds after-ripened in groups 2 and 3 than in group 1. Seeds sown in the field in early summer and watered at short, regular intervals germinated primarily in autumn, while those under natural soil moisture conditions germinated only in spring. Both cohorts completed their life cycle in early summer. Seeds in group 1 had lower percentages of seedling emergence and higher percentages of seedling survival than those in groups 2 and 3. Also, plants from group 1 seeds were larger and produced more seeds per plant than those from groups 2 and 3.

Conclusions

Seed position-dependent mass was associated with quantitative differences in several life history traits of E. distans. The environmentally enforced (low soil moisture) delay of germination from autumn to spring results in a reduction in fitness via reduction in number of seeds produced per plant.     

Dormancy as exaptation to protect mimetic seeds against deterioration before dispersal

Background and Aims

Mimetic seeds simulate the appearance of fleshy fruits and arilled seeds without producing nutritive tissues as a reward for seed dispersers. In this strategy of seed dispersal, seeds may remain attached to the mother plant for long periods after maturity, increasing their availability to naïve seed dispersers. The hypothesis that seed coat impermeability in many tropical Fabaceae with mimetic seeds serves as an exaptation to protect the seeds from deterioration and rotting while awaiting dispersal was investigated.

Methods

Seed coat impermeability was evaluated in five mimetic-seeded species of tropical Fabaceae in south-eastern Brazil (Abarema langsdorffii, Abrus precatorius, Adenanthera pavonina, Erythrina velutina and Ormosia arborea) and in Erythrina speciosa, a ‘basal’ species in its genus, which has monochromatic brown seeds and no mimetic displays. Seed hardness was evaluated as a defence against accelerated ageing (humid chamber at 41 °C for 144 h). Seed development and physiological potential of O. arborea was evaluated and the effect of holding mature seeds in pods on the mother plant in the field for a period of 1 year under humid tropical conditions was compared with seeds stored under controlled conditions (15 °C and 40 % relative air humidity).

Key Results

All five mimetic-seeded species, and E. speciosa, showed strong coat impermeability, which protected the seeds against deterioration in accelerated ageing. Most O. arborea seeds only became dormant 2 months after pod dehiscence. Germination of seeds after 1 year on the plant in a humid tropical climate was 56 %, compared with 80 % for seeds stored in controlled conditions (15 °C, 45 % relative humidity). Seedling shoot length after 1 year did not differ between seed sources.

Conclusions

Dormancy acts in mimetic-seeded species as an exaptation to reduce seed deterioration, allowing an increase in their effective dispersal period and mitigating the losses incurred by low removal rates by naïve avian frugivores.     

The effect of temperature on reproduction in the summer and winter annual Arabidopsis thaliana ecotypes Bur and Cvi

Background and Aims

Seed yield and dormancy status are key components of species fitness that are influenced by the maternal environment, in particular temperature. Responses to environmental conditions can differ between ecotypes of the same species. Therefore, to investigate the effect of maternal environment on seed production, this study compared two contrasting Arabidopsis thaliana ecotypes, Cape Verdi Isle (Cvi) and Burren (Bur). Cvi is adapted to a hot dry climate and Bur to a cool damp climate, and they exhibit winter and summer annual phenotypes, respectively.

Methods

Bur and Cvi plants were grown in reciprocal controlled environments that simulated their native environments. Reproductive development, seed production and subsequent germination behaviour were investigated. Measurements included: pollen viability, the development of floral structure, and germination at 10 and 25 °C in the light to determine dormancy status. Floral development was further investigated by applying gibberellins (GAs) to alter the pistil:stamen ratio.

Key Results

Temperature during seed development determined seed dormancy status. In addition, seed yield was greatly reduced by higher temperature, especially in Bur (>90 %) compared with Cvi (approx. 50 %). The reproductive organs (i.e. stamens) of Bur plants were very sensitive to high temperature during early flowering. Viability of pollen was unaffected, but limited filament extension relative to that of the pistils resulted in failure to pollinate. Thus GA applied to flowers to enhance filament extension largely overcame the effect of high temperature on yield.

Conclusions

High temperature in the maternal environment reduced dormancy and negatively affected the final seed yield of both ecotypes; however, the extent of these responses differed, demonstrating natural variation. Reduced seed yield in Bur resulted from altered floral development not reduced pollen viability. Future higher temperatures will impact on seed performance, but the consequences may differ significantly between ecotypes of the same species.     

Seed dispersal by wind decreases when plants are water‐stressed,potentially counteracting species coexistence and niche evolution

Hydrology is a major environmental factor determining plant fitness, and hydrological niche segregation (HNS) has been widely used to explain species coexistence. Nevertheless, the distribution of plant species along hydrological gradients does not only depend on their hydrological niches but also depend on their seed dispersal, with dispersal either weakening or reinforcing the effects of HNS on coexistence. However, it is poorly understood how seed dispersal responds to hydrological conditions. To close this gap, we conducted a common‐garden experiment exposing five wind‐dispersed plant species (Bellis perennis, Chenopodium album, Crepis sancta, Hypochaeris glabra, and Hypochaeris radicata) to different hydrological conditions. We quantified the effects of hydrological conditions on seed production and dispersal traits, and simulated seed dispersal distances with a mechanistic dispersal model. We found species‐specific responses of seed production, seed dispersal traits, and predicted dispersal distances to hydrological conditions. Despite these species‐specific responses, there was a general positive relationship between seed production and dispersal distance: Plants growing in favorable hydrological conditions not only produce more seeds but also disperse them over longer distances. This arises mostly because plants growing in favorable environments grow taller and thus disperse their seeds over longer distances. We postulate that the positive relationship between seed production and dispersal may reduce the concentration of each species to the environments favorable for it, thus counteracting species coexistence. Moreover, the resulting asymmetrical gene flow from favorable to stressful habitats may slow down the microevolution of hydrological niches, causing evolutionary niche conservatism. Accounting for context‐dependent seed dispersal should thus improve ecological and evolutionary models for the spatial dynamics of plant populations and communities.     

Variation of seed heteromorphism in Chenopodium album and the effect of salinity stress on the descendants

Background and Aims

Chenopodium album is well-known as a serious weed and is a salt-tolerant species inhabiting semi-arid and light-saline environments in Xinjiang, China. It produces large amounts of heteromorphic (black and brown) seeds. The primary aims of the present study were to compare the germination characteristics of heteromorphic seeds, the diversity of plant growth and seed proliferation pattern of the resulting plants, and the correlation between NaCl stress and variation of seed heteromorphism.

Methods

The phenotypic characters of heteromorphic seeds, e.g. seed morphology, seed mass and total seed protein were determined. The effects of dry storage at room temperature on dormancy behaviour, the germination response of seeds to salinity stress, and the effect of salinity on growth and seed proliferation with plants derived from different seed types were investigated.

Key Results

Black and brown seeds differed in seed morphology, mass, total seed protein, dormancy behaviour and salinity tolerance. Brown seeds were large, non-dormant and more salt tolerant, and could germinate rapidly to a high percentage in a wider range of environments; black seeds were salt-sensitive, and a large proportion of seeds were dormant. These characteristics varied between two populations. There was little difference in growth characteristics and seed output of plants produced from the two seed morphs except when plants were subjected to high salinity stress. Plants that suffered higher salinity stress produced more brown (salt-tolerant) seeds.

Conclusions

The two seed morphs of C. album exhibited distinct diversity in germination characteristics. There was a significant difference in plant development and seed proliferation pattern from the two types of seeds only when the parent plants were treated with high salinity. In addition, seed heteromorphism of C. album varied between the two populations, and such variation may be attributed, at least in part, to the salinity.     

The impact of plant and flower age on mating patterns

Background

Over a season, plant condition, amount of ongoing reproduction and biotic and abiotic environmental factors vary. As flowers age, flower condition and amount of pollen donated and received also vary. These internal and external changes are significant for fitness if they result in changes in reproduction and mating.

Scope

Literature from several fields was reviewed to provide a picture of the changes that occur in plants and flowers that can affect mating over a season. As flowers age, both the entire flower and individual floral whorls show changes in appearance and function. Over a season, changes in mating often appear as alteration in seed production vs. pollen donation. In several species, older, unpollinated flowers are more likely to self. If flowers are receiving pollen, staying open longer may increase the number of mates. In wild radish, for which there is considerable information on seed paternity, older flowers produce fewer seeds and appear to discriminate less among pollen donors. Pollen donor performance can also be linked to maternal plant age. Different pollinators and mates are available across the season. Also in wild radish, maternal plants appear to exert the most control over paternity when they are of intermediate age.

Conclusions

Although much is known about the characters of plants and flowers that can change over a season, there is less information on the effects of age on mating. Several studies document changes in self-pollination over time, but very few, other than those on wild radish, consider more subtle aspects of differential success of pollen donors over time.     

Predator satiation and recruitment in a mast fruiting monocarpic forest herb

Background and Aims

Cross-pollination and satiation of seed predators are often invoked to explain synchronous mast reproduction in long-lived plants. However, explanations for the synchronous death of parent plants are elusive. The roles of synchronous seeding and post-reproductive mortality were investigated in a perennial monocarpic herb (Isoglossa woodii) in coastal dune forest in South Africa.

Methods

Pre-dispersal seed predation and seed production were assessed by measuring fruit and seed set of inflorescences sprayed with insecticide or water and with no spray treatments. Seed predation was measured at different densities of I. woodii plants by monitoring removal rates of seed from the forest floor. The influence of adult plants on establishment of I. woodii seedlings was assessed by monitoring growth and survivorship of seedlings in caged and uncaged 1 × 1 m plots in understorey gaps and thickets.

Key Results

Fruit and seed set were similar between spray treatments. An I. woodii stem produced 767·8 ± 160·8 seeds (mean ± s.e.) on dune crests and 1359·0 ± 234·4 seeds on the foredune. Seed rain was greater on the foredune than in other topographic locations. Seed predation rates were 32 and 54 % on dune crests and in dune slacks, respectively, and decreased with seed abundance, number of inflorescences per stem and plant height. Seedling recruitment was greater beneath synchronously dying adult plants than in natural understorey gaps (no I. woodii). However, seedling growth rate beneath I. woodii mid-way through its life-cycle was less than in gaps, although survivorship was similar.

Conclusions

The selective advantage of masting in I. woodii derives from satiation of both pre- and post-dispersal seed predators. In addition, post-seeding mortality of adult plants facilitates seedling establishment. Satiation of seed predators and the benefits of seedling establishment are strong drivers of the evolution of synchronous monocarpy in I. woodii.     

Demography, reproduction, and dormancy along altitudinal gradients in three intermountain Allium species with contrasting abundance and distribution

Little is known about the variation in demographics, flower number, fruit set, and summer dormancy in Allium species native to the Intermountain West region of the United States. The purpose of this study was to investigate demographic patterns, summer dormancy traits, and variation in reproductive characteristics among habitats. Three populations of each of three species, Allium acuminatum, A. brandegei, and A. passeyi, were studied along an altitudinal gradient in northern Utah, USA, from 2004 to 2006. Demographic data were collected from individuals in permanent plots established in each population. Individual flowering plants were periodically monitored and used to calculate reproductive characteristics. Leaf area measurements throughout the 2005 growing season and soil temperature sensors were used to assess the relationship between habitat and dormancy characteristics. Populations of the widely distributed species, A. acuminatum and A. brandegei, were dominated by individuals in seedling and flowering stages while the restricted A. passeyi had populations containing a majority of individuals in the post-seedling, but non-flowering stage-class. There was a strong directional trend in A. acuminatum reproductive traits, with flower number and fruit set decreasing with increasing elevation. The mid-elevation A. brandegei populations were reproductively more successful than the high and low-elevation populations. The high-elevation A. passeyi population had more flowers per plant and higher fruit set in comparison to the lower elevation populations. The onset of summer dormancy as indicated by the timing of leaf senescence, was associated with high soil temperatures specific to each species. In general, the timing of leaf senescence was later in higher elevation populations in all species. A smaller proportion of non-flowering individuals in A. acuminatum and A. brandegei may indicate a high seedling mortality rate or a shorter juvenile phase in comparison to A. passeyi. The A. passeyi populations exhibit demographic characteristics of rare taxa; low seed production and low seedling recruitment. The high number of non-flowering plants in A. passeyi likely includes many reproductively mature individuals which are influenced by the unique habitat and environment of this species. Temperature is likely the key environmental cue inducing summer dormancy in all three species.     

Effects of defoliation and shading on the physiological cost of reproduction in silky locoweed Oxytropis sericea

Background

The production of flowers, fruits and seeds demands considerable energy and nutrients, which can limit the allocation of these resources to other plant functions and, thereby, influence survival and future reproduction. The magnitude of the physiological costs of reproduction depends on both the factors limiting seed production (pollen, ovules or resources) and the capacity of plants to compensate for high resource demand.

Methods

To assess the magnitude and consequences of reproductive costs, we used shading and defoliation to reduce photosynthate production by fully pollinated plants of a perennial legume, Oxytropis sericea (Fabaceae), and examined the resulting impact on photosynthate allocation, and nectar, fruit and seed production.

Key Results

Although these leaf manipulations reduced photosynthesis and nectar production, they did not alter photosynthate allocation, as revealed by ¹³C tracing, or fruit or seed production. That photosynthate allocation to reproductive organs increased >190 % and taproot mass declined by 29 % between flowering and fruiting indicates that reproduction was physiologically costly.

Conclusions

The insensitivity of fruit and seed production to leaf manipulation is consistent with either compensatory mobilization of stored resources or ovule limitation. Seed production differed considerably between the two years of the study in association with contrasting precipitation prior to flowering, perhaps reflecting contrasting limits on reproductive performance.