Maternal environmental effects occur when the phenotype or growth environment of the mother plant affects the offspring phenotype beyond the direct effect of transmitted genes
[1, 2]. The seed is simultaneously an important maternal component and a subsequent offspring. Seed traits of the first generation or even of later generations in some annual plants are dependent on the abiotic environment and seed position on the parent plant during seed development and maturation
. Seed traits of most species vary between and within individuals, and much of the variation is phenotypic
. The adaptive significance of maternal effects on seeds is being increasingly recognized
Maternal effects affect a range of offspring traits simultaneously, and these effects are likely to be highly context-dependent
. However, most studies of maternal environmental effects on seeds have examined only one maternal factor and one seed trait
, which may give an incomplete view of the influence of maternal effects
. For example, maternal plants of Senecio vulgaris grown at lower nutrient levels produced seeds that germinated later and had lower mass than those from plants grown at higher nutrient levels, but their seedlings survived longer when the maternal plant was not supplied with additional nutrients
. Thus, investigation of the interactive effect of different maternal factors on variation in seed traits is needed to gain a complete understanding of maternal environmental effects on seed quality, and thereby on the regeneration of populations.
Using an outcome-based approach, Marshall and Uller (2007) distinguished four types of maternal effects: anticipatory (increase in maternal fitness by increasing offspring fitness), selfish (increase in maternal fitness at the expense of offspring fitness), bet-hedging (reduced variation in maternal fitness by producing offspring with a range of phenotypes), and transmissive (reduction in both maternal and offspring fitness). Although this static framework is useful in distinguishing different types of maternal effects, these effects may be entangled.
Seed heteromorphism is a phenomenon in which a single plant produces different morphophysiological types of seeds
[9, 10]. Seed dimorphism can be considered the main type of this phenomenon, and it is probably a form of bet-hedging that is expressed mostly in annual plants
[9, 11, 12].On the basis of this theory, it is predicted that, in an unpredictable environment, bet-hedging maximizes the geometric mean fitness among generations
. However, most studies have focused on changes in the mean offspring phenotype, and only a few studies have been done on variation in offspring phenotypes
. In fact, there is variation even within each type of seed in heteromorphic species
. To our knowledge, no study has been done on the comparison of seed size variation of heteromorphic species under different environmental regimes. Here we focus on soil fertility and salinity as possible drivers of maternal effects on regeneration.
Nutrient availability to the maternal plant could potentially affect seed production and seed traits
. For example, seed production and seed size, germination and other seed quality traits of Sarcobatus vermiculatus were decreased substantially with nutrient limitation
. This may be a selfish maternal effect, i.e. plants may decrease seed quality and thereby increase total maternal fitness when there is a reduction in the quality of the maternal environment.
Anticipatory maternal effects are predicted to be advantageous in systems where germination conditions are spatially or temporally variable but in a somewhat predictable manner
. For example, Campanula americana grows in habitats where light is a patchily distributed resource, and their seeds typically experience the same light environment as their mother plant. Germination percentage of this species in autumn was higher when the offspring light environment matched the maternal environment
. However, knowledge about the effect of maternal salinity environment on germination of offspring seeds is limited
. We expect that seeds produced by maternal plants growing at high salinity would have higher salt tolerance than those produced by mother plants growing at low salinity, because the saline environment is predictable for the offspring of these seeds.
(Bunge) Freitag & Schütze (Amaranthaceae) is an annual halophyte which is 20–50 cm tall. It occurs in the Gobi Desert of central Asia, where it grows in saline-alkaline sandy soils
]. This species is a model organism for studying interacting maternal effects on regeneration because it occurs (1) in a heterogeneous environment in terms of soil salinity and fertility; and (2) its seeds are dimorphic
]. S. aralocaspica
plants produce brown seeds (non-dormant and high salt tolerance) and black seeds (non-deep physiological dormancy and low salt tolerance)
]. In this study, we tested the hypothesis that seed dimorphism, nutrients and salinity determine variation in offspring seed traits and germination success of S. aralocaspica
via the combination of bet-hedging, selfish and anticipatory maternal effects. This main hypothesis leads to the following specific hypotheses:
The seed morph ratio of S. aralocaspica can be fine-tuned by plant phenotype (plants from dimorphic seeds) and environmental conditions (salinity and nutrient level). We predict that the brown:black seed ratio should decrease under stressful conditions and therefore be negatively correlated with nutrient limitation and salinity. Additionally, we predict that the brown:black seed morph ratio of plants grown from brown seeds should be higher than that of plants reared from black seeds, because brown seeds germinate faster and these plants may therefore experience better growth conditions during the short window of opportunity for establishment than those from black seeds.
The size variation of brown seeds should be higher than that of black seeds, because brown seeds are dispersed further away from the mother plant than are black seeds; consequently, plants from brown seeds may experience more unpredictable environments. Further, low nutrient and high salinity levels should increase seed size variation.
Maternal nutrient limitation should decrease seed size and germination percentage of S. aralocaspica.