The study mentioned previously was conducted on recombinant inbred lines, which although derived from natural ecotypes are not natural genotypes. In order to test how seasonal maternal effects influence the life cycles expressed by natural ecotypes, and in particular whether this rapid-cycling life history actually occurs in natural ecotypes, a demographic study was conducted, the results of which are presented here.
In this study, seeds were collected from four natural populations of A. thaliana
in MA, USA, during their two flowering periods: the first in June and the second in late October through to early December. The seeds from these two cohorts were planted in a common garden immediately after collection, and the cohorts were followed for two generations in order to obtain the demographic data. (See appendix A
for details on experimental set-up.)
The study showed that these natural populations exhibited great variation in life history, exhibiting a winter annual, spring annual and rapid-cycling life history (). In particular, seeds that matured in autumn can germinate the following spring, and those germinants can survive to reproduce. While it is conceivable that autumn-flowering and spring-flowering sibships represent differentiated populations in some situations, in this study a single sibship that was collected from plants flowering in autumn actually produced progeny that reproduced in spring. This result indicates that autumn versus spring flowering is not completely genetically determined. Rather, plasticity of flowering time as a function of the timing of germination probably accounts for populations with mixed life histories.
Figure 3 Transition probabilities between the stages of the life cycles shown in . Numbers represent the probability that one life stage will complete the transition to the next life stage. Probabilities less than 1 are due to mortality or choices at branch (more ...)
The germination behaviour of spring-matured seeds differed greatly from that of autumn-matured seeds with respect to mortality and germination timing of surviving seeds (). Twenty per cent of spring-matured seeds germinated in the autumn, and 1.4 per cent remained dormant and germinated the following spring (while the remaining did not germinate over the 2-year period of the study and were probably dead). By contrast, germination percentages were lower overall for autumn-matured seeds, with 5 per cent of the seeds germinating in the spring and 2 per cent of them remaining dormant until the following autumn (the rest apparently being inviable). Estimated seed mortality, therefore, differed between seeds matured in spring (79%) versus autumn (93%). Moreover, germination phenology itself differed between cohorts; for those seeds that did germinate, 93.5 per cent of the spring-matured seeds germinated in autumn, whereas only 28.6 per cent of the autumn-matured seeds germinated in autumn. These results contrast to the previous experimental studies mentioned above (Munir et al. 2001
; Donohue et al. 2005a
), in that these autumn-dispersed seeds were not able to germinate during the same autumn in which they were dispersed, but rather delayed germination until spring. Very likely, the cooler temperatures experienced by autumn-matured seeds during seed maturation in the field contributed to their dormancy.
In agreement with the previous studies, germination timing had a strong effect on fitness, with winter annual autumn germinants producing an estimated 1700 seeds while spring germinants produce an estimated 60 seeds. In fact, a sensitivity analysis (Caswell 2001
) showed that the transition from (spring matured) seed to germinant was the trait that, if altered, would have the largest effect on projected population growth rate (). The next most important transitions—specifically, the probability that autumn germinants flower in autumn, and the probability that overwintering rosettes survive to reproduce—had sensitivities less than one-third of the transition from seed to seedling. Therefore, changes in germination behaviour are predicted to influence population performance more than changes in any other life stage.
Sensitivity values for each transition. Sensitivities measure the unit change in the projected population growth rate (number of progeny per capita per generation) that would occur if the transition were changed by 1 unit.
While the rapid-cycling life history did occur in natural populations, that life-history pathway actually did not contribute much to the projected growth rate of these populations, as is clear from the extremely low sensitivities of the transitions in that pathway. This is largely because autumn-flowering plants produced so few viable seeds, and those seeds that did germinate (primarily in spring) flowered at a smaller size and consequently produced fewer seeds. However, the transition that avoids that pathway does have an appreciable sensitivity value (1.3); if fewer plants overwintered and reproduced the following spring, but instead reproduced in the previous autumn, then population growth rates would be depressed.
Given these observed transition probabilities, one can ask how population growth rates would be affected if maternal effects did not influence germination. If autumn-matured seeds had the same germination behaviour as spring-matured seeds (i.e. if they had a 20% probability of germinating in autumn, as opposed to 2%, and if they had 1.4% probability of germinating in spring, as opposed to 5%), projected population growth rate is barely altered (a). This is because only a small number of seeds were produced by autumn-flowering plants. If the converse were true, such that spring-matured seeds germinated in the same proportions as autumn-matured seeds, then projected population growth rates would be depressed by 30 per cent, indicating an appreciable influence of seasonal maternal effects on projected population growth rates under some conditions.
Figure 5 Projected population growth rates, λ, based on the matrix of transition probabilities presented in . (a) A comparison of the projected population growth rates when the actual observed transition probabilities were used to calculate λ (more ...)
Moreover, projected population growth rates depend on the relative proportion of seeds that experience the different seed maturation conditions (b). If autumn-matured seeds were equally abundant as spring-matured seeds, the projected population growth rate would be lower, given the observed maternal effects; this is because a higher proportion of all seeds would germinate in spring (having been matured in autumn), and consequently be smaller and have lower fitness. If autumn-matured seeds had been equally abundant as winter annual spring-matured seeds, and if they exhibited the germination behaviour of spring-matured seeds, then the projected population growth rate would increase by 31 per cent compared with the case with the observed maternal effects on germination. By contrast, if spring-matured seeds behaved just as autumn-matured seeds, the projected population growth rate would be reduced by a further 11 per cent, and the population would actually decline, since λ would be less than 1. In this case, when the two seed types are equally abundant, the seasonal maternal effects on germination would actually determine whether the population increases or decreases in size.
These results show that seasonal maternal effects on germination are very likely manifest in natural populations, and they influence fitness, life cycles and the demographic performance of populations. These maternal effects would be more important, moreover, when the different maternal environments, in this case the frequency of the autumn- versus spring-flowering life histories, approach equal frequencies in the population. Thus, population demography is expected to be influenced by the opportunity for maternal environmental effects, via variation in reproductive phenology, and by the magnitude of these maternal effects on seed traits.
More generally, diverse demographic consequences of maternal effects can be expected in plant populations. In C. americana
, for example, adaptive maternal effects caused higher projected population growth rates than experimentally disrupted maternal effects (Galloway & Etterson 2007
), indicating that the matching of maternal cues and progeny environments is important for predicting demographic consequences of maternal effects. Moreover, maternal effects on between-year dormancy would influence bet-hedging dynamics, since greater dormancy can lead to lower temporal variance in fitness and consequently more stable population sizes in temporally variable environments (e.g. Venable 1985
; Brown & Venable 1986
; Venable et al. 1987
; Evans et al. 2007
). In perennial species, maternal effects on between-year dormancy have the potential to influence the age structure of populations, which in turn would influence projected population growth rates, probability of population extinction and genetic variation (Kalisz & McPeek 1992
; Tonsor et al. 1993
). Owing to the pronounced importance of dormancy to plant population dynamics, maternal effects on germination phenology have the potential to strongly determine the demographic dynamics of plant populations.