Elizabeth P. Lacey

Onset of Reproduction in Plants: Size= versus Age-dependency

Understanding the roles of age and size in the timing of first reproduction or flowering in plants has become a goal for those investigating the evolution of life cycle patterns in general. Here I review the studies that are helping to clarify these roles, and indicate some directions for future research.

Variance Models in the Study of Life Histories

We propose a general model that estimates fitness from the joint effects of mean and variance. In this hierarchical model the contribution that each individual trait makes to net fitness proceeds in a stepwise fashion from the individual trait level to the fitness component and cohort fitness levels and, finally, to net fitness. We describe useful mathematical functions that incorporate both mean and variance values at each level. Empirical examples (1) demonstrate that variance, in addition to mean, can be an important determinant of fitness and (2) show how both can be used to estimate fitness, in particular in research addressing the evolution of life history patterns.

PARENTAL EFFECTS IN PLANTAGO LANCEOLATA L. I. : A GROWTH CHAMBER EXPERIMENT TO EXAMINE PRE- AND POSTZYGOTIC TEMPERATURE EFFECTS

In spite of the potential evolutionary importance of parental effects, many aspects of these effects remain inadequately explained. This paper explores both their causes and potential consequences for the evolution of life‐history traits in plants. In a growth chamber experiment, I manipulated the pre‐ and postzygotic temperatures of both parents of controlled crosses of Plantago lanceolata. All offspring traits were affected by parental temperature. On average, low parental temperature increased seed weight, reduced germination and offspring growth rate, and accelerated onset of reproduction by 7%, 50%, 5%, and 47%, respectively, when compared to the effects of high parental temperature. Both pre‐ and postzygotic parental temperatures (i.e., prior to fertilization vs. during fertilization and seed set, respectively) influenced offspring traits but not always in the same direction. In all cases, however, the postzygotic effect was stronger. The prezygotic effects were more often transmitted paternally than maternally. Growth and onset of reproduction were influenced both directly by parental temperature as well as indirectly via the effects of parental temperature on seed weight and germination. Significant interactions between parental genotypes and prezygotic temperature treatment (G × E interactions) show that genotypes differ in their intergenerational responses to temperature with respect to germination and growth. The data suggest that temperature is involved in both genetically based and environmentally induced parental effects and that parental temperature may accelerate the rate of evolutionary change in flowering time in natural populations of P. lanceolata. The environmentally induced temperature effects, as mediated through G × (prezygotic) E interactions are not likely to affect the rate or direction of evolutionary change in the traits examined because postzygotic temperature effects greatly exceed prezygotic effects.

The genetic and environmental control of reproductive timing in a short-lived monocarpic species Daucus carota (Umbelliferae)

(1) Offspring of annual, biennial and triennial Daucus carota were grown under three nutrient regimes in a growth chamber to measure the effects of nutrient supply and maternal age of flowering on offspring size and growth rate and the effects of all four variables on year of flowering. (2) Offspring rosette size and recent growth rate were both good predictors of year of flowering. An increase in size but a decrease in relative growth at the end of the summer were associated with an increased probability of flowering in the next season. The results are consistent with the Wilbur—Collins model, which suggests that both size and recent growth rate influence reproductive timing and that individuals track resources by delaying the year of reproduction if resources abound or by accelerating reproduction if resources become limiting. This model, although proposed for amphibians, may describe the general relationship between growth and reproductive timing in monocarpic plants. (3) Maternal age and nutrient supply influenced rosette size, relative growth rate, and flowering time. Annual maternal plants and high nutrients produced both the largest offspring and the greatest number of annuals. Also, the maternal contribution acted directly upon the year of flowering as well as indirectly through size and recent growth. Both genetic variability and habitat heterogeneity explain the variation in year of flowering in natural populations. (4) The results provide evidence that the early-rosette growth rate and the length of the pre-reproductive period are negatively correlated, as predicted by theories about the evolution of life-history patterns. Rapid growth may help annuals to persist in habitats which generally favour biennials. (5) Response to nutrient supply did not vary among maternal age groups as might be expected in colonizing species. This suggests that phenotypic plasticity in response to nutrient supply evolves independently of year of reproduction.

Parental Effects on Seed Mass: Seed Coat but Not Embryo/Endosperm Effects

Many biologists studying environmentally induced parental effects have indirectly suggested that the parental environment alters seed mass by altering the amount of endosperm or embryo tissue in the seed. We tested this hypothesis by measuring the effects of parental temperature on total seed mass, seed coat mass, and embryo/endosperm mass in offspring of Plantago lanceolata. Parental temperature significantly affected total seed and coat mass but not endosperm/embryo mass. Thus, larger seeds do not contain more resources in the embryo or endosperm than do small seeds. Rather they have more coat mass, which probably strongly influences germination. These results suggest caution when making assumptions about the pathways by which environmentally induced parental effects are transmitted in plant species. We also observed that controlled crosses differed significantly in their response to parental temperature, which provides evidence for genetic variation in environmentally induced parental effects, i.e., intergenerational phenotypic plasticity, in natural populations of P. lanceolata.

Multigenerational effects of flowering and fruiting phenology in Plantago lanceolata

Phenological patterns of flowering and fruiting can be influenced by the effects of reproductive time on seed production. We propose here that these patterns are also influenced by phenological effects on offspring quality. Furthermore, we hypothesize that there are cross-generational trade-offs between parental and offspring components of parental fitness influencing the evolution of reproductive phenology. To test our hypothesis, we examined the multigenerational effects of flowering and fruiting phenology in Plantago lanceolata. Offspring of 30 families were transplanted into field plots to measure the effects of onsets of flowering and fruiting, duration of fruiting, percentage fungal infection, and damage by grasshoppers on total seed production, our measure of the within-generational component of parental fitness. To gather information about cross-generational contributions to parental fitness, we assessed the quality of off- spring produced at different times in terms of seed mass and germination. Families significantly differed in flowering and fruiting onsets. Larger plants began flowering earlier, and earlier flowering plants matured fruits earlier and produced fruits for a longer time. Significant family-mean correlations among these traits suggest that selection on any one trait will change all three traits. A negative family-mean correlation between fruiting onset and seed production suggests that we can expect an antagonistic trade-off in response to selection on these two traits. Early fruiting significantly reduced seed predation by grasshoppers and increased seed production. In contrast, late-maturing seeds were sig- nificantly heavier and germinated more rapidly than did early-maturing seeds produced by the same plants. The directions of the multigenerational effects support the hypothesis that there are cross-generational trade-offs between parental and offspring components of pa- rental fitness. The experiments indicate that multigenerational fitness effects should be considered in future studies addressing the evolution of flowering and fruiting phenology.

PARENTAL EFFECTS IN PLANTAGO LANCEOLATA L. III. MEASURING PARENTAL TEMPERATURE EFFECTS IN THE FIELD

Abstract. 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.

Timing of seed dispersal in Daucus carota

This study describes the temporal pattern of seed dispersal in Daucus carota and examines the fate of seeds dispersed at different dates in SE Michigan. Plants varied greatly in both time of onset and rate of dispersal. Onset was directly related to flowering time, a phenotypically plastic character, and tended to occur earlier in newly established populations. Dispersal rate was similar for different-aged populations and for plants flowering at different times. The latter indicates that later-flowering plants dispersed a greater proportion of seeds in winter. Seed germination in outdoor plots declined when dispersal was delayed experimentally. Winter dispersal distances over snow surpassed autumn dispersal distances. However, only in some years did conditions (high winds and snow cover) required for longer distance dispersal occur while many seeds were still viable. Survival and reproduction of autumnversus spring-germinating offspring varied greatly among years in experimental and natural populations. The fate of seeds dispersed at different times is unpredictable, which may explain the extended dispersal pattern observed in D. carota. Individual variation in dispersal rate is associated with environmental uncertainty in 1) timing of conditions suitable for dispersal over snow and 2) relative success of autumnversus spring-germinating offspring. Early onset of dispersal, more common in the youngest populations, improves chances for local population expansion; late onset of dispersal found in older populations improves chances for new site colonization.

Parental effects in Plantago lanceolata L. II. Manipulation of grandparental temperature and parental flowering time

In an experimental study of Plantago lanceolata L., postzygotic environmentally induced parental effects were (1) transmitted across generations, (2) genotype-specific, and (3) mediated by natural differences in flowering phenology. Individuals were cloned, hand-pollinated and allowed to mature seed at one of two temperatures. Second-generation plants were induced to seed-set at four times during the flowering season. The effects of grandparental temperature (GPT), parental flowering time (PFT) and maternal family (MFAM) on seed size, germination, leaf area and ailometry, flowering time and male sterility in third generation plants were then measured. GPT significantly affected all adult traits and did so more strongly than and often independently of seed weight and germination. The data suggest that heritable GPT effects arise from gametophytic selection or genomic modification. Significant GPT × MFAM interactions were detected for seed weight, leaf area, flowering time, and male sterility. Such genotype-specific responses are necessary if parental temperature is to influence the evolutionary divergence of life history and breeding patterns in populations growing in different temperature regimes. PFT affected leaf area and percentage germination. Natural changes in photoperiod but not temperature may explain the observed PFT effects on germination.

Effect of parental flowering and dispersal times on offspring fate in Daucus carota (Apiaceae)

Seeds collected from parents that flowered at different times were dispersed onto experimental plots at different times during the normal dispersal season. Parental flowering and dispersal times, which are correlated with each other, independently affected offspring germination, growth, and time of reproduction. Estimated population growth rates were highest for offspring that were dispersed early in the dispersal season and that came from early flowering parents. The data provide evidence that 1) an individuals fate is determined by the environment of the previous generation, and that 2) an individuals fitness should be calculated from life history data that span more than one generation.