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Department of Biology, University of Virginia, Charlottesville, Virginia 22903-2477 USA
Received for publication March 28, 2000. Accepted for publication June 27, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Campanula americana • genotype-by-environment interaction • germination • maternal effects • parental effects • paternal effects • seed mass
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Schmid and Dolt, 1994
; Mazer and Gorchov, 1996
; Rossiter, 1996
). First, the maternal parent provisions the offspring, and the quantity and quality of resources available for provisioning are strongly environment dependent. Second, two-thirds of the endosperm genetic material and the cytoplasmic DNA are typically of maternal origin and environmentally influenced gene expression may therefore disproportionately reflect the maternal environment (Mazer and Gorchov, 1996
). Last, the thickness of the seed coat may be affected by the maternal environment, influencing dormancy and timing of germination (Sultan, 1996
; Lacey, Smith, and Case, 1997
; Baskin and Baskin, 1998
). Empirical studies in plants support the expectation that maternal environments commonly influence their offspring's phenotype (Roach and Wulff, 1987
; Rossiter, 1996
; Donohue and Schmitt, 1998
).
In contrast, we know very little about paternal environmental effects. The paternal environment's influence on the offspring is only prezygotic (Lacey, 1996
). As a consequence, the mechanisms by which paternal environments may influence the offspring phenotype are less direct than those of maternal environments (Schmid and Dolt, 1994
; Mazer and Gorchov, 1996
). Until recently paternal environmental effects have frequently been assumed to be negligible (Roach and Wulff, 1987
). However, there is mounting evidence that the paternal environment may influence both pollen quantity and quality (e.g., Young and Stanton, 1990
; Delph, Johannsson, and Stephenson, 1997
; Aizen and Raffaele, 1998
). But it is not known whether these environmental effects on pollen influence the offspring generation. The few studies to date have found equivocal evidence for paternal environmental effects (Young and Stanton, 1990
; Schmid and Dolt, 1994
; Lacey, 1996
). In natural populations, the environment of pollen production, ovule production, and seed production will vary among individuals reflecting small-scale spatial environmental heterogeneity (cf. Antonovics, Clay, and Schmitt, 1987
; Bell, Lechowicz, and Schoen, 1991
; Stratton, 1994
). As a result, pollen produced in one environmental condition will likely fertilize ovules produced in another. Due to this pattern of natural variation, it is important to determine whether both parental environments influence offspring characters. Moreover, it is possible that the expression of paternal environmental effects depends on the maternal environment. There are no studies to date that have tested whether the maternal and the paternal environments jointly affect the progeny phenotype (but see Lacey, 1996
).
Campanula americana is a woodland herb that grows as either an annual or a biennial. Germination time determines life history schedule (Baskin and Baskin, 1984
). Seeds may germinate immediately after dispersal in the late summer or fall, the following spring, or they may enter the seed bank, germinating in either season in the future (Wardle, 1998
). The vegetative rosettes have a vernalization requirement for flowering. Therefore, seeds that germinate in the fall are winter annuals and flower the following summer, whereas those that germinate in the spring exhibit a strict biennial life history and flower the summer of their second year. Because parental effects are typically strongest for juveniles, especially seed characters (Roach and Wulff, 1987
; Schmitt, Niles, and Wulff, 1992
; Platenkamp and Shaw, 1993
; Donohue and Schmitt, 1998
), they may influence life history in this system. If genetically based, parental environmental effects may play a role in the evolution of this polymorphic life history.
To determine the potential for parental environmental effects to influence life history in C. americana, a controlled environment study was conducted in which families from two populations were grown under a series of nutrient and light environments. Nutrient and light were chosen as environmental factors because C. americana is typically found in nutrient-rich soils on roadsides, stream cuts, and relatively open understory habitats where light is patchily distributed (personal observation). As a result these two resources are variable for C. americana and appear to limit its distribution (personal observation). This study addresses the following questions: (1) Do maternal or paternal light and nutrient environments affect seed characters in C. americana? (2) If so, do the maternal and the paternal environments influence offspring characters independently? (3) Is there variation between populations or among families within populations for parental effects suggesting that they are genetically variable?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Johnson, Delph, and Elderkin, 1995
). I will refer to a group of siblings as a "family." Seeds were germinated later in the fall in a growth chamber (25°/15°C 12-h days). Two weeks after germination, seedlings were cold stratified for 6 wk at 5°C to induce flowering (Baskin and Baskin, 1984
).
Parental light environments
Following cold stratification, seedlings were moved to the greenhouse and transplanted into 15.5-cm pots in a soilless potting mix (2:1 Promix BX : Perlite). At this time, eight families from the River site and eight from the Mountain site were arbitrarily selected to evaluate the influence of parental light on offspring seed and germination characters. Two to three individuals from each family were randomly assigned to each of the following light treatments: full sun ("high"), 30% neutral shade ("medium"), and 73% neutral shade ("low"). The treatment levels were chosen to span the light gradient found in natural populations (personal observation). In total, 84 individuals were grown. Groups of 4–5 individuals in the same light level were clustered and surrounded by a shade enclosure if necessary. Individuals were fertilized every 2 wk with 20:20:20 NPK fertilizer and supplemental lighting increased day length to 18 h to stimulate flowering.
Parental nutrient environments
Ten different families from the River site and eight from the Mountain site were selected to evaluate the effect of parental nutrient environment on seed and germination characters. Two or three individuals from each family were randomly assigned to each of the following nutrient treatments: weekly addition of Peters NPK 20:20:20 fertilizer ("high"), no nutrient addition ("medium"), or no supplemental nutrients and the addition of 50% nutritionally inert fritted clay to the potting medium ("low"). The potting medium contained some nutrients and provided a limited nutrient supply to the medium- and the low-nutrient plants. With the exception of the low-nutrient individuals, potting conditions were identical to those for the light experiment. All plants were fertilized twice in the first 2 wk following removal from the cold. However, the fertilizer was diluted in the limited nutrient treatments to one-quarter strength for the medium and one-eighth strength for the low-nutrient individuals. The 90 plants were grown in randomized locations in a separate bay of the greenhouse from the light experiment. Supplemental lights increased day length to 18 h.
Experimental crosses
For each environmental gradient, individuals were crossed to create seeds with all combinations of maternal and paternal environments. Once most plants had started flowering, crosses were conducted separately for each population. Flowers were emasculated in the bud prior to anther dehiscence to prevent self-pollination. On each day of pollinations, plants were arbitrarily divided into two groups; the specific members of each group varied from day to day. In each group, pollen was collected from one newly open flower per plant. Pollen from flowers in the same treatment and population was mixed and applied to open stigmas on plants in all three treatments in the other group. A maximum of three pollinations for each paternal environment were conducted on each maternal plant. Dividing the plants into two groups permitted mixed-donor pollinations while avoiding the potential for self-pollination. However, sib-pollinations were not controlled and because on average eight families contributed to the pollen pool, one of every eight pollen donors was a sibling. Pollinations resulted in nine types of seed for each environmental gradient (3 maternal environments x 3 paternal environments). Because the same families were grown in each level of the environmental treatment, on average the paternal genetic contribution was constant across the paternal environments.
The fruits were collected when ripe, and seeds were counted in each fruit. After the fruits were collected, the aboveground biomass of each plant was harvested and weighed when dry.
Test of parental effects
Parental environmental effects were evaluated for seed characters. A single fruit was chosen for each paternal treatment on each maternal plant and six typical seeds were selected from the 
40 present. This resulted in 15 seeds for each maternal–paternal combination for each family (6 seeds/paternal treatment/maternal plant x 2–3 maternal plants/maternal treatment), and on average of 45 seeds for each maternal and each paternal treatment for each family. Seeds were individually weighed on a microbalance. Seeds from all families and treatments were randomized and placed on damp filter paper in tissue culture trays. The trays were placed in an environmental chamber with 12-h days at 21°/14°C, close to optimum conditions for C. americana (Baskin and Baskin, 1984
). The filter paper was kept moist, and seeds were checked daily for germination (extension of the radicle beyond the seed coat). Germination was scored for 100 d, although the number of days to germination through day 50 (on average 94% of the total) will be presented as inconsistent moisture influenced later germination. Percentage germination was calculated for each treatment combination for each family at day 10 for the River population and day 20 for the Mountain, near their respective germination peaks. The percentage of seeds that had germinated by the peak germination date was analyzed since total percentage germination for some treatments in the River population was not sufficiently variable for analysis (83% on average). Total germination in the Mountain population was only 43%, but the correlation between peak germination and total germination in this population was R = 0.90, therefore peak germination approximates total germination. The influence of parental environments on four characters will be presented: seed number per fruit, individual seed mass, number of days to germination, and percentage germination.
Statistical analysis
Response to the light and nutrient environments in the parental and offspring generations was evaluated using analysis of variance (ANOVA). For parental biomass, ANOVA included the maternal environment and population as fixed effects and family (nested within population) as a random effect. For seed number/fruit, seed mass, and days to germination, ANOVA was conducted with maternal environment, paternal environment, and population as fixed effects. Family (nested within population) and maternal plant (nested within population, family, and maternal environment) were included as random effects. Analyses included all possible interactions except at the level of maternal plant and were conducted using PROC GLM of the SAS statistical package (SAS Institute, 1990
). However, the three-way interaction among maternal environment, paternal environment, and family was not included for seed number/fruit since there was not sufficient replication at this level. In addition, for this variable interactions were combined with the error if not significant. A significant interaction between the maternal and the paternal environment indicated that the parental environments jointly contributed to expression of offspring characters. To understand the pattern of these joint parental effects, ANOVA was used to compare paternal environments within each level of the maternal environment (analyses not shown, but results are indicated on the figures as differences in paternal environment means). When there were significant parental environmental effects, Tukey multiple comparison tests were used to compare treatment levels within a factor.
Because percentage germination was calculated for each family in each maternal and paternal treatment combination, interactions between parental environments and family were not evaluated for this character. In addition, populations were analyzed separately because percentage germination was calculated at the peak germination time, and this time differed between the populations. Parental biomass was square-root transformed, days to germination natural log transformed, and percentage germination arcsine transformed to meet assumptions of normality.
Statistical interactions between the parental environment and population demonstrate that the populations respond differently to the parental environmental treatments. To understand these differences, further analyses were conducted for each population following a significant interaction. Differences in parental effects between populations expressed in a common environment are likely to be genetic. However, because the parental generation was raised from field-collected seed, environmental differences between the sites may have contributed to population differentiation through second-generation "grandparental" environmental effects (cf. Alexander and Wulff, 1985
; Miao, Bazzaz, and Primack, 1991
; Case, Lacey, and Hopkins, 1996
). The contribution of the grandparental field environment is likely to have had a much smaller effect on offspring seed characters than the disparate parental conditions in the greenhouse (e.g., Wulff et al., 1999
). The interaction between the parental environments and family reveals that the expression of parental environmental effects varies across families. Variation among field-collected families in a common environment represents broadsense genetic variation (although it may include grandparental environmental effects, but see above; Kalisz and Wardle, 1994
).
Last, parental effects may act directly on germination characters or may alter patterns of germination through changes in seed size. If seed mass is included in an analysis as a covariate, then the analysis tests for the presence of parental effects that act independently of seed size. If seed mass is not included as a covariate, the analysis tests for parental effects that act both through seed size and independent of seed size. By exploring the consequences of including seed mass as a covariate, the contribution of parental effects on seed size to later characters can be determined.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Offspring response to parental nutrients
Both maternal and paternal nutrient levels influenced seed mass, but the pattern differed between populations (Mat nut x Pop, F2,34 = 3.93, P < 0.03). Seed mass increased in response to increasing maternal nutrient levels in the Mountain population (nearly significant P < 0.055), but decreased slightly in the River population (Fig. 1). However, the pattern of increase in the Mountain population depended on the paternal nutrient level (Table 1). Seeds produced under a low maternal nutrient environment were smaller if they were fathered by plants growing under medium-nutrient conditions; when maternal nutrients were not as limited the paternal environment did not influence seed mass (Fig. 1). In the River population, the paternal nutrient level had a nearly significant effect on seed mass (Table 1, P < 0.06); seeds with high-nutrient fathers tended to be heavier (Fig. 1). In both populations there was a significant maternal nutrient by paternal nutrient by family interaction, revealing genetic variation in the response of seed mass to specific maternal and paternal nutrient combinations (Table 1). Therefore, the patterns of parental effects in Fig. 1 simply represent the average across families for response to the parental nutrient environment.
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The effect of parental nutrient level on the number of days to germination differed among families in both populations, indicating genetic variation in parental nutrient effects (Table 2). There was also trend toward different patterns of parental effects in the two populations (Mat nut x Pop, P < 0.08, Mat nut x Pat nut x Pop, P < 0.07; Table 2). However, there was no clear effect of the maternal or paternal nutrient environment on offspring days to germination in either population. Seeds from the River population germinated earlier (11.1 ± 0.4 d) than those from the Mountain population (14.1 ± 0.7 d). Seed size influenced the number of days to germination (Table 2); large seeds germinated earlier. If parental effects were allowed to influence days to germination through seed size (i.e., no covariate), there was no qualitative change in the results (analysis not shown).
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On average, parental light environments had a greater influence on timing of germination in the Mountain population (Mat light x Pat light x Pop, F4,126 = 4.52, P < 0.002; Fig. 4). In the Mountain population, the maternal and paternal light environments jointly affected days to germination (Table 5). While average days to germination were similar for seeds produced in all maternal light levels, those produced on maternal plants growing in low-light environments germinated earlier if their father grew in intermediate-light conditions (Fig. 4). There was also variation in days to germination in response to maternal light environment among families (Table 5), revealing genetic variation for maternal effects in days to germination in this population. Seed mass did not influence timing of germination in either population.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). If the paternal environment typically acts jointly with the maternal environment, experiments that do not evaluate interactions between the parental environments may miss the contribution of the paternal environment to the offspring phenotype. Because studies have not explored possible interactions between the parental environments, it is not known whether the paternal environmental effects found in other studies (Schmid and Dolt, 1994
; Lacey, 1996
) may also vary across maternal environments.
The source of paternal environmental effects is difficult to determine. A number of studies have demonstrated that pollen quality and quantity varies with the environment and may affect an individual's ability to sire seeds (e.g., Young and Stanton, 1990
; Delph, Johannsson, and Stephenson, 1997
; Aizen and Raffaele, 1998
; Lehtilä and Strauss, 1999
). In natural populations, heterogeneous environments may lead to differences in siring ability among individuals due to variation in pollen quantity or quality. In the present experiment, the environment was constant across individuals within a paternal treatment. However, if the response of pollen characters to the environment varied among families (i.e., genotype-by-environment interaction), the family with the greatest amount of viable pollen may vary across environments. As a consequence, the paternal environment may bias paternity, resulting in a genetic source to the "environmental" paternal effects.
This scenario is possible in the present experiment where pollen was pooled from families in each paternal environmental treatment. In congener C. rapunculoides, pollen number, size, percentage germination, and pollen tube length did not vary with the environment, however, there was a genotype-by-environment interaction for pollen viability (Vogler, Peretz, and Stephenson, 1999
). If true for C. americana, differences in pollen viability among families that also differ for offspring characters could create paternal environmental effects. However, the influence of individuals with particularly high siring ability in any given treatment should be diminished because the composition of the pollen pool differed for each recipient across days and between groups of individuals within days. In addition, paternal effects varied with the maternal environment. It seems likely that differences in pollen quality or quantity would have a consistent effect across maternal treatments (but see Marshall and Ellstrand, 1988
, for a possible mechanism). The only way to fully separate the effects of the paternal environment from genotype-by-interactions for pollen characters is to compare seeds produced by clonal replicates of individuals grown in different environments (e.g., Schmid and Dolt, 1994
; Lacey, 1996
). We are presently using this approach to determine whether genotype-by-environment interactions contribute to the effect of paternal light levels on seed characters.
There are a number of additional potential causes of paternal environmental effects (reviewed in Mazer and Gorchov, 1996
). For example, there may be selection among the developing pollen grains within each environment, such that the genetic composition of the pollen produced by a given individual depends on the environment in which the pollen matured. Alternatively, environment-specific gene expression induced in the male gametophyte may create differences between the progeny produced by the same genetic father growing in different environments. Last, paternal environmental effects may simply be due to nongenetic changes in pollen that affect the offspring phenotype, for example, resource provisioning.
In contrast to the paternal environment, the maternal environment also had an independent effect on seed characters. On average, seed mass increased with increasing maternal resources. This pattern was particularly strong between the low and medium levels for both maternal light and nutrient environments. Similarly, other studies have found seed mass to increase in response to increasing maternal light (Wolfe, 1995
; Sultan, 1996
) and nutrients (Aarssen and Burton, 1990
; Schmitt, Niles, and Wulff, 1992
; Wulff and Bazzaz, 1992
), although, like the River population, there may be little response of seed mass to maternal nutrient level (Wolfe, 1995
; Sultan, 1996
; Weiner et al., 1997
). Seed number per fruit also increased with increasing maternal resources. There was little evidence for a trade-off between seed number and seed size in C. americana (see also Richardson and Stephenson, 1991
); on average, plants with more resources produced more larger seeds. Larger C. americana seeds have been found to grow faster (Richardson and Stephenson, 1992
), and, therefore, favorable maternal light and nutrient environments may enhance offspring survival and fecundity via seed size effects.
Parental environments had a greater influence on percentage germination than on days to germination. While days to germination was jointly influenced by maternal and paternal light levels in the Mountain population, that interaction was largely due to paternal effects expressed when maternal plants were grown under low-light conditions. In contrast, increasing maternal resources, whether light or nutrients, decreased the fraction of seeds with early germination independent of the paternal environment for the River population and to a lesser extent the Mountain population. Similar to our findings here, seeds of high-light maternal plants had a reduced percentage germination in Plantago (but only under dark germination conditions; Schmitt, Niles, and Wulff, 1992
). However, maternal nutrient effects on germination in other studies are not consistent. For example, high parental nutrient levels decrease (Wulff et al., 1999
) or increase (Stratton, 1989
) germination percentage and slow down (Schmid and Dolt, 1994
) or speed up (Stratton, 1989
; Aarssen and Burton, 1990
) germination. Variation in these results may be in part due to the contribution of seed size to germination. Maternal nutrient effects are likely to act through seed size in several of these studies (Stratton, 1989
; Aarssen and Burton, 1990
; Wulff et al., 1999
).
The parental light environment influenced germination characters independent of seed size in C. americana (see also Richardson and Stephenson, 1992
; Kalisz and Wardle, 1994
). In contrast, larger seeds germinated earlier and in greater numbers than smaller seeds when parents were grown under a range of nutrient environments. If the parental nutrient environment was allowed to influence germination characters through seed mass, the magnitude of the parental effects was reduced. Therefore parental environmental effects acting through seed size appear to oppose those that act directly on juvenile characters. Other studies have shown that parental effects expressed through juvenile characters, e.g., seed size, may differ from those expressed directly on later characters (Stratton, 1989
; Galloway, 1995
; Sills and Nienhuis, 1995
). Changes in the seed components may underlie these patterns. Seeds are composed of seed coat and the offspring tissues (endosperm and embryo). Therefore a change in seed mass may be due to either a change in offspring size or in seed coat thickness (e.g., Sultan, 1996
; Lacey, Smith, and Case, 1997
). Because seed mass only influenced germination characters when the parental generation was grown in a range of nutrient conditions, and the seed coat is often associated with timing of germination (cf. Sultan, 1996
; Baskin and Baskin, 1998
), these results suggest that the proportionate allocation to the seed coat may vary across the nutrient gradient, but change little in response to maternal light.
Parental environmental effects differed both between populations and among families within populations. Family variation in parental effects was found in almost every analysis (although it was not evaluated for percentage germination), suggesting that genetic variation for parental effects is pervasive. Genetically based parental environmental effects have been found in other studies (e.g., Schmitt, Niles, and Wulff, 1992
; Plantenkamp and Shaw, 1993
; Wulff, Caceres, and Schmitt, 1994
; Lacey, 1996
; Shaw and Byers, 1998
). Genetic variation within populations provides the opportunity for parental environmental effects to contribute to adaptive evolution. Indeed, the differences between populations for parental effects found here may reflect genetic divergence in response to local selective environments.
In addition to seed characters, parental environmental effects may influence life history. Germination schedule determines life history in C. americana. Seeds that germinate in the fall have an annual life history, while those that germinate in the spring are biennials. The results presented here imply that both the maternal and the paternal light environment may influence life history in the Mountain population. In addition, variation among families in response to maternal light levels in the Mountain population, and in response to the joint effect of maternal and paternal nutrient environments over both populations, implies that parental environmental effects for germination time are genetically variable. Therefore, if there is an association between parental and offspring light environment (more likely for the maternal parent than the paternal parent since pollen dispersal typically exceeds seed dispersal; Levin and Kerster, 1974
) and specific patterns of parental environmental effects enhance fitness, parental environmental effects may contribute to life history evolution in this species.
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FOOTNOTES |
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2 lgalloway{at}virginia.edu;
phone 804-982-5010; FAX 804-982-5626.
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C. Galen and M. L. Stanton Sunny-side up: flower heliotropism as a source of parental environmental effects on pollen quality and performance in the snow buttercup, Ranunculus adoneus (Ranunculaceae) Am. J. Botany, May 1, 2003; 90(5): 724 - 729. [Abstract] [Full Text] [PDF]
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J. R. Etterson and L. F. Galloway The influence of light on paternal plants in Campanula americana (Campanulaceae): pollen characteristics and offspring traits Am. J. Botany, December 1, 2002; 89(12): 1899 - 1906. [Abstract] [Full Text] [PDF]
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< 0.05
0.1 > P > 0.05, * P < 0.05, *** P < 0.001
