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Reproductive Biology |
Department of Biology, Jordan Hall, 1001 East Third Street, Indiana University, Bloomington, Indiana 47405 USA
Received for publication February 11, 2003. Accepted for publication August 29, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: biparental inbreeding depression • Caryophyllaceae • crossing distance • hand pollination • Silene acaulis
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, p. 305). Darwin goes on to discuss a result in which plants pollinated by adjoining plants have lower fitness than when crossed with more distant plants. He speculates that this might be caused by the phenomenon that we now know as "isolation by distance," whereby restricted gene flow leads to population structure (Wright, 1946
; Turner et al., 1982
) and a heightened probability of biparental inbreeding (Waller, 1993
).
Biparental inbreeding is likely to occur in angiosperms with limited seed dispersal that are animal pollinated, especially if these pollinators tend to restrict their flight distances between plants (e.g., Schaal, 1975
). This has led many researchers to investigate whether crossing plants at different distances affects the fitness of the offspring (see below). The underlying premise of these studies is that relatedness should fall off with distance, leading to higher fitness for crosses performed at greater distances. Proximity-dependent fitness has been shown in a wide variety of plants, from trees to herbaceous annuals (e.g., Coles and Fowler, 1976
; Price and Waser, 1979
; Levin, 1984
; Redmond et al., 1989
; Waser and Price, 1989
; Dudash, 1990
; Fenster, 1991
; McCall et al., 1991
; Trame et al., 1995
; Fischer and Matthies, 1997
; Byers, 1998
; Stacy, 2001
). These empirical studies have clearly shown that the identity of an individual's mates can affect the fitness of the resulting offspring.
The purpose of the present study was to examine whether biparental inbreeding depression can explain a phenomenon seen in some gynodioecious species: cross-pollinated offspring from females often have higher fitness than cross-pollinated seeds from hermaphrodites, even though the seeds from the two sexes are equally well provisioned (Schrader, 1986
; Shykoff, 1988
; Ashman, 1992
; Delph and Mutikainen, 2003
). For example, in Silene acaulis, Shykoff (1988)
cross-pollinated both sexes using pollen donors growing within 1–10 m of the focal plants (which reflected bumble bee visitation patterns). She found that the survival of seeds from hermaphrodite seed parents was significantly lower than that of seeds from female seed parents when grown in the greenhouse. Moreover, this phenomenon was recently documented again in experiments on plants from the same site (Delph and Mutikainen, 2003
).
In this study I tested whether the sex-differential offspring survival seen in S. acaulis was caused by biparental inbreeding depression. Specifically, I investigated the hypothesis that hermaphrodites are mating with more closely related individuals than are females when mated with nearby plants and that this higher level of biparental inbreeding corresponds with higher inbreeding depression. Several factors contribute to the plausibility of greater biparental inbreeding for hermaphrodites: (1) adults of S. acaulis are slightly inbred and spatial autocorrelation analysis suggests that relatedness falls off with distance as a consequence of passive seed dispersal (Gehring and Delph, 1999
), (2) offspring are likely to be the same sex as their seed parent because sex inheritance is nuclear-cytoplasmic (such that females segregate more female offspring than do hermaphrodites and vice versa [unpublished data]), and (3) females cannot mate with their female relatives, whereas hermaphrodites can mate with all of their relatives as well as themselves.
Two experiments were performed to test the biparental inbreeding hypothesis and evaluate the fitness consequences of inbreeding. In the first, individuals were crossed with pollen donors from varying distances and the fitness of the resulting seeds was measured. The hypothesis that sex-differential seedling survival is influenced by biparental inbreeding depression would be supported if I observed proximity-dependent fitness, at least for the hermaphrodites, such that the sex-differential offspring survival was greatest at the lower crossing distances. In the second experiment I examined the effect of different levels of inbreeding on offspring fitness. Previous studies of this sort on hermaphroditic species have found that fitness declines linearly with relatedness (Willis, 1993
; Hauser and Loeschcke, 1995
; Mayer et al., 1996
), but no such study has been performed on a gynodioecious species. Comparisons of fitness from this latter experiment with those from the first experiment allowed for an interpretation of how relatedness varies in space and whether it is sufficiently high to create observable biparental inbreeding depression. Hence, this study combines knowledge of population structure with proximity-dependent fitness and experimentally inbred matings to determine whether mating with nearby relatives reduces fitness.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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30%) and hermaphrodites (Delph et al., 1999
). The hermaphrodites are fully self-compatible and their flowers are protandrous. Flowering occurs from June through August and the primary pollinator is Bombus sylvicola. Seeds are passivly dispersed and are likely to fall relatively close to the seed parent. Evidence suggests that sex determination is nuclear-cytoplasmic with dominant restorers (Delph and Mutikainen, 2003
), as has been found for other species of gynodioecious Silene (Charlesworth and Laporte, 1998
).
Crossing-by-distance experiment
Hand pollinations were performed during the summer of 1996, on plants growing in the natural population on Pennsylvania Mountain, at the Slope 2 site used by Gehring and Delph (1999)
and by Shykoff (1988
, 1992
). This site is on the southeastern flank of the mountain at an altitude of 3680 m asl. Based on allozyme genotypes, Gehring and Delph (1999)
found an inbreeding coefficient of 0.084 for adults in this site, which, while low, is significantly greater than zero. Fifteen hermaphrodites and 15 female plants were haphazardly chosen as seed parents for this experiment. Pollen donors from seven different distances (within concentric circles) to these target plants were used for the experimental crosses: 0.5, 1, 2, 4, 10, 15, and 20 m. These distances were chosen based on the population structure at this site: allozyme alleles showed significant positive autocorrelation within 1 m, but quickly declined to show little or no autocorrelation with increasing distance (see Fig. 4 in Gehring and Delph, 1999
). Hence, the crossing distances encompassed distances at which plants were likely to be related to each other as well as distances at which plants were unrelated. At least three flowers were pollinated for each of the crossing distances on each of the 30 plants, for a minimum of 21 flowers pollinated per plant, in order to obtain seeds produced from crosses of known distance. Experimental fruit that were damaged by herbivores prior to seed maturation were replaced with new pollinations whenever possible. In addition, 3–5 flowers were self-pollinated by hand (geitonogamously) on each of the 15 hermaphrodites. Moreover, seeds were collected from flowers open to natural pollination for each of the 30 target plants. Overall, a total of 835 flowers were hand-pollinated in the field. One pollen donor was used for each crossing distance for each target plant, for a total of 210 pollen donors (excluding self-pollinations). Pollen donors were chosen based on their distance to the target plants, with the only additional caveats being that they had to be flowering concurrently and have sufficient flowers to complete the pollinations.
Each flower used in the crosses was capped prior to opening with an inverted 1.5 mL-microcentrifuge tube, which was held in place by pushing a straight pin through the cap and into the plant cushion. Previous work had shown that this technique effectively prevented visitation by all potential pollinators and did not adversely affect fruit set (personal observation). Once the flowers opened they were treated as follows. The anthers were removed on hermaphrodites to prevent self-pollination. Removal of all anthers typically took 2 d, because the flowers contain two sets of anthers that usually mature on successive days. Pollinations of flowers were performed by directly brushing freshly dehisced anthers across the ends of elongated, receptive styles. Following pollination, the caps were replaced and then subsequently removed after the styles had shriveled. Individual flowers were identified by placing a small ring of plastic-coated wire around the base of the pedicel. Seeds were collected only after the ripe fruit had split open to disperse seeds, thereby ensuring that the seeds were fully mature when collected.
Seeds were planted on 25–26 February 1997 in a greenhouse at Indiana University in order to follow germination, death, and the growth of seedlings over a 2-mo period. Ideally, I wanted to use 15 seeds per plant per treatment, which would have resulted in a total of 3825 seeds over 255 plant by treatment combinations, but the actual number was reduced to 3631 seeds over 250 combinations because of insufficient seeds from some crosses. Each seed used in the experiment was individually weighed using a balance accurate to 1 µg and then placed in a labeled microcentrifuge tube. Seeds were planted in 196-cell plastic trays filled with soil. A light depression was made in the center of each cell, to which one seed was added. Mixing all the marked tubes containing the experimental seeds in a box and haphazardly drawing them out for planting randomized the placement of seeds in the trays. The identity of the seed in each cell was recorded and each of the 19 trays was labeled. The planting trays were placed in watertight steel trays to soak up water from below beginning on 26 February 1997, which was considered "Day 0" for subsequent germination timing. Following 2 d of soaking, the trays containing the seeds were removed from the steel trays and were watered from above using a mist nozzle at regular intervals to keep the soil moist. Trays were positioned on three greenhouse benches, and the position of each tray was randomly changed daily for 1 mo and every other day thereafter. High-intensity lights provided supplemental light for 14 h/d.
Seeds were checked daily for germination and/or death and these data were recorded. Germination was defined as being when the cotyledons had emerged from the seed coat, as it was not always possible to view the emerging radical. Each seedling was allowed to grow for 63 d following its germination, after which it was cut off at soil level, placed in a labeled coin envelope, dried in an oven at 60°C for at least 7 d, and subsequently weighed.
Relatedness experiment
In order to estimate inbreeding depression following crosses between individuals of different known relatedness, shoots were taken from several plants growing in the Pennsylvania Mountain population used for the above experiment, whose relative spatial position in the population had been mapped. These shoots were rooted and allowed to grow into mature, flowering plants in a greenhouse at Indiana University; these plants were the "grandparental" generation. Once these grandparents were flowering, their flowers were hand-pollinated as above, using pollen from donors whose "original" positions in the population were at least 20 m from the plant receiving the pollen to avoid biparental inbreeding. Crosses were made with at least two pollen donors per seed parent to produce both full-sibling and half-sibling families. The resulting seeds were then grown to flowering in a greenhouse; these plants were the "parental" generation. Note that all parents were produced by outcrossing and therefore should have minimal variation in their inbreeding coefficients (which should be zero or very low). These parents were hand pollinated to produce offspring that varied in their relatedness. Hermaphrodite seed-parents were geitonogamously selfed to produce inbred seed. In addition, both hermaphrodite and female seed-parents were crossed to each of three different pollen donors: a full-sibling, a half-sibling, or an unrelated individual (neither of whose grandparents was growing close to the seed-parent's grandparents in the natural population). These sets of crosses produced seed that belonged to one of four relatedness cross types: selfed (F = 0.5), crosses between full-sibs (F = 0.25), crosses between half-sibs (F = 0.125), or outcrossed (F = 0). Ten female and 18 hermaphrodite parents were crossed in this way to produce approximately 25 seeds of each cross type per seed parent. Seeds were collected when ripe.
Seeds were planted on 24–25 September 1998 in a greenhouse at Indiana University in order to follow germination and death. From 23 to 25 seeds from each parent and cross-type combination were weighed (a total of 2505 seeds), placed in labeled microcentrifuge tubes, and planted as above in the crossing-by-distance experiment. Observations of germination and death were made daily, as above, from planting until 63 d after germination for each seed (up to 22 December 1998). This allowed for direct comparisons with the above experiment, in terms of looking at how inbreeding affected death in the early seedling stage. Thereafter, each seedling was followed for an additional 3 mo, and new deaths were recorded. These latter deaths were included in calculations of relative fitness for the various inbred treatments. Relative fitness was a multiplicative fitness measure that took into account whether or not a seed germinated and whether each seedling was still alive up to 5 mo post-planting; it was calculated by dividing the mean multiplicative fitness of each inbred treatment by the mean multiplicative fitness of the outcross treatment for each seed parent.
Statistical analysis of the crossing-by-distance experiment
Statistical analyses were performed using SPSS 10.0 for Macintosh computers (SPSS, 1999
). Means per plant (i.e., seed parent) for each treatment were used in the analyses to avoid pseudoreplication (i.e., analyses were not done on a seed-by-seed basis). Data on the percentage of seeds germinating and surviving were arcsine (square-root) transformed prior to analysis, and data shown in the figures for these analyses are back-transformed means. Seed mass was not found to affect germination or survival of seedlings (data not shown) and was therefore not included in analyses. Analyses of variance were used to analyze the impact of sex (of the seed parent), treatment, seed parent, and the sex-by-treatment interaction on the percentage of seeds that germinated, the percentage of seedlings that survived for 2 mo, and seedling mass after 2 mo of growth. Sex and treatment were considered fixed effects, and seed parent was a random effect nested within sex. There were nine different treatments counting the seven crossing-distance treatments (0.5, 1, 2, 4, 10, 15, and 20 m) and the naturally pollinated and self-pollinated treatments. The selfing treatment was necessarily performed only on hermaphrodites and the naturally pollinated treatment is unlikely to be strictly comparable between hermaphrodites and females, as some of the seeds from this treatment could be the result of self-pollination on hermaphrodites but not on females. Hence, ANOVA models were performed using data from only the seven crossing-distance treatments in order to make things comparable between the sexes. Nevertheless, comparisons between the selfed, naturally pollinated and crossing-distance treatments were considered informative; consequently, comparisons among all treatments were made using Scheffé's a posteriori tests.
Statistical analysis of the relatedness experiment
Statistical analyses of the percentage of seeds that germinated and seedlings that survived for 2 mo and the percentage of individuals still alive 5 mo after planting were identical to those done for the crossing-by-distance experiment, except that treatment in these cases was categorized by known crosses (half-sib crossed, full-sib crossed, and outcrossed) rather than distance. Once again, the ANOVAs were performed without the selfed treatment (with the exception of the two-way ANOVAs described below), and then comparisons among all treatments were made using Scheffé's a posteriori tests.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Relatedness experiment: germination
The mean percentage of seeds germinating per treatment ranged from 82 to 90% (backtransformed means of 85 to 95%, see Fig. 4). Sex did not significantly affect germination (Table 2A): excluding the values for selfed seeds, seeds from hermaphrodites and females both averaged 91% germination. The effect of treatment (i.e., cross type) was marginally significant, but Scheffé's a posteriori test revealed that none of the treatments differed significantly from each other in germination (Fig. 4). The effect of seed parent was significant, however the sex-by-treatment interaction was nonsignificant (Table 2A).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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I know of five additional studies in which crosses at different distances did not significantly affect offspring fitness, although in each of these cases selfing led to significant inbreeding depression (Galen et al., 1985
; Newport, 1989
; Schlicting and Devlin, 1992
; Hauser and Loeschcke, 1994
; Oostermeijer et al., 1995
). Clearly, whether or not crosses at close distances will lead to a reduction in fitness relative to more distant crosses depends on the degree and extent of population structuring. Trame et al. (1995)
explicitly evaluated this relationship in a study of Agave schottii. They found that a genetic analysis of relatedness matched results of inbreeding depression when crosses were made at different distances: individuals close to each other had higher mean genetic similarity than individuals further away and the plants had significantly lower relative fitness when crossed at close distances.
Relatedness
The results of the relatedness experiment allow me to evaluate why no crossing-by-distance effect was found for survival, even though population structure exists at a fine scale. I found that in addition to selfed seeds dying more often than outcrossed seeds, half- and full-sib crosses also led to a significant reduction in survival during the first 2 mo for seeds from hermaphrodite seed-parents but not for those from female seed-parents. These results indicate that the lack of a crossing-by-distance effect is probably a consequence of the degree of relatedness among near-neighboring adults in the population not being high enough to cause significant biparental inbreeding depression in seedling survival as it was measured in this study.
The results of this experiment also suggest why adults are only slightly inbred at the study site (f = 0.084; Gehring and Delph, 1999
), even though hermaphrodites regularly produce selfed seed (mean of 28%; Marr, 1997
). The multiplicative fitness estimates for progeny from both sexes revealed that the relative fitness of inbred seeds in the relatedness experiment was significantly lower than that of outcrossed seeds for all three levels of inbreeding (selfing, full-sib, and half-sib). These inbreeding depression values were obtained from a relatively benign greenhouse habitat and only included measures of fitness up to 5 mo after planting and are therefore likely to be an underestimate of what inbreeding depression is in the field. Note also that death is relatively high in the field during the first few years even for seedlings that become established enough to produce a shoot, at least at the site used in this study (unpublished data). Hence, it seems probable that seeds that are the product of either selfing or a cross between related individuals are unlikely to become established adults in the harsh alpine environment. In other words, uniparental and biparental inbreeding depression is sufficiently high that the coefficient of inbreeding for the established adults is kept fairly low.
Sex-differential survival
The sex-differential seedling survivorship that has been reported previously (Skykoff, 1998; Delph and Mutikainen, 2003
) and which was the focus of the present study was once again seen: seedlings from hermaphrodite seed-parents survived less well than those from female seed-parents in the crossing-by-distance experiment. Delph et al. (1999)
showed that differential seed provisioning is not the cause of this phenomenon. For each of the eight seed-provisioning traits they measured, seeds from females were either equally or slightly less well provisioned than those from hermaphrodites, which negates the possibility of small but nonsignificant differences adding up to better provisioning of seeds from females. Moreover, Delph and Mutikainen (2003)
falsified two additional hypotheses to explain the sex-differential survival phenomenon. They showed that the cytotype of an individual did not affect its probability of survival, so even though hermaphrodites and females may differ in their cytotype frequencies in the population, this doesn't account for the greater death of seeds from hermaphrodites. They also showed that the degree of gametophytic selection, which could differ between longer-styled pistillate flowers and shorter-styled perfect flowers, was not responsible for the survival differences. Similarly, the results of the present study refute the biparental inbreeding hypothesis as a mechanism. Nonetheless, this study is the third one to find that seedlings from hermaphrodites die more often than those from females, indicating that this is a highly repeatable phenomenon.
One mechanism that has not been eliminated as a plausible explanation for this phenomenon involves a cost of restoration. Under this hypothesis, the alleles that restore male-fertility and make an individual hermaphroditic cause negative pleiotropic effects. Theoretical models have shown that such costs are required for the maintenance of the polymorphism that leads to nuclear-cytoplasmic gynodioecy (Charlesworth, 1981
; Delannay et al., 1981
; Gouyon and Couvet, 1985
; Frank, 1989
; Gouyon et al., 1991
; Bailey et al., 2003
). Moreover, the polymorphism can be maintained regardless of whether the cost of restoration occurs only when a mismatch exists between the restorer and the male-sterility gene, only when the restorer is correctly matched with a male-sterility gene it can restore, or when it is constitutive and occurs independently of the match (see Bailey et al., 2003
). The higher percentage of seedling death from seeds from hermaphrodites relative to those from females in the crossing-by-distance experiment support the negative pleiotropy hypothesis and lend credence to the existence of a cost of restoration.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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