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Brief Communication |
2Institute of Arctic Biology and Department of Biology and Wildlife, University of Alaska, Fairbanks, Alaska 99775 USA; 3Department of Biology, Norwegian University of Science and Technology, N-7491 Trondheim, Norway; 4School of Biological Sciences, King Henry Building, University of Portsmouth, Portsmouth PO1 2DY, UK
Received for publication August 21, 2003. Accepted for publication June 3, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Dalechampia scandens • Euphorbiaceae • genetic load • inbreeding depression • male gametophyte • mating-system evolution • pollen competition
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Marshall and Ellstrand, 1986
; Mulcahy and Mulcahy, 1987
; Winsor et al., 1987
; Quesada et al., 1993
; see reviews in Willson, 1994
; Skogsmyr and Lankinen, 2002
). Thus, floral features that might promote intense competition between pollen grains (e.g., attracting pollinators delivering large, genetically diverse pollen loads, long styles allowing long "races" between tubes, circular or spherical stigmas concentrating pollen at the same starting point, and reduced number of ovules relative to numbers of arriving pollen) have been interpreted as potential adaptations that allow females to improve the mean fitness of their offspring by selecting superior diploid fathers for them (Mulcahy, 1983
).
Although Mulcahy's seminal paper (Mulcahy, 1979
) and later review (Mulcahy and Mulcahy, 1987
) discussed the role of pollen competition in potentially selecting superior haploid (gametophyte) genotypes for fertilization, the ecological context of these considerations has been one of cross-pollination. Yet as a simple extension, we could also expect that pollen competition might influence the average quality of the gametophytes fathering offspring, and hence influence offspring fitness, under scenarios of biparental inbreeding or self-fertilization. Because some 60% or more of the genome is thought to be expressed in the male gametophyte stage (e.g., Ottaviano et al., 1982
), there is potential for screening additive or nonadditive genetic variance during pollen competition. In particular, we suspect that genetic load hidden as recessive alleles in the diploid phase might be expressed and purged in the haploid phase.
Charlesworth and Charlesworth (1992)
linked the concepts of pollen competition, genetic load, and inbreeding depression to show, theoretically, that intense pollen competition is unlikely to increase offspring fitness more than slightly. Since they concluded that pollen competition was unlikely to be of evolutionary significance, they did not develop the interconnection between these concepts further. Subsequent empirical work, however, has indicated that pollen competition does often affect offspring fitness significantly (Winsor et al., 1987
; Quesada et al., 1993
; Snow and Spira, 1996
; Johannsson and Stephenson, 1997
; Skogsmyr and Lankinen, 2000
) and that pollen-tube growth rates indeed show heritable variation (Schlichting et al., 1990
; Quesada et al., 1996
; Skogsmyr and Lankinen, 2000
). Hence pollen competition may be of considerable evolutionary importance. Recent research suggests also that intermittent self-fertilization probably occurs more widely than previously thought (Vogler and Kalisz, 2001
).
It seems therefore appropriate to reexamine the potential effects of pollen competition under conditions of inbreeding. Here we suggest that pollen competition may have important consequences in reducing the cost of inbreeding through reduction of the genetic load of additive or, more likely, recessive deleterious alleles prior to fertilization (mitigation of inbreeding depression under the partial-dominance model; see Roff, 2002
). We suspect these effects are especially important in plants with mixed mating systems and populations experiencing variable pollination environments; both conditions now appear to be common.
One major doubt about the evolutionary significance of pollen competition in natural plant systems derives from the expectation that selection for fast-growing tubes should be so strong that, if there is genetic variation for the trait, fast tubes should be rapidly fixed in the population. Variance in pollen-tube growth rates would therefore be of environmental origin (hence not of evolutionary significance) or reflect recent mutation and be extremely limited (Charlesworth and Charlesworth, 1992
; Walsh and Charlesworth, 1992
). However, fixation of rapid tube growth may be prevented in populations of outcrossing plants that experience frequent pollen limitation, significant variation in intensity of pollen competition, or gene flow among subpopulations with conflicting selective pressures (Schlichting et al., 1990
; Wilson et al., 1994
; Delph et al., 1997
; Lankinen and Skogsmyr, 2001
). Indeed, Herrera's (2002
, 2003
) recent studies of male-gametophyte distributions across stigmas within and among populations of a number of species demonstrate just how variable pollen competition can be: it can range from few grains experiencing no competition to many grains experiencing intense competition across flowers on the same plant, as well as among plants and among years. Genetic variation in pollen-tube growth rates may also be maintained by other factors affecting the intensity of pollen competition, including the position of pollen grains on the stigma and the length that pollen tubes must grow to reach the ovules (e.g., Mulcahy and Mulcahy, 1975
; Armbruster et al., 1995
) and variation in the time of pollen arrival (Snow 1986
; Thomson, 1989
; Spira et al., 1996
).
It is generally thought that outcrossing allows the maintenance of recessive deleterious alleles, whereas frequent inbreeding leads to the purging of recessive deleterious alleles. Thus we might expect most populations to be either outcrossing and experiencing strong (if rare) inbreeding depression, or selfing and experiencing little or no inbreeding depression. Intermediate ("mixed") mating systems would be very rare (Lande and Schemske, 1985
; Schemske and Lande, 1985
). It follows, then, that populations would rarely experience inbreeding depression in the wild either because populations with genetic loads rarely experience much inbreeding or because they contain few recessive deleterious alleles. Thus there would be relatively little opportunity for selection for traits that mitigate inbreeding depression.
Recent studies, however, indicate that a large proportion of plant populations probably have mixed mating systems (Vogler and Kalisz, 2001
), leading to the possibility that many populations self fairly often yet still have sufficient genetic load to experience inbreeding depression. We may therefore expect plants with mixed mating systems to experience periodic inbreeding depression and thus be subject to periodic selection for traits that mitigate such effects.
The commonness of spatial and temporal variability in pollination intensities (Bierzychudeck, 1981
; Snow, 1982
; Burd, 1994
; Wilson et al., 1994
; Herrera, 2002
, 2003
) and the apparent commonness of mixed mating systems (Vogler and Kalisz, 2001
) thus argue for the potential importance of selection for features promoting competition even among self-pollen. If this scenario is correct, pollen competition could have important consequences for plant fitness even when interactions among, or female choice between, different sporophytic father genotypes does not occur. Specifically we suggest that pollen competition might ameliorate inbreeding depression, not by influencing inbreeding rates, but rather by reducing the number of recessive deleterious alleles that are involved in fertilization.
The hypothesis that floral traits promoting pollen competition evolved, in part, as adaptations to mitigate inbreeding depression leads to several predictions, the simplest being that offspring produced through selfing with more intense pollen competition should have higher fitness than offspring produced through selfing with less intense pollen competition, at least in plants with mixed mating systems. Here we present the results of an experiment that tests this prediction.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Webster and Armbruster, 1991
). It has unisexual flowers borne in pseudanthial inflorescences that act ecologically as bisexual blossoms (Webster and Webster, 1972
). Pistillate flowers are three per blossom, each containing three ovules and producing up to three seeds. Pistillate flowers have long styles with large stigmatic surfaces extending from the style tip to about two-thirds of the way to the style base (Armbruster et al., 1995
). This large stigmatic area probably increases total pollen arrival rates by increasing pollinator attraction (higher total fragrance production by stigmatic tissues) and/or increasing the target area for pollen landing on stigmas, although at the cost of decreased "fairness" in the pollen-tube race to the stigmas (some grains, by chance, being much closer to the ovules; Armbruster, 1996
). This "cost" is reduced somewhat by those pollen grains landing on the side of the style being forced to grow their tubes backwards to the stylar tip before being "allowed" to proceed to the ovules. This may be a compensatory adaptation reducing the proportional random variation in the length tubes grow to the ovules (Armbruster et al., 1995
). Additional details on the dynamics of pollen-tube growth are presented in Armbruster et al. (1995)
.
Although self-compatible, the blossoms secrete a terpenoid resin reward that attracts resin-collecting bees, usually resulting in considerable outcrossing in nature (Armbruster, 1985
). In the absence of pollinators, however, flowers set seed readily through functional autogamy (within-blossom geitonogamy; Armbruster, 1988
, 1993
). It is not known if D. scandens experiences inbreeding depression in the wild, but it seems likely given the intermediate and highly variable outcrossing rates.
Experiments
Four genetic individuals of Dalechampia scandens (Euphorbiaceae) were planted and grown under identical greenhouse conditions. Upon flowering, geitonogamous pollinations (pollination between flowers on the same plant, hence self-fertilization) were conducted on emasculated blossoms. An equivalent aliquot of pollen was placed on each style by touching the tip of a toothpick to an open, first-day staminate flower on the same plant. This resulted in placing an average of 209 pollen grains per stigma (1 SD = 49; N [for estimate] = 10). We manipulated the intensity of pollen competition without changing pollen number, which allowed assessment of the effect of pure competition rather than "genetic sampling" (i.e., chance sampling of superior gametophytes with application of more pollen; see Paschke et al., 2002
; Bernasconi et al., 2003
). This was accomplished by taking advantage of the elongated stigmatic surfaces of D. scandens flowers to place pollen loads in either a narrow band on the lateral surface of the stigma (low pollen dispersion [positional variance] and more-intense pollen competition) or spread widely and evenly along the lateral surface of the stigma (high pollen dispersion and less-intense pollen competition). Our assumption that high variance in pollen position on the stigma decreased the intensity of pollen competition (if there is any) was based on the knowledge that any increase in the random component of variance in which pollen grain succeeds in fertilization (e.g., a pollen grain that is successful only because its tube, by accident of pollen arrival site, needs to grow a shorter distance to reach the ovules) necessarily decreases any systematic components of variance (e.g., faster tubes reflecting superior genotypes).
A total of 102 pistillate flowers in 34 blossom inflorescences were pollinated, with the experimental unit being the blossom inflorescence (N = 34), each containing three pistillate flowers, each of these with up to three seeds. Statistical analyses were based on the mean seed mass of the 1–9 seeds produced by each blossom (we did not consider flowers within a blossom to be independent). Mature seeds were captured in mesh bags (the fruits are explosively dehiscent capsules), harvested, and weighed. Seed mass was used as a measure of offspring fitness, with maternal effects estimated and "removed" statistically in the analysis of variance (ANOVA; see Byers and Waller, 1999
). Seeds from each blossom were weighed and the blossom mean calculated. These means were then categorized by maternal parent, date of pollination, and treatment, and analyzed using factorial ANOVA, with maternal parent, pollination date, and experimental treatment as factors. Variance components were estimated with the SAS maximum-likelihood procedure for unbalanced designs, with type-III sums of squares used for hypothesis testing (SAS Institute, 1990
). While measures of inbreeding depression in later life history stages would have been desirable, at least for comparison, there is good biological justification for focusing on early stages. The effects of deleterious genes that are most likely to be purged through pollen competition (and inbreeding) are generally expressed in early life history stages (Husband and Schemske, 1996
).
To check the appropriateness of seed mass as a metric of offspring fitness, in a separate experiment (using a larger number of seeds from the same plants) we used logistic regression to examine the relationship between seed mass and probability of germination and seedling survival to 3 wk (after cotyledon expansion). Heavier seeds were more likely to germinate (Wald 
2 = 77.14, P < 0.0001, N = 413) and produce seedlings that survive to 3 wk (Wald 2 = 34.44, P < 0.0001, N = 170; maternal/block effects were not significant and dropped). We tested also for potential tradeoffs between seed mass and seed number in each blossom, but found no evidence for such a relationship (r = 0.135, P = 0.357, N = 45; maternal/block effects were not significant and dropped).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2 = 0.049, P = 0.825). The mass per seed, however, was significantly greater when pollen was applied to stigmas in the configuration of low pollen dispersion (resulting in more-intense, potential pollen competition) than when applied in the configuration of high pollen dispersion (resulting in less intense, potential pollen competition; P = 0.021; Table 1). The mean seed mass produced with low pollen dispersion was 0.0169 g (1 SE = 0.009), and with high pollen dispersion it was 0.0146 g (1 SE = 0.007). Maternal environmental and/or maternal genetic effects were also important, as is to be expected when measuring fitness components early in the offspring life cycle (P = 0.004; Table 1). There was also a marginally significant effect of pollination date (P = 0.055; Table 1).
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2 = 2.749, P = 0.097; trend in predicted direction), the mean growth rate of the radicle did differ significantly between pollen-dispersion treatments (F1,24 = 4.75, P = 0.04; maternal/block and date effects were not significant and dropped). Seeds produced from low-dispersion pollinations showed faster radicle growth rates (0.0235 cm/h) than seeds from high-dispersion pollinations (0.0179 cm/h). |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Thus, the present experiment should be regarded as a preliminary test of our hypothesis. In addition to the above ambiguities, we examined only a limited number of genotypes from only one population of one species. We were also unable to assess late components of offspring fitness, in part because these plants are quite long lived. These caveats notwithstanding, our results suggest that further inquiry into the inbreeding-mitigation hypothesis is warranted.
Although the evolutionary significance of pollen competition has been questioned on a number of grounds (Charlesworth and Charlesworth, 1992
; Walsh and Charlesworth, 1992
), accumulating data seem to support its importance in plant evolution (Winsor et al., 1987
; Schlichting et al., 1990
; Quesada et al., 1993
, 1996
; Snow and Spira, 1996
; Johannsson and Stephenson, 1997
; Skogsmyr and Lankinen, 2000
). In this context, pollen competition has been considered to be a mechanism promoting maternal "choice" and/or competition among diploid (sporophyte) fathers. However, because plants with mixed mating systems often do have significant genetic loads and experience inbreeding depression (e.g., Johnston and Schoen, 1996
; Newman and Pilson, 1997
; Chang and Rausher, 1999
; Kephart et al., 1999
; Routley et al., 1999
; Carlson, 2002
; also see review in Husband and Schemske, 1996
), we expect that pollen competition may also commonly play a role in the mitigation of inbreeding depression.
This study is, to our knowledge, the first to examine the role of pollen dispersion (spatial variance) on the stigmas as a factor affecting the intensity of pollen competition and offspring fitness (but see related studies of the elongated stigmas in Dianthus by Mulcahy and Mulcahy [1975]
and McKenna and Mulcahy [1983]
and in Silene by Purrington [1993]
and Lassere et al. [1996]
). Spatial variance is, however, directly analogous to temporal variance in pollen arrival, which has received more attention (e.g., Snow, 1986
; Thomson, 1989
; Spira et al., 1996
), and both clearly affect the "fairness" and intensity of pollen competition. In the analysis of sources of variation that may contribute to the maintenance of genetic variation in pollen-tube growth rates (e.g., Lankinen and Skogsmyr, 2001
), dispersion of pollen on the stigmas can be seen to be important in those plant species that, like Dalechampia and many Caryophyllaceae, have elongated stigmatic surfaces. Indeed, elongated stigmatic surfaces (relative to equidimensional ones of the same area) must have evolved for reasons not related to pollen competition, because they must usually reduce the positive effects of pollen competition by introducing positional variance (which may explain why elongated stigmas are relatively rare), depending on the relationship between stigma shape, stigma size, number of arriving pollen, and the variance in position (see Armbruster et al., 1995
; Armbruster, 1996
).
The zoological literature contains an interesting parallel to our hypothesis that pollen competition might reduce inbreeding depression by purging deleterious alleles. Some authors have used similar reasoning to suggest that the haplodiploid sex-determination system might reduce inbreeding depression in invertebrates. The argument is that, under partial dominance, inbreeding depression should be low in haplodiploids (e.g., Hymenoptera), because most of the recessive genetic load should be expressed, and hence purged, in the haploid males (Bruckner, 1978
; Werren, 1993
; Antolin, 1999
). Available data largely support this idea, although ambiguities remain (see Henter, 2003
).
Several previous studies have addressed the related issue of gamete competition reducing biparental inbreeding depression. Inbreeding may be reduced or completely eliminated by females mating with multiple fathers (leading to sperm competition) in crickets (Tregenza and Wedell, 2002
) and in plants (Paschke et al., 2002
; see also discussion in Walsh and Charlesworth, 1992
). The results of these studies suggest that sperm or pollen compete, or are in some way screened by the mother, so that genetically compatible sperm perform most fertilizations. However, these studies involved matings with several different individuals of varying genetic relatedness, rather than self-fertilization, so the gametes may be screened by relatedness to the mother instead of through expression of deleterious alleles. Hence the evolutionary dynamics are likely to be quite different from the processes described here.
Interestingly, one recently published study appears to provide additional data that directly support our hypothesis that screening of self pollen during tube growth enhances offspring fitness. Kephart (2004
; S. Kephart, Willamette University, personal communication) found that the progeny of hand self-pollinations of Silene douglasii var. oraria (Caryophyllaceae) showed significantly higher fitness for many traits than did the progeny of open-pollinated plants (which also received mostly self-pollen, but with much lower pollen loads on the stigmas). This would appear to be a consequence of greater pollen competition preventing pollen with expressed deleterious alleles from fertilizing ovules in the hand-pollination treatment (S. Kephart, Willamette University, personal communication).
The results of the present study suggest an unappreciated methodological complication in studies of inbreeding depression in plants. If pollen competition moderates the effects of inbreeding depression, as our results suggest, then studies of inbreeding depression ought to control for the intensity of pollen competition. For example, heavy pollinations, causing high pollen competition, may lead to underestimating inbreeding depression, relative to low-intensity pollinations. Thus, variation in pollination intensity could introduce large amounts of variance in estimates of inbreeding depression. Because most experiments on inbreeding depression usually do not (apparently) tightly control pollination intensity (see Stone and Motten [2002]
and references cited therein), inconsistencies among studies (see reviews in Byers and Waller, 1999
; Stone and Motten, 2002
), and results inconsistent with (e.g., Mayer et al., 1996
), or only weakly consistent with (e.g., Husband and Schemske, 1996
), expected trends could be artifacts of within- and among-experiment variation in intensity of pollen competition (see Byers and Waller, 1999
).
We suggest that the potential connection between pollen competition and the costs of inbreeding thus deserves further exploration, both theoretically and empirically. Two additional, untested predictions emerge from our hypothesis: (1) as implied above, estimates of inbreeding depression should be lower in experiments involving more intense pollen competition than in experiments with less-intense pollen competition; and (2) beneficial effects of pollen competition on fitness of offspring produced by self-pollination should be more pronounced in highly outcrossed (but self-compatible) populations than in highly inbred populations. Preliminary results from a parallel ongoing study of inbreeding depression in Collinsia (Plantaginaceae; A. Lankinen and W. S. Armbruster, unpublished data) indicate that estimates of inbreeding depression are indeed affected by the amount of pollen used in the experiment. There remains a compelling need to test the three predictions of the inbreeding-mitigation hypothesis across a broad sample of species.
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FOOTNOTES |
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5 Reprint requests: School of Biological Sciences, King Henry Building, University of Portsmouth, Portsmouth PO1 2DY, UK (E-mail: scott.armbruster{at}port.ac.uk
)
6 Current address: P.O. Box 146, Burke, New York 12917 USA (E-mail: sweetcicely1{at}netscape.net
)
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