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Reproductive Biology |
2Department of Biology, 208 Mueller Lab, The Pennsylvania State University, University Park, Pennsylvania 16802 USA; 3Department of Biology, The Pennsylvania State University, Altoona, Pennsylvania 16601 USA
Received for publication December 17, 2003. Accepted for publication September 2, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Cucurbita • female function • inbreeding depression • male function • pollen
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Because each plant donates two sets of chromosomes to selfed seeds and only one set to outcrossed seeds, alleles that increase the selfing rate will increase in frequency unless the magnitude of inbreeding depression is severe enough to overcome the transmission advantage of selfing (Fisher, 1941
). In the absence of pollen discounting, biparental inbreeding, and fitness effects due to genetic associations among loci, complete outcrossing should evolve when selfed progeny are less than one-half as fit as outcross progeny (ID > 0.5), but complete selfing should occur under less severe inbreeding depression (Lloyd, 1979
; Charlesworth and Charlesworth, 1987
, 1990
).
Predictions on the evolutionary dynamics of a population, therefore, depend on accurate measures of inbreeding depression. Many studies have estimated the strength of inbreeding depression in a variety of plants, but until recently most studies have concentrated on the effect of inbreeding on female function (see Charlesworth and Charlesworth, 1987
; Uyenoyama et al., 1993
; Husband and Schemske, 1996
) but ignored the effect on male function, even though most plants are hermaphrodites (Charnov, 1982
) and contribute, on average, half of their genes through male function. Because fruit and seed set are simpler to measure and represent a larger per-unit resource investment than pollen (Schlessman, 1988
), male function is often overlooked or oversimplified in studies requiring estimates of fitness. Therefore, if male and female functions are differentially affected by inbreeding depression, studies that ignore male function may lead to biased estimates of inbreeding depression.
Fitness through female function depends on such factors as pistillate flower number, pollinator attraction and pollen deposition, fruit set, ovule number, and seed set. More fruits and seeds are initiated than a plant is typically able to mature, so plants that produce more pistillate flowers or ovules may not produce a larger seed set but may produce higher quality offspring through nonrandom fruit and seed abortion (Stephenson et al., 1986
; Winsor et al., 1987
; Stephenson et al., 1988
). Many studies have shown that inbreeding reduces the quality and survivorship of seeds, and several studies have shown that inbreeding also reduces the number of pistillate flowers, fruits, and seeds per fruit (see reviews by Charlesworth and Charlesworth, 1987
; Husband and Schemske, 1996
; Byers and Waller, 1999
). Because pistillate flowers, fruits, and seeds are generally expensive to produce relative to staminate flowers and pollen (Lloyd and Webb, 1997
), the loss of vigor associated with inbreeding depression tends to reduce fitness through female function.
Fitness through male function depends on the probability of siring success, which is influenced by factors such as staminate flower number, pollen quantity per flower (but see Ashman, 1998
), pollen dispersal, pollen germination rate and viability, pollen–pistil interactions, and pollen tube growth rate (see Stephenson et al., 1992
). The number of staminate flowers influences both the quantity of pollen produced as well as the probability of visitation and pollen removal by pollinators (Devlin et al., 1992
). The quantity of pollen produced per flower influences the amount of pollen removed during a single pollinator visit and ultimately the amount of pollen deposited on a stigma. Following pollen germination on a stigma, pollen tube growth rates depend upon resources stored within the pollen grain, the genotype of the pollen, pollen–pistil interactions, and perhaps pollen–pollen interactions and pollen–megagametophyte interactions (Stephenson et al., 1992
; Taylor and Hepler, 1997
; de Graaf, 2001
). Factors that slightly reduce the speed of germination or the growth rate of pollen may therefore reduce siring success, especially under conditions of pollen competition (Stephenson et al., 1992
; Delph et al., 1997
).
Only a few recent studies have examined the effect of inbreeding on some aspect of pollen production and siring ability. Jóhannsson et al. (1998)
and Chang and Rausher (1999)
found that inbreeding reduced the number of staminate flowers produced in Cucurbita pepo L. subsp. texana (A. Gray) Filov (Cucurbitaceae) (Lira et al., 1995
) and Ipomoea purpurea (L.) Roth (Convolvulaceae), respectively, and Carr and Dudash (1995
, 1997
) found that inbred plants produced fewer pollen grains per flower than outcrossed plants in Mimulus guttatus DC. (Scrophulariaceae). Several studies have found reduced stainability (viability) of pollen produced by inbred plants (Willis, 1993
; Mayer et al., 1996
) or a reduced frequency of normal pollen grains (del Castillo, 1998
). Melser et al. (1999)
showed that pollen from inbred plants is less viable, has a slower growth rate, and demonstrates reduced siring success than pollen from outcrossed plants in Echium vulgare L. (Boraginaceae), and Jóhannsson et al. (1998)
showed that pollen from inbred plants grew more slowly in vitro and sired fewer seeds in vivo in competition with a tester line than pollen from outcrossed plants. Inbreeding depression therefore appears to reduce the amount of pollen available for export, pollen viability, and the ability to compete against pollen from outcross plants for access to ovules. Moreover, reductions in flower number associated with inbreeding may also affect pollinator visitation rates.
As different suites of genes are expressed during pollen and ovule/seed/fruit development (Coen and Meyerowitz, 1991
; Meagher, 1992
; Yanofsky, 1995
), there is little a priori reason to expect that the effects of inbreeding on male and female functions should be tightly correlated except insofar as the overall reduction in vigor associated with inbreeding depression. Some studies suggest that male and female reproductive success are correlated with each other as a function of plant size (Broyles and Wyatt, 1993
), but other studies suggest that male and female reproductive success are unrelated or negatively correlated (e.g., Bertin, 1982
; Marshall and Ellstrand, 1986
; Schlichting and Devlin, 1989
). This apparent contradiction is possible if plant size is a good predictor of fitness in general but if male and female fitnesses respond differently to stress and are limited by different conditions. Several studies have shown that environmental factors affect male and female fitness traits differently (Bertin, 1982
; Schlichting and Devlin, 1989
; Devlin and Ellstrand, 1990
), and that fitness estimates based only on female fitness may underestimate the effects of stress treatments (Schlichting, 1986
). Because total fitness is the sum of fitness achieved through the male and female functions, overall inbreeding depression is effectively the average inbreeding depression between male and female functions. Therefore, estimates of total inbreeding depression based only on measurements of female fitness are likely to be biased in unpredictable ways. In many models of the evolution of plant breeding systems, an inbreeding depression value of 0.5 represents an unstable equilibrium between complete selfing and complete outcrossing. It is important, therefore, to accurately measure the magnitude of inbreeding depression.
Only a few studies have directly compared inbreeding depression on male and female functions, and the results are inconsistent. Some studies suggest that the magnitude of inbreeding depression is similar for male and female fitness (Damgaard and Loeschcke, 1994
) in which case inbreeding depression for female function is a good predictor of total inbreeding depression. Other studies, however, suggest that there is little correlation between inbreeding depression for male and female functions. Melser et al. (1999)
found strong inbreeding depression for both male and female components of fitness in Echium vulgare but found no correlation between them. Chang and Rausher (1999)
found that inbreeding depression reduces fitness more for female function than for male function, and del Castillo (1988)
found strong inbreeding depression for female function (seed number) but no detectable inbreeding depression for a male function trait (pollen viability) in Phacelia dubia (L.) Trel. (Hydrophyllaceae). Conversely, studies of Mimulus guttatus (Carr and Dudash, 1995
, 1997
) have found much stronger inbreeding depression for male function (pollen number and viability) than for female function (ovule number and seed number). In these cases, inbreeding depression based only on female fitness would be misleading, and measurement of both is necessary to estimate total inbreeding depression accurately.
In this study, we examine the magnitude of inbreeding depression in both the male and female functions of Cucurbita pepo subsp. texana.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Decker-Walters, 1990
). Only one staminate or pistillate flower is produced per node, and flowers last only for one day. Although it is self-compatible, the existence of separate staminate and pistillate flowers prevents autogamous selfing, and the spatial arrangement of staminate flowers opening on older nodes clustered toward the center of the plant and pistillate flowers opening on younger nodes away from the center of the plant seems to promote outcrossing and reduce the potential for geitenogamous selfing.
Prior to the start of the experiment a random sample of seeds was collected from plants growing in a natural population in Texas, USA. In order to reduce the likelihood of sampling from related plants, seeds were collected from plants spaced no closer than 15 m along a linear transect. Seeds were grown in an experimental garden and plants were outcrossed to produce an initial population of f = 0 plants. We randomly selected five f = 0 progeny to found five maternal families, and reserved the remaining lines to serve as potential pollen donors. Pistillate flower buds were covered with cheesecloth bags prior to anthesis to exclude pollinators, and single-sire hand pollinations were performed following anthesis (Jóhannsson et al., 1998
). In the following growing season, plants were pollinated with both self and outcross pollen, resulting in f = 0.5 and f = 0 progeny, respectively. In the next season, the f = 0 plants were outcrossed (f = 0) and selfed (f = 0.5) again, and the f = 0.5 plants were selfed to produce f = 0.75 plants. Outcross pollen donors were used only once within a family.
In the summer of 2000, 250 f = 0 seeds and 250 f = 0.75 seeds were planted in potting soil at a depth of 1 cm in 10 cm "jiffy" pots and arrayed in a randomized block design in a greenhouse. The experiment was also repeated in the summer of 2001 using 125 f = 0 seeds and 125 f = 0.75 seeds. Equal numbers of seeds from each of five maternal families were used in both years. Time to germination was scored by screening for emergence at 12-h intervals. After most seedlings had one or two leaves, 300 (in 2000) and 100 (in 2001) seedlings were transplanted to an experimental garden at the Pennsylvania State University Agricultural Experimental Station at Rock Springs, Pennsylvania. Plants were sprayed with pesticides at 2-wk intervals to control herbivory. In addition, to estimate vegetative vigor in 2000, 75 f = 0 and 75 f = 0.75 seeds were grown in a greenhouse, and after three weeks, the sum of the petiole lengths of the first three leaves was recorded.
After transplanting, the number of new staminate and pistillate flowers was recorded each day to determine days to first flower and total flower production. Once per week, staminate flower buds were lightly clamped with a twist-tie prior to opening to prevent pollen removal and then were collected at anthesis. Anthers and loose pollen were removed and dried in scintillation vials in a drying oven at 45°C for 2 wk before being rehydrated for 1 d in a 0.5% NaCl solution and then sonicated for 15 min to dislodge pollen from anthers. Pollen number and size were determined using an Elzone EX180 particle counter (Particle Data, Inc., Elmhurst, Illinois, USA).
On three dates in 2000 and two dates in 2001, fresh pollen from each plant was sprinkled onto Brewbaker and Kwack (Brewbaker and Kwack, 1963
) pollen-germination media containing 10% sucrose, allowed to germinate and grow for 30 min, then 2 mL of 70% ethanol was applied to arrest growth. In vitro growth rate of pollen tubes was determined using the mean length of 30 pollen tubes per plate using image analysis (Rich et al., 1989
). When pollen was collected from the same plant on more than one date, the mean pollen tube growth rate was used for analysis.
After the first lethal frost in September in 2000 and 2001, the total number of mature fruits per plant was recorded, and two fruits per plant were collected for seed extraction. Seed count was calculated by dividing the total seed mass by the mass of a random sample of 25 seeds. The mean seed count of the two fruits was used in analysis. Seed viability was measured by planting a sample of 20 seeds per fruit in flats in the greenhouse and recording percentage germination at 3 wk. To estimate overall vegetative vigor, in August 2000 the length of the main stem on each plant was measured.
To account for correlations among characters, multivariate analysis of variance (MANOVA) was used to test for an overall effect of coefficient of inbreeding on female characters when fruits per plant, seeds per fruit, and percentage germination of seeds were analyzed simultaneously. A second MANOVA was used to test for an overall effect of coefficient of inbreeding on male function when staminate flowers per plant, pollen per anther, and in vitro pollen tube growth rate were analyzed simultaneously.
The data were analyzed with Minitab (Minitab, Inc., State College, Pennsylvania, USA) using a general linear model with coefficient of inbreeding as a fixed effect and maternal family and year as random effects. Staminate and pistillate flower numbers and fruit number were transformed using a square-root transformation to meet statistical assumptions. The mean inbreeding depression for each trait was calculated as 1 – ws/wo where ws is the mean value for inbred plants within a family and wo is the mean value for outcrossed plants. A multiplicative estimate of inbreeding depression for female fitness was calculated for each family as 1 – (relative fitnesses for fruits per plant x seeds per fruit x % germination). Similarly, a multiplicative estimate of inbreeding depression for male fitness was calculated as 1 – (relative fitnesses for staminate flower number per plant x pollen per anther x pollen tube growth rate).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; del Castillo, 1998
; Jóhannsson et al., 1998
; Chang and Rausher, 1999
; Melser et al., 1999
). We found significant levels of inbreeding depression for both male and female traits, although inbreeding depression was generally more severe for female traits. No inbreeding depression was found for early vegetative traits, owing perhaps to the relatively benign greenhouse conditions during seed germination and perhaps to purging of early-acting deleterious alleles during the previous round of inbreeding.
Significant levels of inbreeding depression were found for several components of female fitness. Inbred plants matured fewer fruits and produced marginally fewer pistillate flowers. Seed set in open-pollinated fruits did not differ among inbred and outbred plants, but seeds from inbred mothers were significantly less likely to germinate under greenhouse conditions than seeds from outcrossed mothers. Barring geitonogamy or biparental inbreeding, seeds produced from open pollination are likely to be sired by pollen from unrelated plants and should therefore have a coefficient of inbreeding of 0. When f = 0 seeds are produced on inbred mothers, however, the seeds are less likely to germinate, suggesting that inbred mothers fail to provision their seeds as well as an outcrossed mother as a consequence of maternal effects associated with inbreeding depression in the maternal environment (Jóhannsson et al., 1998
; Vogler et al., 1999
).
Unlike most inbreeding studies which use f = 0.5 inbred plants, we used f = 0.75 plants to investigate inbreeding depression when maternal and genetic inbreeding effects are confounded. Maternal effects have been detected for male and female reproductive traits as a result of herbivory, temperature stress, soil fertility, mycorrhizal infection, and patterns of prior fruit set affecting the maternal parent (Roach and Wulff, 1987
; Young and Stanton, 1990
; Stephenson, 1992
; Wolfe, 1993
; Stephenson et al., 1994
; Delph et al., 1997
). Maternal effects have also been found for inbreeding. For example, Vogler et al. (1999)
found that inbred Campanula rapunculoides L. (Campanulaceae) plants produced 40% fewer seeds than outcrossed plants following pollination with the same unrelated pollen donor. Therefore, the genetic effects of inbreeding depression may be compounded by maternal effects when pollinations are performed on inbred mothers (Wolfe, 1993
).
Significant levels of inbreeding depression were also found for several components of male fitness. Inbred plants produced significantly fewer staminate flowers per plant and marginally fewer pollen grains per flower. Several studies have shown that pollinators preferentially forage where floral densities are greatest (e.g., large floral display) (Willson and Price, 1977
; Stephenson, 1979
; Queller, 1983
; Stephenson and Bertin, 1983
; Devlin et al., 1992
). Moreover, given the general decrease in vigor with inbreeding, nectar volume (not measured) could also decrease pollinator visitation and pollen pickup and delivery.
Pollen produced on inbred plants was marginally smaller than pollen produced on outcrossed plants. Because both viable and inviable grains were counted, this may reflect a greater proportion of inviable pollen in inbred plants. The diameter of inviable pollen may be substantially smaller than that of viable grains and the proportion of viable grains tends to decline with inbreeding (Kelly et al., 2002
). Pollen produced on inbred plants also grew significantly more slowly in vitro than pollen produced on outcrossed plants, reducing the probability of siring success. Quesada et al. (1995)
and Jóhannsson and Stephenson (1997)
showed that pollen performance in vitro parallels pollen performance in vivo in C. pepo, and Jóhannsson et al. (1998)
found that pollen from inbred plants sired fewer seeds in vivo than pollen from outcrossed plants. Inbred plants also started flowering later during the season than outcrossed plants, thereby reducing the length of the breeding season.
Though the magnitude of inbreeding depression varies considerably by species and by trait, the results reported here are generally consistent with other studies. The overall level of inbreeding depression is relatively low, however, even though we are using f = 0.75 instead of the more typical f = 0.5. Inbreeding depression for seed set was 0.07, much lower than other reported values: 0.24 (Chang and Rausher, 1999
), 0.48 (Koelewijn, 1998
), and 0.87 (Husband and Schemske, 1995; Vogler et al., 1999
). However, we found elevated values of inbreeding depression for percentage germination of seeds, 0.34, compared to 0.23 (Vogler et al., 1999
) and 0.25 (Husband and Schemske, 1995). We also found higher multiplicative inbreeding depression for female fitness (0.59) than Chang and Rausher (1999)
(0.24).
Few studies report means for male fitness parameters, but of those that do most report moderate levels of inbreeding depression. For a more direct comparison, we selected studies reporting results using f = 0.75. Our estimate of inbreeding for staminate flower production, 0.28, was intermediate in range from 0.07 (Koelewijn, 1998
) to 0.38 (Willis, 1999
), but we found very low inbreeding depression for pollen number, 0.1, compared to 0.62 (Carr and Dudash, 1997
). We did not measure pollen viability, but several studies that did found moderate inbreeding depression, 0.26 (Carr and Dudash, 1997
) and 0.34 (Willis, 1999
), while another found negligible inbreeding depression, 0.1 (Mayer et al., 1996
). Our multiplicative estimate of male fitness (0.43) was also intermediate between Chang and Rausher (1999)
(0.13) and Carr and Dudash (1997)
(0.8). Though highly variable, most reported values of inbreeding depression for components of male function appear to be greater than 0.05 but less than 0.5.
Although spatial and temporal separation of staminate and pistillate flowers in C. pepo subsp. texana (Decker and Wilson, 1987
) reduces the probability of geitonogamous selfing, there is no genetic self-incompatibility system to prevent selfing, and the presence of both staminate and pistillate flowers open on the same day on the same plant suggests the potential for a moderate selfing rate, depending on the number and order of flowers visited during pollination. Selfing serves as a form of reproductive assurance in some species, but the lack of perfect flowers reduces the opportunity for autogamous selfing, and pollinator-mediated selfing offers little reproductive assurance when pollinators are rare or unreliable, although it would still be beneficial for isolated individuals which are limited more by access to conspecifics than by access to pollinators.
In many models of mating system evolution, inbreeding depression is often assumed to principally affect viability and thus influence male and female functions equally. This is likely to be the case for plants that typically outcross and thus accumulate a large genetic load, revealed in the form of strong early-acting inbreeding depression. However, in plants which routinely self, inbreeding is likely to be expressed more strongly for late-acting traits if prior inbreeding has exposed highly deleterious alleles to selection and purging (Husband and Schemske, 1996
). Husband and Schemske (1996)
also concluded from their review of the literature that inbreeding depression is often expressed most strongly during the reproductive phase of the life cycle, especially in partially selfing species.
Plants are often depicted as accumulating resources (nutrients, carbohydrates, and water) and then allocating these resources to growth, maintenance, and reproduction (Charnov, 1982
). Because most plants are hermaphrodites, the resources allocated to reproduction must then be further partitioned between male and female functions. At the population level, fitness through male and female functions must be equal. Individuals, however, often differ in their allocation to the male and female functions which, in turn, may translate into quantitative differences among individuals in their contributions through male and female fitness (e.g., Devlin and Stephenson, 1987; Lloyd, 1987
; Schlichting and Delesalle, 1997
; Thompson et al., 2003
). Resource availability has been shown to affect several components of female fitness including fruit number, seed number, and offspring vigor (Lee, 1988
; Stock et al., 1989
; Stratton, 1989
; Stephenson, 1992
) as well as components of male fitness such as the number of pollen-bearing flowers (Stephenson, 1984
; Stanton et al., 1987
; Vasey et al., 1987
) and pollen production per flower and pollen performance (see Stephenson et al., 1992
, 1994
; Delph et al., 1997
). Because male and female traits may be influenced by different genes (Coen and Meyerowitz, 1991
; Meagher, 1992
; Yanofsky, 1995
) and because some genes are expressed in the pollen but not in the sporophyte (Mascarenhas, 1989
; Ottaviano and Mulcahy, 1989
; Willing et al., 1998
), it seems reasonable to expect that male and female functions will respond in different ways as a result of inbreeding, especially if inbreeding depression constrains the timing or utilization of resources that are required (often on different schedules) for the two sexual functions. In some species, moderate levels of resource deprivation lead to an increase in staminate flower production while reducing resource allocation to the female function (Freeman et al., 1981
). Female function generally requires greater per-unit resource allocation than male function (Lloyd and Webb, 1997
), but in general environmental stress should tend to favor resource allocation to whichever component is less costly, although this may vary depending on which resource is limiting given a particular stress condition. In the case of herbivory, for example, there is little reason to expect equal or proportional responses to herbivory for male and female functions, and the direction is not necessarily consistent (Mutikainen and Delph, 1996
). Therefore, there is little a priori reason to expect that male and female functions will respond to inbreeding in the same way or to the same extent.
Variation among families in response to inbreeding is important in some models for the evolution of mating systems (Uyenoyama, 1993
; Husband and Schemske, 1996
; Dudash et al., 1997
; Vogler et al., 1999
; Willis, 1999
). We found no significant differences among families for male traits, but most showed consistent and significant inbreeding depression across families. Several female traits, however, varied significantly among families indicating that genes responsible for inbreeding depression in female traits are lineage-specific. Most traits showed variation among families in the strength of inbreeding depression, suggesting that different mutations are affecting different traits, as opposed to single genes with pleiotropic effects on fitness. Inbreeding depression for female function was generally higher across families for most traits, though percentage seed germination and staminate flower number showed much stronger inbreeding depression in one family than in the other families. Similarly inbreeding depression for fruit production was nearly twice as high in one family but had typical levels of inbreeding depression for the other traits. Because we only used five families in this study, it is possible that a different set of five families might yield different results.
Differences in the degree of inbreeding depression for male and female function can influence mating system evolution. Rausher and Chang (1999)
proposed a model in which a mixed mating system can be maintained when inbreeding depression is greater than 0.5 for female function but when the total inbreeding depression is less than 0.5. In the present study, we found that C. pepo subsp. texana, a species that has a mixed mating system, has a multiplicative estimate of inbreeding depression above 0.5 for female function but a total inbreeding depression estimate that was also greater than 0.5, slightly too high to maintain a mixed mating system according to this model. Inbreeding depression for most individual traits was found to be less than 0.5, however, so predictions about the evolutionarily stable strategy may be sensitive to the choice of fitness parameters used. Although the magnitude of inbreeding depression differs between male and female function in C. pepo subsp. texana, inbreeding depression does not appear to present a strong barrier to selfing.
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FOOTNOTES |
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4 Corresponding author cnh1{at}psu.edu
. phone: 814-863-6360, fax: 814-865-9131
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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