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Ecology |
Botany Department, University of British Columbia, Vancouver, British Columbia V6T 1Z4 Canada
Received for publication July 5, 2000. Accepted for publication February 8, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Anthonomus melancholicus • breeding system • Curculionidae • gynodioecy • Malvaceae • predispersal seed predator • Sidalcea hendersonii
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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); however, this loss of male function may be compensated either by producing more seeds or higher quality seeds than hermaphrodites (Ashman, 1992
). The level of compensation required for females depends on the genetic control of male sterility. Because cytoplasmic factors are usually maternally inherited, cytoplasmic and cytoplasmic nuclear control of male sterility may result in a higher frequency of male sterile progeny and permit the maintenance of gynodioecy where nuclear control may not (Maurice et al., 1994
). Theoretical models predict that when the inheritance of male sterility is nuclear, females must produce more than twice as much seed as hermaphrodites for male sterility genes to persist, but if maternally inherited cytoplasmic factors are involved, females may require smaller advantages in seed production (Lewis, 1941
; Lloyd, 1974a
; Charlesworth, 1981
; Delannay, Gouyon, and Valdeyron, 1981
; Schultz, 1993
).
Two principal hypotheses have been proposed to explain the maintenance of females in gynodioecious populations. The outcrossing hypothesis proposes that the progeny of females experience higher fitness because female flowers are obligately outcrossed, while the seeds of hermaphrodite flowers may result from self-fertilization and could exhibit inbreeding depression (Lewis, 1941
; Charlesworth and Charlesworth, 1978
; Ganders, 1978
). The outcrossing hypothesis has been extensively tested with population genetics models (e.g., Lewis, 1941
; Ross and Shaw, 1971
; Lloyd, 1974b
; Charlesworth and Charlesworth, 1978
; Charlesworth and Ganders, 1979
; Delannay, Gouyon, and Valdeyron, 1981
; Webb, 1981
; Schultz and Ganders, 1996
). The frequency of females at equilibrium, p, can be estimated by
is the inbreeding depression in the progeny from selfing, and f is the seed production of hermaphrodites relative to females (modified from Charlesworth and Charlesworth, 1978
). From this equation, the frequency of females increases as s and increase or f decreases. Even in the absence of differences in seed production, females may be maintained at equilibrium when selfing and inbreeding are high, i.e., s > 0.5 (Lloyd, 1974b
; Charlesworth and Charlesworth, 1978
; Ganders, 1978
; Schultz and Ganders, 1996
).
The second hypothesis, the resource allocation hypothesis, proposes that maternal genotype and/or maternal environment may be an important source of female advantage (Van Damme and Van Delden, 1984
; Ashman, 1992
). Female plants may allocate more resources to ovules and seed development than hermaphrodites because females do not expend resources on male function. Developmental advantages associated with maternal parentage have been reported for a number of species including Sidalcea oregana ssp. spicata (Ashman, 1992
), Cucurbita foetidissima (Kohn, 1989
), Phacelia linearis (Eckhart, 1992
), and Eritrichum aretioides (Puterbaugh, Wied, and Galen, 1997
). Outcrossing advantages and maternal-sex effects can operate simultaneously or at different stages of the life cycle (Shykoff, 1988
; Ashman, 1992
; Sakai et al., 1997
).
Although many genetic models of the maintenance of male sterility may incorporate ecological parameters (Ross, 1982
), ecological effects are infrequently identified or examined in isolation, perhaps because they are difficult to quantify or separate from genetic factors. Ecological factors can play a significant role in mating system evolution, and in some cases, may even overshadow an initial genetic disposition (Stebbins, 1957
; Jain, 1976
; Barrett and Harder, 1996
). We report here an ecological condition where hermaphrodite plants may experience higher levels of seed predation than female plants and suggest that pest pressure affects the frequency of females in populations of Sidalcea hendersonii.
A few examples of sex-related predation preferences have been reported. Sex-specific leaf-feeding by insects has been observed in the dioecious species Hippohoa rhamnoides and Cannabis sativa (Gatima and Giklova cited in Bawa and Opler, 1978
). Cox (1982)
describes the incidental destruction of male flowers by bats, birds, and rodents seeking pollen, and staminate inflorescences of dioecious Simarouba glauca are considerably more likely than females to sustain feeding damage from moth larvae (Bawa and Opler, 1978
). Also, hermaphrodite plants in a gynodioecious population of Iris douglasiana were shown to experience higher levels of seed predation by moth larvae than females (Uno, 1982
). Anecdotal evidence suggests that pollen/flower eating beetles preferentially attack the hermaphroditic flowers in a gynodioecious population of Tellima grandiflora (Wagner and Miller, 1984
).
The objective of this research was to determine the relative importance of several factors that could contribute to the maintenance of females in populations of Sidalcea hendersonii, specifically: (1) What is the genetic basis of male sterility? (2) What are the effects of inbreeding and maternal parentage on fitness? (3) Do seed predators prey selectively on the seeds of one sex? (4) Is there a positive relationship between the degree of seed destruction in hermaphrodites and the frequency of females in a population?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Pollinator observations during this study indicate that these plants are pollinated primarily by species of Bombus.
Seed predators
Two species of weevils, Macrorhoptus sidalcea Sleeper and Anthonomus melancholicus Dietz (Curculionidae), parasitize the flowers of S. hendersonii in British Columbia and often coexist in host populations. Our collections revealed the presence of Macrorhoptus sidalcea (Fig. 1) in populations of S. hendersonii along the east coast of Vancouver Island and at Delta, British Columbia on the mainland. Mating pairs of M. sidalcea were observed in blossoms of S. hendersonii in June. Female weevils deposit their eggs in immature carpels, and the larvae complete their development in the fruit (a 5–9 seeded schizocarp) prior to seed dispersal. When a seed has been consumed, the larva may tunnel through the lateral carpel wall to feed on an adjacent seed. Pupation occurs in the cavity being formed by the larva, and the adult exits through a hole chewed in the carpel wall (Burke, 1973
).
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Experimental study: growth conditions, fitness measures, and breeding design
In September 1994, seed of S. hendersonii was collected at random from female and hermaphrodite individuals from populations at Delta and Comox, British Columbia. Seeds (mericarps) were scarified and placed in a mixture of peat and fungicide (oxine benzoate 2.5%) at 9°C for 14 d. Germinated seeds were planted into pots at the University of British Columbia greenhouse and then transferred to insect-free growth chambers just prior to flowering. The growth chamber was maintained at 20°C with an 8-h photoperiod.
To identify the mode of inheritance for male sterility and the presence of fitness differences between the sexes, crosses (891 total) were performed between 17 female and 13 hermaphrodite plants and between separate hermaphrodite individuals. All hermaphrodite plants were also self-pollinated to test for inbreeding depression. Each maternal plant received pollen from several different pollen donors, although single flowers received pollen from one donor only. Each pollen donor was crossed to several different seed parents. Eight hermaphroditic individuals were used as pollen donors for crosses with females. These same eight individuals, as well as three additional pollen donors, were used for crosses between hermaphrodites.
Stamens at anthesis were removed from hermaphrodite flowers and used in hand pollinations. Both outcrossed and self-pollinated hermaphrodite seed parents were emasculated prior to receiving pollen. Protandry minimized the chances of contamination from self-pollen as the style typically emerged from the androecium 2–3 d following emasculation at anthesis.
The seeds produced from these crosses were harvested during the fall of 1995 and the number of viable seeds and unfertilized ovules was determined. The progeny from all crosses between any pair of parents were considered a family, while all progeny of any one seed parent were considered a maternal family. Thirty families with sufficient seed stock for genetic interpretation and statistical comparisons were selected. Female mothers were grouped into three maternal families (of 5, 4, and 2 families, respectively), and hermaphrodite mothers were grouped into five maternal families (of 3, 3, 4, 4, and 5 families, respectively).
In January 1996, the seeds from the selected families (660 seeds from female families, 361 seeds from outcrossed hermaphrodite families, and 82 seeds from selfed hermaphrodites) were planted. The seedlings were exposed to the same environmental conditions as the parent plants except that the growth chamber temperature and daylight hours were increased to accelerate germination and flowering (23°C, 12-h photoperiod). Germination was monitored every 1–2 d for 3 mo, and germinating seeds were marked for later detection of seedling mortality. To reduce position effects, individual pots were randomized and rotated every 2 wk for 4 mo, at which time the plants were too large and fragile to rotate. Survival was determined after 5 mo. The sex of each individual and the proportion of plants that flowered within 13 mo were scored. The results for sex determination were based on offspring from several different parent combinations; however, some parents produced more flowering offspring than others. Due to space limitations at the time of flowering, 250 female offspring (randomly selected within each family) were moved to a second growth chamber and used only for sex determination.
Field study: female frequency, seed set, and seed predation
Six populations of S. hendersonii were included in this study, one located at Delta, British Columbia (Ladner Marsh, LA) in the Lower Fraser Valley, and the other five from Vancouver Island (Campbell River, CR; Comox, CX; Duncan, DU; Port Alberni, PA; Sayward, SY). The relative frequency of females in each population was determined by scoring the sex of plants as encountered during surveys.
In June of 1995 and 1996, single racemes from female and hermaphrodite individuals were randomly selected and marked for subsequent measures of seed set and seed predation. At each population, 28–40 racemes per sex were collected both years in August. For estimates of seed set and seed predation by Anthonomus weevils, we counted the number of intact and completely consumed fruits. For fruits infested by tunneling Macrorhoptus weevils, we counted the number of damaged and undamaged seeds.
The average number of seeds per fruit was determined from a sample of the first ten intact fruits from the base of the stem upward. Every seed from this sample was dissected and classified as viable, unfilled (including unfertilized ovules and aborted seeds), or tunneled (containing larvae, weevil tunnels, or exit holes). Tunneled seeds will be referred to as "Macrorhoptus predation."
The number of completely eaten seeds was estimated (since no seeds remained to be counted) by multiplying the number of completely eaten fruit by the average seed production/fruit for the corresponding raceme. Completely eaten seeds will be referred to as "Anthonomus predation." Total seed predation per sex per population was calculated as the sum of tunneled and completely eaten seeds (Macrorhoptus predation + Anthonomus predation).
Analyses
Observed progeny sex ratios in the experimental population were compared to expected Mendelian ratios for a nuclear model, and differences were analyzed using a chi-square test. Differences in seed production among female, outcrossed hermaphrodite, and self-pollinated hermaphrodite parents were evaluated with a Kruskal-Wallis one-way ANOVA on ranks. Nonparametric analyses were performed when the data were not normally distributed and/or variances were unequal and when values could not be transformed. Differences in progeny performance were evaluated with a chi-square test. Multiplicative fitness (after Sakai, Karoly, and Weller, 1989
) was estimated for each maternal parent group as the product of seed production and progeny performance at all stages (overall fitness = proportion of viable seed produced x proportion of germinated seeds x proportion of seedlings that survived x proportion of progeny that flowered). Inbreeding depression was estimated as = 1 – ws/wo where wo is the overall fitness estimate of outcrossed progeny and ws is the overall fitness estimate of selfed progeny.
A nonparametric Mann-Whitney rank sum test was applied to compare mean values of females and hermaphrodites in natural populations for seed set and seed predation. All statistical analyses were performed with SigmaStat® v. 2.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2 = 0.0123; P > 0.5), while hermaphrodite mothers gave rise to hermaphrodite offspring only (44 progeny).
Female frequency
The mean frequency of females in natural populations of S. hendersonii was 39%, though values ranged from 14 to 54% (CR: 44%, N = 100; CX: 54%, N = 129; DU: 49%, N = 175; LA: 21%, N = 300; PA: 52%, N = 66; SY: 14%, N = 337).
Fitness measures
Experimental population
From hand pollinations, female parents had the highest overall fitness followed by outcrossed hermaphrodite parents, and selfed hermaphrodites had the lowest value. Outcrossed females produced 22% more viable seeds/fruit, had 31% greater germination, 7% higher survival, and 22% greater flowering success than outcrossed hermaphrodites (Table 1). Fitness measures for progeny of outcrossed hermaphrodite plants were three times higher than for progeny of self-pollinated hermaphrodites. Inbreeding depression is estimated at 0.67 ( = 1 – 0.01/0.03). This may be an underestimate, since estimates of inbreeding depression under greenhouse or growth chamber conditions are often lower than estimates under field conditions (Dudash, 1990
).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Kaul, 1988
; Kohn, 1989
).
This relatively uncomplicated result is surprising since a cytoplasmic–nuclear interaction was reported to control male sterility in the closely related gynodioecious congener S. oregana ssp. spicata (Ashman, 1992
). At least nine other gynodioecious Sidalcea species are known, suggesting that gynodioecy is not a recent development in the genus. The genetic control of an apparently well-established male sterility system in Sidalcea might be expected to be relatively complex. Alternatively, the frequency of gynodioecy in Sidalcea could also indicate that Sidalcea species are simply more susceptible to male sterility mutations, and the independent appearance of nuclear controlled gynodioecy is certainly possible. Another explanation for this inconsistency is that male-sterile cytoplasm may have been fixed in these populations of S. hendersonii. Some models suggest that cytoplasmic-nuclear gynodioecy is a nonequilibrium state inclined to evolve towards nuclear male sterility (Charlesworth and Ganders, 1979
; Delannay, Gouyon, and Valdeyron, 1981
). If male-sterile cytoplasm becomes fixed in a population, male sterility would appear to be controlled by nuclear genes (Charlesworth and Ganders, 1979
).
Theoretical models predict that for nuclear-controlled male sterility genes to persist, female Sidalcea hendersonii plants should be more than twice as fit as hermaphrodites. The requirements for female maintenance are the same if a fixed sterile cytoplasm interacts with nuclear, recessive, fertility-restoring alleles.
Fitness measures
Experimental population
If female advantage is the result of a difference in outcrossing rates and inbreeding depression, outcrossed hermaphrodites should have higher fitness than self-pollinated hermaphrodites. If differences in performance are a function of maternal sex-allocation effects, then females should have higher fitness than both outcrossed and selfed hermaphrodites. In the experimental population, outcrossed hermaphrodites did have higher fitness values than self-pollinated hermaphrodites, supporting the outcrossing hypothesis. However, females had higher fitness than outcrossed hermaphrodites, suggesting that maternal sex effects occur as well. Relative to females, outcrossed hermaphrodite fitness was estimated to be 0.18, indicating that 82% of the female advantage is most likely due to a maternal effect such as resource allocation differences between the sexes (i.e., females do not expend resources on pollen production). Compared to females, hermaphrodite fitness is reduced an additional 12% when inbreeding occurs.
Inbreeding depression was estimated at 0.67, suggesting that many of the progeny from selfing do not reproduce. An estimate of 0.67 for inbreeding depression is considered to be high, although inbreeding depression values were reported to range from 0.62 to 0.94 in gynodioecious Schiedea salicaria (Sakai, Karoly, and Weller, 1989
) and from 0.96 to 0.98 in gynodioecious Bidens sandvicensis (Schultz and Ganders, 1996
). Though inbreeding depression does appear to be high in S. hendersonii and differences in performance traits for outcrossed and selfed hermaphrodites are statistically significant, the values for overall fitness are so minute (<0.04) that perceived performance differences between the two may not be meaningful.
Natural populations
Averaged for all study populations, the proportion of viable seed to total ovules for females is 0.44 and for hermaphrodites is 0.44, i.e., f = 1 in Eq. 1. Overall, no maternal effect or outcrossing advantage is evident from seed viability data gathered in the field. These results do not eliminate the possibility of inbreeding effects because measures of fitness in natural populations can be complicated by ecological factors. For instance, developing seeds may also abort due to insufficient pollination, limited nutrients, or disease. In addition, most of the advantages associated with outcrossing and maternal effect reported for the experimental population may be detected in later life history stages that were not measured for natural populations.
The similarity in levels of seed production for females and hermaphrodites may also be affected by mating patterns in natural populations. For instance, the protandrous flowers of hermaphrodites could favor outcrossing in hermaphrodites and increase hermaphrodite fitness. Furthermore, females can also experience inbreeding depression if crossed with relatives. Biparental inbreeding in females of gynodioecious Hawaiian Bidens has been estimated to be as high as 25% (Sun and Ganders, 1988
).
Female frequency
The selfing rate of hermaphrodites was not measured, but it could not be high enough to explain observed female frequencies using Eq. 1. If = 0.67 and f = 1, for the female frequency to be P > 0.01, hermaphrodites of S. hendersonii must have a high selfing rate of >0.75. Even if the selfing rate were 1.0, the female frequency would only be 0.25. Despite a liberal estimate of selfing in natural populations, these values for selfing, inbreeding depression, and relative seed production are not great enough to explain the high frequency of females in populations of S. hendersonii (often exceeding 50%). When gynodioecy is determined by nuclear genes, a female frequency of 50% or higher implies that the populations are either not in equilibrium for their outcrossing rates or are functionally dioecious, i.e., hermaphrodite plants essentially function as males (Charlesworth and Charlesworth, 1978
; Ganders, 1978
). If S. hendersonii populations are functionally dioecious, selection may favor hermaphrodites that allocate additional resources to male function that could facilitate the evolution of dioecy. However, there was no indication of female sterility in hermaphrodites, as every flower examined for this study contained ovules, and hermaphrodites did produce viable seed in nature and in the experimental population. Furthermore, despite the high frequency of females, gynodioecy appears to persist in Sidalcea species with no known occurrence of obligate dioecy.
Sex-biased seed predation
In all cases of sex-biased predation in S. hendersonii, hermaphrodite plants experienced more damage than females. Sex-biased predation was evident only in populations where A. melancholicus occurred and was always correlated with completely eaten seeds. At Ladner Marsh, where M. sidalcea occurred exclusively, females and hermaphrodites experienced the same levels of seed predation. Macrorhoptus sidalcea was not a selective predator. Macrorhoptus sidalcea also occurs on S. nelsoniana in Oregon and has not demonstrated selective behavior on these plants either (Gisler and Meinke, 1997
).
The basis for discrimination between flower types by weevils was not investigated in this study. It seems highly likely that adult females of A. melancholicus, whose preferred food is pollen, may select hermaphrodite flowers rather than female flowers because they are attracted to pollen and improve their reproductive efficiency by using the same plant to brood their young. Weevils may further be attracted to the larger flowers of hermaphrodites, which form larger floral displays. Bruchid seed beetles were found to be attracted to larger flowers in Hibiscus moscheutos (Kudoh and Whigham, 1998
); however, no effect of petal size on rates of seed predation was evident. Also in Ipomopsis aggregata, predispersal seed predation by the dipteran Hylemya sp. increased with increasing inflorescence size (Brody and Mitchell, 1997
).
In gynodioecious and dioecious species that experience differential predation (e.g., Bawa and Opler, 1978
; Cox, 1982
; Uno, 1982
; Wagner and Miller, 1984
), the hermaphroditic or male flowers were attacked more frequently than the female flowers. Female Iris plants were thought to escape high levels of predation since they complete flowering and their capsules mature before the onset of the predator's developmental cycle (Uno, 1982
). Bawa and Opler (1978)
suggested a similar synchrony of male flowering and predator cycle in dioecious Simarouba.
Although many other species of Sidalcea are host to weevil predators (Dimling, 1992
; S. Gisler, Oregon Department of Agriculture, personal communication; T.-L. Ashman, University of Pittsburgh, personal communication), this is the first reported case of sex-biased seed predation in a Sidalcea species. It is possible that selective predation has not been reported for other species of Sidalcea because they do not share the same seed predators. Anthonomus melancholicus is not reported to be a predator of S. malvaeflora (Dimling, 1992
), S. campestris, S. virgata, or S. nelsoniana (S. Gisler, Oregon Department of Agriculture, personal communication). Anthonomus melancholicus or its ancestors may have accompanied S. hendersonii in its postglacial migration, and predator and host plant differentiated together.
Mating system and sex-biased seed predation
Females must produce significantly more seeds than hermaphrodites for male sterility mutations to be maintained in gynodioecious populations. The high frequency of females could not be completely explained by the mechanism of sex determination, inbreeding depression, or, in natural populations, maternal effects. Founder effects or genetic drift could possibly be responsible for these high frequencies. If, however, predation is included in the fecundity parameter, the average value for A. melancholicus infested populations is f = 0.64. With a value of s = 0.75 and = 0.67, the equilibrium frequency of females is now 27%, a high value that is much closer to observed frequencies of females in natural populations (Eq. 1 does not strictly apply when there are maternal effects on fitness other than seed set, but the results should be approximately correct). A model for Eq. 1 demonstrates the high selfing rates required for females to exist without seed predation, compared to much lower requirements when seed predation is considered (Fig. 5).
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proposed a model for the evolution of dioecy resulting from sex-related flower destruction by vertebrate pollinators. Perhaps a model for the evolution or maintenance of gynodioecy due to sex-biased seed predation could be similarly devised. The answers to the questions posed in the introduction follow. (1) Male sterility in S. hendersonii appears to be controlled by nuclear gene(s). (2) Despite experimental evidence of maternal effect and inbreeding depression, differences in viable seed production in nature were not evident unless seed predation was considered. (3) Sex-biased seed predation does occur in Sidalcea hendersonii. The seed predator Anthonomus melancholicus selectively consumed hermaphrodite seed resulting in significantly greater seed production for females. (4) The high degree of seed destruction in hermaphrodite plants appears to sustain high frequencies of females in populations of S. hendersonii. Sex-biased seed predation may provide the necessary advantage to females in this gynodioecious species.
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FOOTNOTES |
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2 Author for reprint requests, current address: Bureau of Land Management, West Eugene Wetlands Field Office, 751 South Danebo, Eugene, Oregon USA 97402 (melanie{at}peak.org
).
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  A. C. McCall Leaf damage and gender but not flower damage affect female fitness in Nemophila menziesii (Hydrophyllaceae) Am. J. Botany, March 1, 2007; 94(3): 445 - 450. [Abstract] [Full Text] [PDF]
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S.-M. Chang Female compensation through the quantity and quality of progeny in a gynodioecious plant, Geranium maculatum (Geraniaceae) Am. J. Botany, February 1, 2006; 93(2): 263 - 270. [Abstract] [Full Text] [PDF]
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M. Lopez-Villavicencio, A. Branca, T. Giraud, and J. A. Shykoff Sex-specific effect of Microbotryum violaceum (Uredinales) spores on healthy plants of the gynodioecious Gypsophila repens (Caryophyllaceae) Am. J. Botany, May 1, 2005; 92(5): 896 - 900. [Abstract] [Full Text] [PDF]
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 E. ASIKAINEN and P. MUTIKAINEN Preferences of Pollinators and Herbivores in Gynodioecious Geranium sylvaticum Ann. Bot., April 1, 2005; 95(5): 879 - 886. [Abstract] [Full Text] [PDF]
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L. F. Rosas, J. Perez-Alquicira, and C. A. Dominguez Environmentally induced variation in fecundity compensation in the morph-biased male-sterile distylous shrub Erythroxylum havanense (Erythroxylaceae) Am. J. Botany, January 1, 2005; 92(1): 116 - 122. [Abstract] [Full Text] [PDF]
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K. Andreasen and B. G. Baldwin Reexamination of relationships, habital evolution, and phylogeography of checker mallows (Sidalcea; Malvaceae) based on molecular phylogenetic data Am. J. Botany, March 1, 2003; 90(3): 436 - 444. [Abstract] [Full Text] [PDF]
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