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Reproductive Biology |
Departamento de Ecología Evolutiva, Instituto de Ecología, UNAM A.P. 70–275, Mexico D.F. 04510, Mexico
Received for publication March 10, 2004. Accepted for publication September 23, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: compensatory advantage • distyly • Erythroxylaceae • Erythroxylum havanense • flowering synchrony • Mexico • morph-biased male-sterility
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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the evolution of sex specialization has been a subject of deep interest among evolutionary biologists. The presence of male sterility in hermaphroditic plants has been considered a key factor influencing the evolution of sexual specialization (Lloyd, 1975
; Charlesworth and Charlesworth, 1978
; Couvet et al., 1990
; Maurice et al., 1993
; Schultz, 1994
; Webb, 1999
), because both theoretical and empirical evidence point out that male sterility in hermaphroditic species may represent the first step in the evolution of dioecy (Kohn, 1988
; Weller and Sakai, 1991
; Charlesworth, 1991
; Mayer and Charlesworth, 1992
; Geber et al., 1999
; Gigord et al., 1999
). Because hermaphroditic plants achieve roughly half of their fitness through the male function, male sterility results in a reproductive disadvantage. Consequently, for females to be maintained within a population, male-sterile individuals must compensate for the fitness loss through the male function (Charlesworth, 1981
; Gouyon and Couvet, 1987
; Delph et al., 1999
). Several theoretical studies have shown that the magnitude of compensation required to maintain male-sterile individuals in the population is determined by the mode of inheritance of male sterility. In the case of nuclear inheritance, females must be more than twice as fecund as hermaphrodites (Ross and Gregorious, 1985
; Frank, 1989
; Gouyon et al., 1991
). When male sterility is due to a cytoplasmic mutation, females will spread in the population with only a slight reproductive advantage (Lewis, 1941
; van Damme, 1983
; Belhassen et al., 1991
; Koelewijn and van Damme, 1995
). If both nuclear and cytoplasmic genes are responsible for male sterility (i.e., the inheritance is nucleocytoplasmic), the magnitude of compensation is expected to be intermediate between that expected for nuclear and cytoplasmic inheritances (Lewis, 1941
; Charlesworth, 1981
; Gouyon and Couvet, 1987
).
Although some part of the variation in fecundity between females and hermaphrodites might be associated with the mode of inheritance and the physiological mechanism of compensation (e.g., genetic variation for resource reallocation), it is well known that female fecundity also depends on several environmental factors (pollinators, resource and pollen limitation, reproductive phenology, seed predation, population sex structure, and metapopulation dynamics). For example, female plants of the gynodioecious Phacelia dubia had higher fruit and seed set than hermaphrodites after hand-pollination, but no evidence of compensation was observed in natural conditions (Del Castillo, 1993
). Such a result suggests that ecological factors might have a strong influence on the relative fecundities of females and hermaphrodites in natural conditions. Nonetheless, studies evaluating the magnitude of compensation in gynodioecious species usually assume that mating opportunities are equal for all plants within a population, and that the magnitude of female compensation depends exclusively on post-pollination mechanisms. It is therefore reasonable to expect that the extent of compensation could be influenced by ecological factors, particularly those determining the likelihood of pollination and ovule fecundation. For instance, even though male-sterile plants have the ability to produce more or better seeds, pollen or pollinator limitation could reduce the advantages of compensation. In accordance, given that the magnitude of female compensation of male-sterile individuals has been considered as a key factor in both the maintenance of gynodioecy and the evolution of dioecy (Gouyon et al., 1991
; Maurice et al., 1993
, 1994
; Schultz, 1994
), the influence of environmental variance in the expression of compensation could affect the tempo and mode of the evolutionary trajectory of sex specialization in species with male sterility. Few studies, however, have taken into account the combined effects of male sterility and ecological factors on the magnitude of female compensation (but see Williams and Fenster, 1998
; Graff, 1999
; Taylor et al., 1999
; Marshall and Ganders, 2001
; Ramsey and Vaughton, 2002
).
In this study we evaluated the effects of both male sterility and reproductive synchrony (a factor influencing pollinator attraction and the availability of mates) on the magnitude of female compensation in a natural population of the distylous shrub Erythroxylum havanense Jacq. (Erythroxylaceae), a species with morph-biased male sterility (Domínguez et al., 1997
). A study involving five populations showed that pin individuals produce on average 49% more viable pollen than thrums (Cuevas et al., in press
). Results from hand-pollination experiments showed that male-sterile thrum plants may have a strong compensatory advantage. The probability to survive to age 8 and reproduce associated to the progeny derived from thrum mothers was 0.092, while this value amounted 0.033 for the progeny derived from pin mothers (a 2.8 reproductive advantage; Avila-Sakar and Domínguez, 2000
). Although this advantage is expressed after hand-pollination, we have noticed that the magnitude of compensation under natural conditions may show a striking variation among reproductive seasons (Domínguez et al., 1997
; Avila-Sakar and Domínguez, 2000
; C. A. Domínguez, personal observation).
On the other hand, it has been shown that female fitness in E. havanense is highly influenced by flowering synchrony (Domínguez and Dirzo, 1995
). Flowering phenology of E. havanense is characterized by a marked intra- and inter-individual flowering synchrony. Selection analyses showed that flowering time explains 20–27% of the individual variance in female fecundity, indicating that fitness is highly dependent on flowering synchrony (Domínguez and Dirzo, 1995
). Selection gradients on flowering time for 1987 and 1988 were opposite in sign, indicating the presence of a heterogeneous regime of natural selection. It was further demonstrated that such heterogeneity was a consequence of the annual variation in the patterns of rainfall (Domínguez and Dirzo, 1995
).
Hence, E. havanense is a species in which mate availability and/or mating likelihood depend on flowering synchrony, an attribute highly influenced by environmental variance (Domínguez and Dirzo, 1995
). Moreover, male-sterile thrum individuals show a marked compensatory advantage after hand-pollination (Avila-Sakar and Domínguez, 2000
), but whose magnitude varies from year to year in natural conditions (Domínguez et al., 1997
). This situation offers the opportunity to evaluate whether or not the expression of compensation in male-sterile plants depends on flowering synchrony. In this study we evaluated the joint effects of male sterility, flower production, and flowering synchrony on the female reproductive success of individuals from a natural population of Erythroxylum havanense from the Pacific coast of Mexico.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The vegetation is a dense tropical deciduous forest. A detailed description of the flora and climate of the Chamela region can be found in Bullock (1986)
, Lott et al. (1987)
, and Noguera et al. (2002)
.
Study plant
Erythroxylum havanense is a perennial distylous shrub with complete intramorph incompatibility (i.e., no fruits are produced from crosses within the same morph; Domínguez, 1990
). Plants grow on patches of 20–80 individuals. Flowering initiates 7–10 d after the first intense rains that mark the beginning of the wet season when individual flowering thresholds are reached by the increase in soil humidity (Domínguez and Dirzo, 1995
). Once flowering is triggered, individual plants flower for a very short period (2.8 ± 0.1 d, mean ± 1 SE hereafter). The availability of water for plants depends on a series of highly heterogeneous environmental factors as topographic zone (slopes, plateaus or gullies, aspect; Domínguez and Dirzo, 1995
), soil characteristics (texture, organic matter content, infiltration; Domínguez and Dirzo, 1995
; Cotler et al., 2002
), and rainfall heterogeneity (García-Oliva et al., 1991
; García-Oliva et al., 2002
). All these environmental attributes interact with each other to produce a complex spatio-temporal dynamics in terms of water availability for plants. Accordingly, flowering phenology may range from synchronous years characterized by short flowering periods (5.7 ± 0.9 d) in which 84% of the total flower production occurs in two peak flowering days; to asynchronous years with relatively extended flowering periods (up to 20 d) and a more evenly distribution of flower production (Domínguez and Dirzo, 1995
). Flowers are small (
1 cm of diameter), and stigma receptivity is limited to the first half of the day. Erythroxylum havanense is mainly pollinated by wild bees of the genus Trigona (Apidae) and Xylocopa (Anthophoridae) (Domínguez et al., 1997
). Fruits are ovoid red drupes (1 cm long) that contain only one fertile ovule, and thus are single seeded. As mentioned above, E. havanense is also characterized by morph-biased male sterility associated with a compensatory female advantage in thrum plants (Domínguez et al., 1997
; Avila-Sakar and Domínguez, 2000
). The magnitude of compensation, however, shows a marked temporal variation among reproductive seasons.
Data collection
Reproductive phenology
During the reproductive season of 2000 we followed the flowering and fruiting phenology of all the reproductive plants from the Ardilla population (N = 76). For each plant we made daily censuses to record the number of flowers, immature fruits, and ripe fruits. Censuses were initiated the first day a plant produced flowers (7 June 2000) and finished when all fruits in the population had ripened (12 July 2000).
Flowering synchrony
Flowering synchrony in E. havanense had been previously measured as the inter-individual variation in flowering initiation day (see Domínguez and Dirzo, 1995
). Nonetheless, the extreme flowering synchrony we observed in 2000 (see Results) precluded the usage of this index. Instead, we used an index that accounted for the small differences in the timing of flower production that we observed among the individuals from the Ardilla population in 2000. For each plant we estimated the proportion of its flowers that were produced during the peak flowering day of the population. This value ranges from 1 to 0. Plants with values (synchrony index) close to 1 produced a high proportion of their flowers when a large amount of pollen and ovules were available in the population. Values close to zero indicate plants that produced most of their flowers out of synchrony with the population.
Male sterility
To assess the amount of variation in male sterility, as well as to estimate the repeatability of this attribute, we made in vitro pollen cultures during the reproductive seasons of 1998 and 1999 for the same 24 plants. In the 1999 sample, 23 new plants were included for a total of 47 individuals. One day before anthesis several branches on each plant were bagged to prevent pollinator visitation and contamination with pollen from other plants. Pollen collections were made on the day of anthesis between 0900 and 1200. We collected four flowers per plant, and each of four anthers per flower was rubbed onto the surface of previously prepared culture medium on a microscope slide. The medium was modified from Mazer (1987)
and was composed of 250 g/L of sucrose, 0.238 g/L of H3BO3, 0.357 g/L of Ca (NO3) 2·4H2O and 8.33 g/L of agar. Previous experiments have shown this culture medium is adequate for the evaluation of pollen viability in E. havanense (Avila-Sakar and Domínguez, 2000
; Cuevas et al., in press
). Time between pollen collection and initiation of cultures was always less than 5 min. Cultures were incubated in Petri dishes at ambient temperature, and after 12 h of growth they were fixed with FAA (formaldehyde (37–40%), ethyl alcohol (95%), glacial acetic acid, and water; 10 : 50 : 5 : 35 v/v) and sealed with clear nail polish. Using an optical microscope (Olympus model BH 2, with 40x optical magnification) we counted the number of germinated and nongerminated pollen grains on every slide. For each plant we calculated the fraction of germinated to total pollen grains from the pooled data (16 slides), and this measure was used as an estimation of the level of male sterility per plant.
Data analysis
Male sterility
We first investigated the effect of floral morph on the level of male sterility by means of one-way analysis of variance (JMP 4.0.4., SAS, 2001
). Male sterility was arcsine transformed to improve normality of the error distribution. Because of the difficulty of measuring the heritability (h2) of male sterility in E. havanense (it takes 8 yr for this species to reproduce), we measured its repeatability through the calculation of the interclass correlation coefficient between levels of male sterility in 1998 and 1999 (N = 24 plants). Repeatability measures the amount of the phenotypic variance in a trait due to permanent differences between individuals. Given that permanent differences can be attributed both to genetic variance and to the local environment, the repeatability of a trait sets an upper limit to the degree of genetic determination (Falconer and Mackay, 1996
).
Effects of morph, flowering synchrony, and flower number on fruit production
In order to evaluate the differences in fruit production between pin and thrum plants taking into account the variance in flower number and flowering synchrony, we performed a covariance analysis (PROC GLM, SAS, 1989
). Morph, flowering synchrony, and flower number were included as the main factors in this analysis. We also included the quadratic terms of flower number, and all the interactions among the three main factors. The significance of the morph term should be indicative of compensation if higher fruit production is associated to the more sterile morph. Flowering synchrony measures the dependence of female fitness on the availability of potential mates and on the likelihood of pollination (i.e., the ecological factors). Because flower number has a strong effect on fruit production (Domínguez and Dirzo, 1995
), we included this variable within the analysis. Given that flower number and flowering synchrony were measured in very different scales and because we were interested in comparing their relative effects on fruit production, they were standardized to mean zero and standard deviation 1 prior to analysis ([x – 
]/SD). This procedure allowed a direct comparison between these variables because they were expressed in units of standard deviations.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Male sterility
Male sterility ranged from 0.43 to 1, with a mean of 0.75 (±0.019). Preliminary paternity analysis for the same population investigated in this study showed that plants with levels of male sterility higher than 0.9 sire not a single seed; thus, they can be considered completely male sterile (F. Rosas and C.A. Domínguez, unpublished data). Accordingly, 14% of the plants in the Ardilla population were completely male-sterile. Thrum plants had a higher proportion of completely male-sterile plants (0.23) than pins (0.05), and also a higher level of male sterility (0.81 ± 0.02 and 0.68 ± 0.02, for thrum and pin plants, respectively; F1, 45 = 13.56, P = 0.006, R2 = 0.21; Fig. 1). The estimated repeatability of male sterility was 0.47 (±0.11), indicating that a relatively high fraction of the phenotypic variation in male sterility is explained by permanent differences among individuals (F1, 22 = 15.8, P = 0.0006, R2 = 0.39). The significant difference in male sterility between floral morphs, along with its constant expression through time (repeatability), suggests that male sterility in E. havanense has a heritable component that is independent of environmental variation.
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), flowering synchrony had a positive and significant effect on fruit production. Flower number had also a positive effect on fruit production, simply indicating that plants with many flowers produce more fruits. The significance of the interaction flowers x morph showed that the slope of fruit production on flower number was higher for thrum plants. Hence, the more male-sterile morph (i.e., thrum) was more efficient to mature fruits as the number of flowers per plant increased (Fig. 2). As indicated by the significance of the interaction between flowers x synchrony, natural selection favored those plants that produced many flowers and flowered in synchrony with the population. The combined effects of flower number and flower synchrony had a dramatic influence on the reproductive compensation of thrum plants. Because compensation in E. havanense may be defined as the relative fecundity of thrum vs. pin individuals, and flowering synchrony had a marked influence on the reproductive output of both morphs, the magnitude of compensation changed as a function of an environmentally induced trait. Based on the model adjusted by the covariance analysis, we produced two different scenarios regarding the effect of flowering synchrony on the magnitude of compensation (expected fruit production of pins = 63.6 + 147.99 x flowers + 86.13 x synchrony + flowers x synchrony x 253.9; and expected fruit production of thrums = 128.62 + 385.98 x flowers + 86.13 x synchrony + flowers x synchrony x 253.9). Figure 2A shows the expected fruit production of pin and thrum plants flowering under relatively high flowering synchrony conditions (synchrony index = 0.5 SD above the population mean). This figure also shows the estimated values of compensation under this scenario (fruit production of thrums/fruit production of pins). Figure 2B, in contrast, illustrates plants flowering out of synchrony with the population (synchrony index = –0.5 SD below the population mean). It is clear from these figures that fruit production is highly dependent on both flower number and flowering synchrony, but, unexpectedly, the magnitude of compensation was higher under low synchrony conditions.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), and even so we were able to detect an important difference between synchronous and asynchronous plants. Consequently, it could be expected that the effect of synchrony on the reproductive compensation of synchronous vs. asynchronous thrum plants would be even greater in years allowing a higher variation in flowering times (see Domínguez and Dirzo, 1995
). Although we found a marked effect of flowering synchrony on the compensatory advantage of thrums, the direction of such an effect was opposite to our original expectative. Flowering synchrony decreased, instead of increased, the magnitude of compensation. Because pin individuals produced almost no fruits when they flowered out of synchrony, there was an eightfold difference in fruit production between synchronous and asynchronous pin plants. Contrastingly, synchronous thrum plants only produced two times as many seeds as thrum individuals flowering out of synchrony (cf. Fig. 2). As a consequence, the magnitude of the compensatory advantage of thrum plants decreased with flowering synchrony. This result should be interpreted with caution because, although the relative fecundity of thrums (fruit production of thrums/fruit production of pins) showed an inverse relationship with flowering synchrony, the absolute fecundity of both morphs was much higher when plants flowered in synchrony with the population.
The inverse relationship between compensation and synchrony found in this study calls for an explanation. Asynchronous flowering produces a relatively poor reproductive environment (mate, pollen, and pollinator limitation: Augspurger, 1980
, 1981
; Domínguez and Dirzo, 1995
; Domínguez et al., 1997
) that reduces the opportunities for successful reproduction of both morphs. Although we actually observed a reduction in fruit production in asynchronous flowering individuals, the negative consequences were more severe on pin than thrum plants. Given that the only difference between the pollen produced by the floral morphs is a higher frequency of abnormal pollen grains in thrum plants (there are no differences in pollen production neither in pollen size, Vázquez-Santana et al., 1996
; Domínguez et al., 1997
), a load of thrum pollen has a smaller number of viable pollen grains. Hence, pin plants that flowered out of synchrony with the population were exposed to low pollen loads composed of low-quality pollen grains. Thrum plants were also exposed to low pollen loads, but they were pollinated with relatively high-quality pollen. This asymmetry in the qualities of the pollen loads received by each morph could explain the meager fruit production of pin plants and also the elevated value of compensation observed when plants flowered out of synchrony.
Mass flowering has been envisioned as an attribute favored by natural selection because opportunistic pollinators should take advantage of the concentrated amount of rewards that flowering synchrony provides (Gentry, 1974
; Augspurger, 1980
, 1981
; Gross and Werner, 1983
; Mori and Pipoly, 1984
; Dieringer, 1991
). Besides of increasing the attractiveness of a flowering patch to pollinators, flowering synchrony also produces the conditions that maximize the rates of pollen-donation deposition and the opportunities to find mates. This is particularly true for E. havanense because this is a self-incompatible species that requires pollinator visitation to produce fruits. In fact, previous studies have shown that flowering in synchrony with the population has marked consequences on the reproductive success of E. havanense individuals (Domínguez and Dirzo, 1995
).
Accordingly, we think that the differences in the curves describing reproductive compensation as a function of flower number could be explained by the influence of synchrony on the foraging behavior of pollinators. When plants flowered in high synchrony, the curve of compensation reached a plateau at relatively low flower numbers (Fig. 2A). Asynchronous flowering, in contrast, produced a curve in which compensation always increased (Fig. 2B). It is possible that large numbers of flowers confer an important advantage when plants flower out of synchrony, because these plants monopolize most of the few available pollinators. Large pin plants are also expected to attract more pollinators, but because most of the pollen they received is nonviable, their fecundity should be low. When plants flowered in synchrony with the population fruit production increased at a higher rate (number of fruits per flower), but compensation showed an asymptotic behavior around a value of two. These observations suggest that the high concentration of resources brought about by flowering synchrony reduces the threshold (number of flowers) used by pollinators to discriminate against plants with few flowers. Under these circumstances, both morphs would receive enough viable pollen and fecundity would depend mainly on post-pollination mechanisms.
Obviously the above interpretation depends on the assumption that pollinators discriminate among plants that differ in flower number. Previous studies have shown that the most common species of pollinators of E. havanense forage preferentially on plants with many flowers (Domínguez et al., 1997
). Moreover, the average fruit set of large plants (those above the mean value of flower number) was significantly higher than that of the small ones (0.41 ± 0.04 and 0.22 ± 0.02 fruits per flower; for large and small plants, respectively; F1, 75 = 10.48, P = 0.001), suggesting that pollinator visitation was more intense in the former than in the latter individuals. Pollen limitation has also been proved to affect female fecundity in the gynodioecious Silene vulgaris (McCauley et al., 2000
), and in Wurmbea biglandulosa (Ramsey and Vaughton, 2002
).
Results of this study support previous findings (Domínguez et al., 1997
; Avila-Sakar and Domínguez, 2000
) indicating that the partial loss of the male function of thrum individuals of Erythroxylum havanense is compensated by a fitness increase through the female function. After hand-pollination thrum individuals outperform pin ones as maternal plants by producing more and better seeds (Avila-Sakar and Domínguez, 2000
). However, as this study demonstrates, the expression of compensation in natural conditions depends on flowering synchrony, probably because of its effect on successful pollination. As a consequence, the magnitude of the reproductive compensation of thrum plants of E. havanense ranged from zero (in small plants) to almost ten (in the larger plants). Reproductive compensation has been described in other species with male sterility (reviewed in Shykoff et al., 2003
), and the magnitude of this parameter is thought to be involved in the maintenance of male-sterile individuals and in the evolution of dioecy (Lewis, 1941
; Charlesworth and Charlesworth, 1978
; Gouyon and Couvet, 1987
; Maurice et al., 1993
, 1994
; Schultz, 1994
; Charlesworth, 1999
). Theoretical models predict that in the most stringent conditions (nuclear inheritance), male-sterile individuals should exhibit a twofold compensatory advantage to be maintained in the population (Lewis, 1941
; Charlesworth, 1999
). Nucleocytoplasmatic inheritance, in contrast, requires just a subtle fecundity advantage for polymorphism to be maintained (Couvet et al., 1986
; Gouyon and Couvet, 1987
; Schultz, 1994
). Although we do not know the genetic mechanism determining male sterility in E. havanense, our results suggest that this attribute has a heritable component (see also Domínguez et al., 1997
). Moreover, independently of the particular mechanism of inheritance, the values of compensation observed in this study were very close, or even much higher, than the most stringent theoretical threshold (under nuclear inheritance) for male-sterile individuals to be maintained in the population. This result suggests that the magnitude of the fecundity compensation (seed production, the quantitative compensation; sensu Alonso and Herrera, 2001
) observed in E. havanense is high enough as to maintain male-sterile individuals in the population. Given that this species also shows a qualitative compensatory advantage (offspring quality; Avila-Sakar and Domínguez, 2000
), the overall value of compensation should be far beyond the theoretical threshold.
Our finding of environmentally induced variation in the expression of the reproductive compensation of E. havanense suggests that the selective dynamics of male sterility may change on an annual basis depending on the level of flowering synchrony (Domínguez and Dirzo, 1995
). Highly synchronous years would allow maximum fruit production and a relatively low compensatory advantage. Nonetheless, such an advantage is high enough as to favor the permanence of male-sterile individuals. On the other hand, because of the disproportionate effect that pollinator limitation and the scarcity of potential consorts (see Williams and Fenster, 1998
; Taylor et al., 1999
; Ramsey and Vaughton, 2002
) have on the quality of the pollen loads received by pin plants, the compensatory advantage of thrums is boosted during years of low flowering synchrony. Thus, in the particular case of E. havanense, male-sterile individuals always enjoy a compensatory advantage whose magnitude changes dramatically depending on flowering synchrony. Given that male sterility in natural populations is considered a key factor in the evolution of sex specialization in hermaphrodite species (Lloyd, 1975
; Charlesworth and Charlesworth, 1978
; Maurice et al., 1993
; Shultz, 1994
; Webb, 1999
), the potentially intense influence of environmental variance in the expression of compensation could affect the rate of evolution of the reproductive system of E. havanense. In general terms, the findings of this study suggest that environmental heterogeneity has the potential to affect the expression of the compensatory advantage of male-sterile individuals in gynodioecious species and, therefore, the evolutionary trajectory of sex specialization.
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FOOTNOTES |
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The authors thank Rubén Pérez Ishiwara, César Abarca, Eduardo Cuevas, and Martha Palomino for field assistance and logistic support. Luis E. Eguiarte, Juan Fornoni, Francisco Molina, Mauricio Quesada, and two anonymous reviewers made valuable comments on early drafts of the manuscript. This paper was written in partial fulfillment of the requirements for the Ph.D. degree of L.F.R. at the Universidad Nacional Autonoma de Mexico (UNAM). This study was supported by a Ph.D. grant from CONACYT to L.F.R. and a grant from the PAPIIT program from Universidad Nacional Autónoma de Mexico (IN209600) to C.A.D. 
2 Author for correspondence (tejada{at}servidor.unam.mx
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Augspurger C. K. 1980 Mass flowering of a tropical shrub (Hybanthus prunifolius): influence on pollinator attraction and movement. Evolution 34: 475-488[CrossRef][ISI]
Augspurger C. K. 1981 Reproductive synchrony of a tropical shrub: experimental studies on effects of pollinators and seed predators on Hybanthus prunifolius (Violaceae). Ecology 62: 775-788[CrossRef][ISI]
Avila-Sakar G. C. A. Domínguez 2000 Parental effects and gender specialization in a tropical heterostylous shrub. Evolution 54: 866-877[ISI][Medline]
Belhassen E. E. Dommée B. Atlan A. Gouyon P. H. Pomente D. Assoud M. W. Couvet 1991 Complex determination of male sterility in Thymus vulgaris: genetic and molecular analysis. Theoretical and Applied Genetics 82: 137-143[ISI]
Bullock S. H. 1986 Climate of Chamela, Jalisco, and trends in the south coastal region of Mexico. Archives for Meteorology, Geophysics, and Bioclimatology 36: 297-316
Charlesworth B. 1991 The evolution of sex chromosomes. Science 251: 1030-1033
Charlesworth B. D. Charlesworth 1978 A model for the evolution of dioecy and gynodioecy. American Naturalist 112: 975-997[CrossRef][ISI]
Charlesworth D. 1981 A further study of the problem of the maintenance of females in ginodioecious species. Heredity 46: 27-39
Charlesworth D. 1999 Theories of the evolution of dioecy. In M. A. Geber, T. E. Dawson, and L. F. Delph [eds.], Gender and sexual dimorphism in flowering plants, 33–60. Springer Verlag, Berlin, Germany
Cotler H. E. Durán C. Siebe 2002 Caracterización morfo-edafológica y calidad de sitio de un bosque tropical caducifolio. In F. Noguera, J. Vega-Rivera, A. García-Aldrete, and M. Quesada-Avendaño [eds.], Historia Natural de Chamela, 17–79. Universidad Nacional Autónoma de Mexico, Mexico
Couvet D. A. Atlan E. Belhassen C. Gliddon P. H. Gouyon F. Kjellberg 1990 Co-evolution between two symbionts: the case of cytoplasmic male-sterility in higher plants. In D. Futuyma and J. Antonovics [eds.], Oxford survey in evolutionary biology, 225–250. Oxford University Press, Oxford, UK
Couvet D. F. Bonnemaison P. H. Gouyon 1986 The maintenance of females among hermaphrodites: the importance of nuclear-cytoplasmic interactions. Heredity 57: 325-330[ISI]
Cuevas G. E. F. Molina-Freaner L. E. Eguiarte C. A. Domínguez In press Patterns of male sterility within and among populations of the distylous shrub Erythroxylum havanense (Erythroxylaceae). Plant Ecology
Darwin C. 1877 The different form of flowers of the same species. John Murray, London, UK
Del Castillo R. F. 1993 Consequences of male sterility in Phacelia dubia. Evolutionary Trends in Plants 7: 15-22
Delph L. F. M. A. Bailey D. L. Marr 1999 Seed provisioning in gynodioecious Silene acaulis (Caryophyllaceae). American Journal of Botany 86: 140-144
Dieringer G. 1991 Variation in the individual flowering time and reproductive success of Agalinis strictifolia (Scrophulariaceae). American Journal of Botany 78: 497-503[CrossRef][ISI]
Domínguez C. A. 1990 Consecuencias ecológicas y evolutivas del patrón de floración sincrónico y masivo de Erythroxylum havanense Jacq. (Erythroxylaceae). Doctoral dissertation, Universidad Nacional Autónoma de Mexico, Mexico D.F., Mexico
Domínguez C. A. G. Avila-Sakar S. Vázquez-Santana J. Marquez-Guzmán 1997 Morph-biased male sterility in the tropical distylous shrub Erythroxylum havanense (Erythroxylaceae). American Journal of Botany 84: 626-632[Abstract]
Domínguez C. A. R. Dirzo 1995 Rainfall and flowering synchrony in a tropical shrub: variable selection on the flowering time of Erythroxylum havanense. Evolutionary Ecology 9: 204-216[CrossRef][ISI]
Falconer D. S. T. F. C. Mackay 1996 Introduction to quantitative genetics. Longman, Edinburgh, UK
Frank S. A. 1989 The evolutionary dynamics of cytoplasmic male sterility. American Naturalist 133: 345-376[CrossRef][ISI]
García-Oliva F. A. Camou J. M. Maass 2002 El clima de la region central de la costa del Pacífico mexicano. In F. Noguera, J. Vega-Rivera, A. García-Aldrete, and M. Quesada-Avendaño [eds.], Historia Natural de Chamela, 3–10. Universidad Nacional Autónoma de Mexico, Mexico
García-Oliva F. E. Ezcurra L. Galicia 1991 Patterns of rainfall distribution in the Central Pacific coast of Mexico. Geografiska Annaler 73A: 179-186
Geber M. A. T. E. Dawson L. F. Delph 1999 Gender and sexual dimorphism in flowering plants. Springer Verlag, Berlin, Germany
Gentry A. H. 1974 Flowering phenology and diversity in tropical Bignoniaceae. Annals of the Missouri Botanical Garden 61: 728-759[CrossRef][ISI]
Gigord L. C. Lavigne J. A. Shykoff A. Atlan 1999 Evidence for effects of restorer genes on male and female reproductive functions of hermaphrodites in the gynodioecious species Thymus vulgaris L. Journal of Evolutionary Biology 12: 596-604[CrossRef][ISI]
Gouyon P. H. D. Couvet 1987 A conflict between two sexes, females and hermphrodites. In S. C. Stearns [ed.], The evolution of sex and its consequences, 245–261. Birkhäuser, Basel, Switzerland
Gouyon P. H. F. Vichot J. M. M. van Damme 1991 Nuclear-cytoplasmic male sterility: single-point equilibria vs. limit cycles. American Naturalist 137: 498-514[CrossRef][ISI]
Graff A. 1999 Population sex structure and reproductive fitness in gynodioecious Sidalcea malviflora malviflora (Malvaceae). Evolution 53: 1714-1722[CrossRef][ISI]
Gross R. S. P. A. Werner 1983 Relationships among flowering phenology, insect visitors, and seed set of individuals: experimental studies on four co-occurring species of goldenrod (Solidago: Compositae). Ecological Monographs 53: 95-117
Koelewijn H. P. J. M. M. van Damme 1995 Genetics of male sterility in gynodioecious Plantago coronopus. I. Cytoplasmic variation. Genetics 139: 1749-1758[Abstract]
Kohn J. R. 1988 Why be a female?. Nature 335: 431-433[CrossRef]
Lewis D. 1941 Male sterility in natural populations of hermaphrodite plants. New Phytologist 40: 56-63[CrossRef]
Lloyd D. G. 1975 The maintenance of gynodioecy and androdioecy in angiosperms. Genetica 45: 325-329[CrossRef][ISI]
Lott E. J. S. H. Bullock J. A. Solís-Magallanes 1987 Floristic diversity and structure of upland and arroyo forest of coastal Jalisco. Biotropica 19: 228-235[CrossRef][ISI]
Marshall M. F. R. Ganders 2001 Sex-biased seed predation and the maintenance of females in a gynodioecious plant. American Journal of Botany 88: 1437-1443
Maurice S. E. Belhassen D. Couvet P. H. Gouyon 1994 Evolution of dioecy: can nuclear-cytoplasmic interactions select for maleness?. Heredity 73: 346-359
Maurice S. D. Charlesworth C. Desfeux D. Couvet P. H. Gouyon 1993 The evolution of gender in hermaphrodites of gynodioecious populations with nucleo-cytoplasmic male sterility. Proceedings of the Royal Society of London, Series B, Biological Sciences 251: 253-261[CrossRef]
Mayer S. S. D. Charlesworth 1992 Genetic evidence for multiple origins of dioecy in the Hawaiian shrub Wilkstroemia. Evolution 46: 207-215[CrossRef][ISI]
Mazer S. J. 1987 Parental effects on seed development and seed yield in Raphanus raphanistrum: implications for natural and sexual selection. Evolution 41: 355-371[CrossRef][ISI]
McCauley D. E. M. S. Olson D. R. Taylor 2000 The influence of metapopulation structure on genotype fitness in a gynodioecious plant. Evolutionary Ecology 14: 181-194
Mori S. A. J. J. Pipoly 1984 Observations on the big-bang flowering of Miconia minutiflora (Melastomataceae). Brittonia 36: 337-341[CrossRef][ISI]
Noguera F. A. J. H. Vega-Rivera A. N. García-Aldrete M. Quesada-Avendaño 2002 Historia Natural de Chamela. Universidad Nacional Autonoma de Mexico, Mexico D.F., Mexico
Ramsey M. G. Vaughton 2002 Maintenance of gynodioecy in Wurmbea biglandulosa (Colchicaceae): gender differences in seed production and progeny success. Plant Systematics and Evolution 232: 189-200[CrossRef][ISI]
Ross M. D. H. R. Gregorius 1985 Selection with gene-cytoplasm interactions. II. Maintenance of gynodioecy. Genetics 109: 427-439
SAS. 1989 SAS/STAT user's guide, release 6.08. SAS Institute, Cary, North Carolina, USA
SAS. 2001 JMP User's Guide, release 4.0.4. SAS Institute, Cary, North Carolina, USA
Schultz S. T. 1994 Nucleo-cytoplasmatic male sterility and alternative routes to dioecy. Evolution 48: 1933-1945[CrossRef][ISI]
Shykoff J. A. S. O. Kolokotronis C. L. Collin M. L. Villavicencio 2003 Effects of male sterility on reproductive traits in gynodioecious plants: a meta analysis. Oecologia 135: 1-9[ISI][Medline]
Taylor D. R. D. McCauley S. Trimble 1999 Colonization success of females and hermaphrodites in the gynodioecious plant Silene vulgaris. Evolution 55: 745-751
van Damme J. M. M. 1983 Gynodioecy in Plantago lanceolata L. II. Inheritance of three male sterility types. Heredity 50: 253-273[ISI]
Vázquez-Santana S. C. A. Domínguez J. Márquez 1996 Embriología de Erythroxylum havanense (Erythroxylaceae), una especie heterostílica. Boletín de la Sociedad Botánica de Mexico 59: 25-33
Webb C. J. 1999 Empirical studies: evolution and maintenance of dimorphic breeding systems. In M. A. Geber, T. E. Dawson, and L. F. Delph [eds.], Gender and sexual dimorphism in flowering plants. Springer Verlag, Berlin, Germany
Weller S. G. S. G. Sakai 1991 The genetic basis of male sterility in Schidea (Caryophyllaceae), an endemic Hawaiian genus. Heredity 67: 265-273[ISI]
Williams H. L. C. B. Fenster 1998 Ecological and genetic factors contributing to the low frequency of male sterility in Chamaecrista fasciculata (Fabaceae). American Journal of Botany 85: 1243-1250
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