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Reproductive Biology |
T. H. Morgan School of Biological Sciences, University of Kentucky, 101 Morgan Bldg., Lexington, Kentucky 40506-0225 USA
Received for publication May 17, 2001. Accepted for publication October 4, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: asexual reproduction • bryophytes • Marchantiacae • Marchantia inflexa • selection • sexual dimorphism • trade-offs
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Sexually dimorphic traits may evolve and be maintained through natural selection when sex-specific selection leads to different phenotypic trait optima for the sexes (Putwain and Harper, 1972
; Dawson and Geber, 1999
). In combination with sex-specific selection, environment-dependent selection may lead to habitat partitioning and spatial segregation of the sexes (Lloyd and Webb, 1977
; Kohorn, 1994
; Dawson and Geber, 1999
; Delph, 1999
) that can maintain sexual dimorphisms in vegetative and reproductive characters. Sex-specific costs of plasticity may contribute to the spatial segregation of sexes when selection on traits is environment-dependent and plasticity of a trait, independent of the trait itself (Van Tienderen, 1991
), is under sex-specific selection.
The focus of studies of plant sexual dimorphisms has been on differences between mature females and males in traits associated with sexual reproduction. Sexual dimorphism is expected in adult plants in which the sexes exhibit differences in resource allocation as a result of different costs of sexual reproduction (Lloyd and Webb, 1977
; Charnov, 1982
; Lloyd, 1982
; Meagher and Antonovics, 1982a
; Meagher, 1984
; Shine, 1989
; Eppley, Stanton, and Grosberg, 1998
; Delph, 1999)
. Monomorphism of the sexes is expected in preadults because plants exhibit indeterminate growth and nonreproductive individuals, regardless of sex, likely experience similar growth constraints (Lloyd and Webb, 1977
). However, preadult sexual dimorphisms have been reported in seed plants and bryophytes for characters including growth rates (Allen, 1919
; Godley, 1964
; Lloyd, 1973
; Shaw and Gaughan, 1993
; McLetchie and Puterbaugh, 2000
) and asexual reproductive rates (Voth and Hamner, 1940
; McLetchie and Puterbaugh, 2000
). Sexual dimorphism in vegetative characters associated with preadult plants may result from correlated selection on adult sexual reproductive traits such as inflorescence architecture (Kohorn, 1994
; Geber, 1995
). Measuring selection on sexually dimorphic characters in preadults is important because natural selection may act with different magnitudes and in opposing directions among life stages of individuals (Schluter and Smith, 1986
; Andersson, 1994
; Preziosi and Fairbairn, 2000
), and the adaptive significance of adult sexual dimorphisms may be confounded by the action of strong selection on sexually dimorphic traits in preadults (Purrington and Schmitt, 1998
).
We used Marchantia inflexa (Nees et Mont), a dioecious, thallose liverwort, to examine the maintenance of sexually dimorphic preadult traits. In Marchantia, sex determination is under genetic control of sex chromosomes (Bischler, 1986
). Marchantia inflexa females and males are sexually dimorphic in growth and asexual reproductive rates (McLetchie and Puterbaugh, 2000)
. Marchantia inflexa ranges from the southern USA to northern Venezuela (Bischler, 1984
). Caribbean populations are typically female-biased and include sexually reproducing females and males (McLetchie and Puterbaugh, 2000)
. Populations in the USA are typically unisexual and maintained solely through asexual reproduction (Schuster, 1992
).
Preadult M. inflexa reproduce asexually via the production of specialized asexual propagules. This makes M. inflexa especially suitable for studies of selection on asexual fitness because, unlike most plants, asexual reproduction and growth are distinct processes. We used a measure of asexual reproductive output as a metric for asexual fitness. Fitness in seed plants is typically some measure of total sexual reproductive output, i.e., number of sexually produced offspring contributed to the next generation. In clonal plants, clonality results in the production of new individuals and the spread of the genotype and thus is considered a measure of fitness (Fagerstrom, 1992
; Shaw and Beer, 1997
). Our measure of "asexual fitness" is in accord with the measure of gametophyte fitness proposed for mosses (Shaw and Beer, 1997
) and with clonal fitness for a meristem–meristem plant cycle (Fagerstrom, 1992
). It is not uncommon for bryophyte populations, and even species, to become entirely unisexual (Longton and Schuster, 1983), with the absence of males most common (Longton and Schuster, 1983; Stark, Mishler, and McLetchie, 1998
). In the case of unisexual bryophyte species, asexual reproductive output is the only estimate of fitness. Thus, both asexual and sexual reproduction contribute to an individual's lifetime fitness.
We focused on asexual reproductive output because all bryophytes display some mode of asexual reproduction, all have the potential for clonal expansion (During, 1990
; Newton and Mishler, 1994), and for many dioecious species, sexual reproduction is rare (Longton and Schuster, 1983). In dioecious clonal plants, females and males can allocate resources differently to sexual and asexual reproductive processes. Therefore, selection acting separately on asexual and sexual fitness components may have implications for the evolution and maintenance of sexual dimorphisms.
The purpose of this study was to uncover possible mechanisms for the maintenance of sexual dimorphisms in preadult traits via selection on asexual fitness. We used phenotypic and genotypic selection analyses (Lande and Arnold, 1983
; Rausher, 1992
) to estimate the magnitude and direction of selection on traits in female and male M. inflexa in two light environments. We asked the following questions: (1) Is sex-specific selection acting on asexual fitness of M. inflexa in such a way as to maintain sexual dimorphisms in preadult characters? (2) Is selection environment-dependent? (3) Is there sex-specific selection on plasticity of traits, independent of the traits themselves, that is consistent with the geographical distribution of the sexes? We hypothesized that selection on asexual fitness would be sex-specific in direction or magnitude because M. inflexa exhibits sexually dimorphic preadult traits. Given what appears to be a wider geographic distribution of females relative to males and the prevalence of female-biased populations (Bischler, 1984
; but see McLetchie and Puterbaugh [2000
] where sex ratio did not differ from 1 : 1), we predicted that selection on sexually dimorphic traits would be environment dependent. Further, we hypothesized that the more widely distributed sex, females, would be more plastic than males and that males might experience an environment-dependent cost of plasticity consistent with their limited geographical distribution. Although our focus was on asexual reproduction, we also included a limited analysis of selection on sexual fitness.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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To measure sex-specific and environment-dependent selection on pre-adult characters in M. inflexa, we grew replicates of female and male genotypes under two different light environments in a greenhouse. Stock plants used in this experiment were collected in June 1999 along Quare River in the Hollis Reservoir watershed on the island of Trinidad, The Republic of Trinidad and Tobago. We collected 40–43 vegetative tips from patches where only females or only males were expressing sex. The collected tips were presumed to be female or male, respectively. Each tip was collected from a different, randomly chosen patch along 2–3 km of stream length, and all patches were separated from each other by water. This collection method increased our likelihood of collecting individuals that were not members of the same genet. Field-collected thallus tips were individually transplanted into pots and maintained in a greenhouse on a capillary watering system as described below.
Alan Whittemore (New York Botanical Garden, Bronx, New York, USA) verified identification of the species and voucher specimens were deposited at the Missouri Botanical Garden (St. Louis, Missouri, USA, specimen nos. MO92113 and MO92115) and the National Herbarium of the Republic of Trinidad and Tobago (St. Augustine, Trinidad specimen no. TRIN34616, D. N. McLetchie, collector).
We planted gemmae, from randomly chosen female and male stock plants, into plastic pots (5.9 cm diameter and 2.7 cm deep) in Feburary 2000. We used a total of 16 female and 14 male genotypes because one of the presumed males was actually a female. Several gemmae per pot were planted on steam-autoclaved soil (collected from the North Farm, University of Kentucky, Lexington, Kentucky, USA), and these were thinned to 1 plant/pot 10 d after planting. We had a total of 420 pots, consisting of seven replicates per genotype across two shade treatments. Pots had individual lids fitted with either 55% or 73% shade cloth to provide treatments of high light or low light, respectively. Pots were placed on a single greenhouse table with locations randomized. Pots were placed directly on a capillary mat, one edge of which was submerged in a water trough, and filled with deionized water.
The planting day was considered day 0. We checked plants every 2 d beginning on day 16 to record dates that the mericells first split into two mericell regions (referred to as split), date of onset of asexual reproduction (referred to as cup onset), and date of first sex structure production (sex expression). Number of cups was counted on day 120 and number of sex structures counted on day 150. Photographs of plants were taken every 2 wk beginning on day 49 using a Nikon Coolpix 950 digital camera. Total green plant area was measured in square millimeters on a Macintosh computer using the public domain NIH Image program (developed at the U.S. National Institutes of Health and available on the internet at http://rsb.info.nih.gov/nih-image/).
Shade treatments were chosen based on McLetchie and Puterbaugh (2000)
and unpublished preliminary trials in which plants were grown successfully from gemmae through sexual maturation in 0%, 55%, 63%, and 73% shade (N. McLetchie, unpublished data). The low-light environment was chosen because, although levels of sex expression changed in relation to canopy closure in the field (N. McLetchie, unpublished data), under extremely low light plants have severely retarded growth rates (L. Fuselier, unpublished data).
Greenhouse temperatures ranged from 22°C at night to 25°C during the daytime, day length ranged from 11 h to 13.5 h throughout the year. In Trinidad, plants experience day lengths of 12 to 13 h, temperatures from 24°C to 26°C, on average, through the year (Muller, 1982
). To compare greenhouse light conditions to field light conditions we used hemispherical photographs, taken at low sun angles (to avoid scattering of light), though a 180° fish-eye lens (FC-E8) on a tripod-mounted digital camera (Nikon 950, Nikon Corporation, Tokyo, Japan). Images were analyzed using Scanopy (Reagent Instruments, Quebec City, Quebec, Canada) to estimate the amount of photosynthetically active photon flux density (PPFD, in moles per square meter per day) reaching a site. We used only direct PPFD and assumed no cloud cover. We used two images from field sites and a single greenhouse image. Photographs from the field were taken as part of an unrelated field experiment (N. McLetchie, unpublished data) and were chosen to represent the highest and lowest light levels among 20 microsites with M. inflexa. In the field, PPFD ranged from 19.03 to 5.23 mol·m–2·d–1. In the greenhouse, PPFD was 12.25 mol·m–2·d–1 under 55% shade and 7.34 mol·m–2·d–1 under 73% shade. Therefore, the light environments in the greenhouse were within the range of those experienced by plants at field sites.
Clonal fitness
The number of cups on day 120 was used as a metric for asexual fitness. This is an appropriate measure of asexual fitness because the number of cups on a plant is positively related to the number of gemmae produced (McLetchie and Puterbaugh, 2000)
and numbers of gemmae represent asexual reproductive output. The cup count on day 120 was late enough that plants in both shade treatments were well into cup production by this time.
Selection analyses
We used age at first split, age at onset of asexual reproduction, and area at day 49 in phenotypic and genotypic selection analyses to examine directional and nonlinear selection on female and male phenotypes (Lande and Arnold, 1983
). Previously, area, number of cups, and number of mericell splits were described as dimorphic in M. inflexa (McLetchie and Puterbaugh, 2000)
. Timing to first mericell split and plant area at day 49 represent differences in mericell production and early growth. Timing of cup onset is an important characteristic of asexual reproduction because gemmae production and dispersal are likely important to patch colonization.
Selection analyses take into account not only direct selection but also indirect selection that can obscure the influence of direct selection on a trait. Partial regression coefficients of standardized traits regressed onto relative fitness provide measures of direct selection, selection gradients (Beta), after controlling for correlations with other characters. The coefficient from a regression of a single trait on relative fitness provides a measure of total selection, the selection differential (s), which includes effects of indirect selection via correlated characters (Lande and Arnold, 1983
). Inclusion of quadratic terms in addition to standardized trait values permits the examination of patterns of direct (gamma) and total (g) disruptive and stabilizing selection. Additionally, a significant interaction between two traits indicates the action of correlative selection and indicates that the relationship between two traits is under selection. A selection differential statistically different from zero indicates that a trait has not reached its equilibrium value (Lande, 1980
; Lande and Arnold, 1983
).
Trait values were standardized by sex and shade treatment by subtracting the mean and dividing by the standard deviation of the measure. Fitness values were made relative within each sex and treatment by dividing by mean fitness in each sex-shade group. Data were not normally distributed, and residuals from preliminary analyses were likewise non-normal. Transformations did not improve normality. We used jackknife regression, a resampling method that is unbiased by non-normal data, via the program Freestat (Mitchell-Olds, 1989
) to generate more accurate measures of standard error and more reliable probability values for selection analyses. Correlations among standardized variables were examined using PROC CORR in SAS (1990)
but because the data were non-normal, probability values were considered approximate.
Phenotypic selection analyses included all plants (each gemmule) as "individuals," whereas in genotypic selection analyses, we used the genotype mean measure for the traits in each sex-shade group. Unlike phenotypic selection analyses, genotypic selection analysis reduces the likelihood that results are biased by environmentally induced correlations that impact fitness (Rausher, 1992
). We present two analyses from the same experimental data because of the limitations of both phenotypic and genotypic selection analyses. Our phenotypic selection analyses suffer the limitations of possible environmentally induced correlations and correlations due to genetic relatedness. Our genotypic selection analysis is the stronger and more conservative method but suffers the limitation of reduced power. We did not use genotypic selection data in nonlinear regression because of reduced power to detect differences. We interpret our results in light of both analyses and stress those results that are significant in phenotypic selection analyses and, whether significant or not, are of the same direction and magnitude in the genotypic selection analyses. Selection gradients and differentials significant in the phenotypic selection analyses alone, and with contradictory results in the genotypic selection analysis, cannot be definitively interpreted.
Sex-specific and environment-dependent selection
We used analyses of covariance (ANCOVA) within each shade treatment with relative fitness as the dependent variable, sex as a main effect, and the standardized plant traits as covariates to examine if selection was sex-specific. A significant sex-by-trait interaction indicated sex-specific selection (Donohue et al., 2001)
. To determine if selection was environment-dependent, we used similar ANCOVAs within each sex with shade as a main effect; a significant interaction between shade and trait indicated environment-dependent selection. Selection gradients were considered significantly different if for two gradients the mean ± 1 SE (generated from jackknife regression) did not overlap. ANCOVAs were conducted using SAS (SAS, 1990
).
Plasticity
We used plasticity of a trait and the mean genotype trait value in genotypic selection analyses to examine selection on plasticity of traits independent of the traits themselves (Donohue et al., 2001)
. We calculated plasticity for each genotype as the difference between values of the trait in the two shade treatments such that maximum plasticity would have a positive value. Relative fitness was calculated as the number of cups divided by the mean number of cups for the genotype across the two shade environments. We conducted selection analyses for each sex–shade combination. We used the same variables in an ANCOVA where relative fitness was the dependent variable, sex was the main effect, and standardized plasticity and trait values were covariates. An interaction between sex and trait plasticity indicated sex-specific selection on the plasticity of that trait independent of the trait itself.
Sexual fitness
We conducted additional phenotypic selection analyses with female plants that expressed sex in 55% shade and had sex structures on day 150 to examine the magnitude and direction of selection on sexual fitness and possible trade-offs between asexual and sexual reproductive processes. Number of sex structures present on day 150 was used as a metric for sexual fitness because this should be directly and positively related to spore production. Our measure of sexual fitness is potentially a representation of the number of sexually produced progeny contributed by a plant to the next generation. However, this metric for sexual fitness may be flawed because it is unknown how closely the number of sex structures translates into spore progeny. Split, area, cup onset, and timing to sex expression were standardized and regressed onto relative sexual fitness. We conducted a second analysis to examine the relationship between trait plasticity and sexual fitness by regressing the traits and their plasticities (excluding onset to sex expression) onto sexual fitness. Numbers of plants that expressed sex in 73% shade and number of males that expressed sex in 55% shade were too few to analyze. Finally, we conducted a second phenotypic selection analysis using standardized values of split, area, cup onset, and timing to sex expression regressed on relative asexual fitness. This permitted a comparison of the magnitude and direction of selection acting on sexual and asexual fitness components.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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for plants in 55% shade.
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). Our results are interpreted in the light of both analyses in that they were either significant in both or significant in the phenotypic selection analysis and of similar direction and magnitude in the genotypic selection analysis.
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Cup onset for females in 73% shade was not significantly correlated with other variables. However, cup onset in females in 55% shade was negatively correlated with area (Table 2). There may have been some correlation (albeit not significant) that influenced total selection for cup onset in 55% shade such that the differential was nonsignificant. There may also have been correlated variables that influenced total selection but were not included in the models.
Sex-specific selection
Sex-specific phenotypic selection for larger area and earlier cup onset was detected for plants in low light (Table 4). Under 73% shade, males experienced stronger direct and total selection for larger area compared to females, and direct selection for earlier cup onset was stronger for females than males (Table 4). When genotypic means were used in this analysis, these differences were not significant. Detection of differences using genotype mean phenotypes was confounded by small sample size in genotypic selection analyses. The direction and relative magnitude of selection on area and cup onset for females and males were similar in the genotypic and phenotypic analyses (Table 3). No significant differences in magnitude or direction of selection between the sexes were detected for plants in 55% shade (Table 4).
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Plasticity
Females tended to exhibit greater plasticity of cup onset ( = 56.97) compared to males ( = 39.64) but these differences were not significant in a t test (Fig. 1). In genotypic selection analysis, females exhibited a cost of plasticity in onset of asexual reproduction in 55% shade. There was no significant direct selection detected for other trait plasticities in either sex for either treatment (Table 5). When trait and trait plasticities were compared in an ANCOVA, results showed that females were under significantly greater direct selection than males for lower plasticity in timing to asexual reproduction in 55% shade (F = 7.02, P = 0.02; Table 5 and Fig. 1). Additionally, the magnitude of selection on plasticity in first mericell split differed between the sexes (F = 5.33, P = 0.03). Males with a plastic response for split in 55% shade were not favored by selection, whereas plastic split response was favored in females in 55% shade. However, neither of these selection differentials were significant in selection analyses. Probability values from the ANCOVA were used for this analysis because residuals were normally distributed. Sex-specific differences might have resulted as a statistical artifact of comparing a highly variable population (females) with a less variable population (males), but because the magnitude of direct selection for females was very high, the results likely indicate an actual pattern.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Lande and Arnold, 1983
).
Selection on preadult traits
Differences in trait means between the sexes detected in this study were consistent with McLetchie and Puterbaugh (2000)
and indicate that sexual dimorphisms do occur early in the life cycle in traits associated with asexual reproduction. This is significant because most studies of sexual dimorphism have been restricted to comparisons of adult life stages (Geber, 1999
). Age of onset of sexual dimorphism and the degree of correlation between selection on juvenile and adult traits are unknown for most dimorphic dioecious plants. Lloyd and Webb (1977)
suggested that sexual dimorphisms should not occur prior to sexual maturity. In female-biased populations of Rumex acetosa, sexual dimorphisms in phenology were not evident until shortly before sexual reproduction (Korpelainen, 1993
). Sexual dimorphisms in resource allocation in Silene latifolia were not evident until plants began investing in sexual reproduction (Delph and Meagher, 1995
). Our results corroborate these studies in that we found selection on asexual fitness favored monomorphism of the sexes in preadult characteristics. However, sexual dimorphisms were evident in plants prior to sexual reproduction. Preadult sexually dimorphic traits have been detected in angiosperms and bryophytes for characters such as germination ability (Newton, 1972
; Conn and Blum, 1981
; Cameron and Wyatt, 1990
; McLetchie, 1992
; Carrol and Mulcahy, 1993
; Purrington, 1993
; Shaw and Gaughan, 1993
; Taylor, 1994
; Shaw and Beer, 1999
; McLetchie, 2001
), embryo competitive ability (Conn and Blum, 1981
), and regeneration rates (Longton and Greene, 1979
). Our results suggest that the expression of preadult sexual dimorphisms in the face of opposing selection pressure may result from correlations with traits associated with sexual fitness in adults (Geber, 1999
).
Sex-specific selection
Selection should favor different phenotypic optima in the two sexes if natural selection maintained sexual dimorphism via sex-specific selection (Kohorn, 1994
; Geber, 1995
). At an equilibrium level of sexual dimorphism, selection differentials for traits in the two sexes are not significantly different from zero and each sex rests at its respective trait optimum (Geber, 1999
). Sex-specific selection has been implicated in the evolution of sexual size dimorphism in cases in which size is heritable and differences between the sexes evolve as a product of differential selection pressures and low genetic correlations between the sexes (Lande, 1980
; Slatkin, 1984
). High genetic correlations of traits between the sexes will slow the evolution of dimorphisms even under sex-specific selection regimes and will extend the period of time that suboptimal phenotypes are expressed in a population (Lande, 1980
; Meagher, 1984
). We detected sex-specific selection in preadult traits in M. inflexa, but the direction of selection in relation to asexual fitness did not drive the sexes toward different phenotypic optima. Although disruptive selection acted on cup onset in females in low light and in males on area in high light, given the strength and magnitude of directional selection on phenotypes, these patterns do not implicate different phenotypic optima for the sexes. Knowledge regarding the heritability of the traits considered in this study is lacking but must be elucidated to assess the impacts of genetic correlations in these traits between the sexes.
Environment-dependent selection
Environment-dependent selection and adaptive significance of light environments to sexually dimorphic clonal expansion traits may maintain sexual dimorphisms via spatial segregation of the sexes. In seed plants, light environment influences internode elongation and flowering response among other traits, and there is evidence that photomorphogenic shade avoidance responses are adaptive (Schmitt, McCormac, and Smith, 1995
; Dudley and Schmitt, 1995). In bryophytes, characteristics of the light environment are important in timing and speed of gametangial induction (Benson-Evans, 1964
; reviewed in Longton, 1990
), production of gemmae (Lockwood, 1975
), and thallus growth (Voth and Hamner, 1940
).
A number of studies on angiosperm sexual dimorphism document how adaptations that increase mating success influence responses to sexual selection such that vegetative sexual dimorphisms are correlated with environmental characteristics (Dawson and Geber, 1999
). For example, males of wind-pollinated taxa may specialize on drier habitats to increase chances of pollen dispersal (Dawson and Bliss, 1989
), whereas females may have higher reproductive success in protected areas. Differences in morphology related to habitat differences may be maintained as a result of the greater stresses imposed by reproduction (usually on the female) in the environment in which it occurs (Wallace and Rundel, 1979
). If females and males are better adapted to different environments, spatial segregation of the sexes and biased sex ratios along environmental gradients may result (Dawson and Bliss, 1989
; Dawson and Ehleringer, 1993
). Also, if the resource cost of reproduction is higher for one sex, that sex is expected to be under selection to increase resource uptake (Dawson and Geber, 1999
). Thus, biased sex ratios correlated with habitat characters may result because one sex specializes on high quality habitats and drops out of suboptimal habitats.
We detected environment-dependent selection in M. inflexa in relation to asexual fitness, but there were no patterns that suggested that one sex consistently outperformed the other sex in either light environment. The magnitude of selection on females for early onset of asexual reproduction differed across environments such that selection was stronger under low light than under high light. Male M. inflexa experienced greater total selection for larger area and early cup onset in low light compared to high light. Relative to plants in high light, males in low light expressed maladaptive cup onset and size phenotypes and females expressed a maladaptive cup onset phenotype. However, females tended to be slightly smaller than males in low light, a trend favored by selection. In nature, the frequency with which the sexes experience different light environments and the importance of additional environmental variables such as temperature and photoperiod will influence response to environment-dependent selection and may contribute to the spatial distribution of the sexes.
Plasticity
Costs of plasticity may arise in organisms through a physiological cost of being plastic in an environment (Van Tienderen, 1991
). When maintenance of trait plasticity is costly, nonplastic genotypes will be favored over plastic genotypes with the same trait mean. Sex-specific selection on plasticity and sex-specific costs of plasticity may influence the geographic distribution and contribute to spatial segregation of the sexes and skewed sex ratios. Because female M. inflexa are more widely distributed than males and populations are typically female-biased (Bischler, 1984
; but see McLetchie and Puterbaugh [2000
] where 1 : 1 sex ratios were found), we predicted that females were the more plastic of the sexes. Sex-specific selection for increased plasticity in females relative to males in traits associated with clonal expansion would provide evidence for an influence of plasticity on the spatial distribution of the sexes. We detected a cost of plasticity in onset of asexual reproduction in females that is incongruent with the wide distribution of females relative to males. When plasticity of traits was examined in the context of sexual fitness, females were under direct selection to increase plasticity in size. This is in accordance with our original hypothesis that females should display more plasticity, as evidenced by their wider geographic distribution, and that selection should act to increase plasticity in females.
Adult sex ratios of bryophyte are frequently skewed from a 1 : 1 ratio at the local patch and population levels. In liverworts and mosses, the ratios are most commonly female-biased (Longton and Schuster, 1983; Bowker et al., 2000
and references therein) and in some cases, entirely female (Longton and Schuster, 1983). In the southern USA, the northernmost reach of M. inflexa's range, some populations are entirely female or entirely male (Schuster, 1992
). If, as our results indicate, females are more plastic than males, females might thrive in environments where males fail. This pattern is in accordance with the distribution of sex ratios in the species and suggests a need for further research on adaptive plasticity and environmental correlates of sex ratios in M. inflexa populations.
Sexual fitness
Differences in resource allocation as a result of different costs of sexual reproduction between the sexes can lead to sexual dimorphism (Lloyd and Webb, 1977
; Charnov, 1982
; Lloyd, 1982
; Meagher and Antonovics, 1982b
; Meagher, 1984
; Shine, 1989
; Eppley, Stanton, and Grosberg, 1998
; Delph, 1999
). Physiological condition and future reproduction compete with current reproduction to produce negative phenotypic correlations and trade-offs among traits (Stearns, 1992
). A negative correlation between sexual and asexual reproductive output is predicted by life history theory, but clear-cut empirical demonstrations of this trade-off are few (Cheplick, 1995
; but see Sutherland and Vickery, 1988
; Reekie, 1991
; Westley, 1993
). We detected a trade-off between asexual and sexual fitness for female M. inflexa in high light. In high light, sexual fitness was highest for females that produced sex structures earlier. However, females that produced sex structures early also produced cups later. Late onset of cup production resulted in lower asexual fitness.
These opposing selective forces will interact to determine the pattern of selection experienced over an individual's lifetime (Schluter and Smith, 1986
; Schluter, Price, and Rowe, 1991
). In the context of sexual fitness, for females in high light, selection differentials for split, area, and asexual reproductive onset were not statistically different from zero, indicating that these traits were at their equilibrium. Selection on asexual fitness favored monomorphism of the sexes, but this was incongruent with patterns of phenotypic expression observed in nature. Thus, it appears that selection on sexual fitness, rather than asexual fitness, exerts more influence on phenotypic evolution of sexually dimorphic characters in females.
A greater relative influence of sexual fitness for females is expected because most sexually dimorphic traits in plants are believed to be a consequence of higher costs of reproduction incurred by females relative to males (Lloyd and Webb, 1977
). Higher costs of sexual reproduction lead to larger trade-offs with other traits for females (Putwain and Harper, 1972
; Lloyd and Webb, 1977
; Meagher and Antonovics, 1982b
). To compensate for these trade-offs, females may allocate more energy than males to leaf tissue early in life so they will have resources to allocate to sexual reproduction later (Delph, 1990
; Delph, Lu, and Jayne, 1993
). Unfortunately, our data for male allocation to sexual reproduction was limited, and we were unable to compare the sexes in terms of selection on both sexual and asexual fitness components. Our findings do however, underline the importance of investigating selection on components of fitness in different life stages of plants to reveal possible mechanisms for the maintenance of sexual dimophisms in dioecious species.
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FOOTNOTES |
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2 Author for reprint requests (lcfuse0{at}uky.edu
)
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P < 0.06
