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Reproductive Biology |
2Department of Ecology and Evolutionary Biology, U-3043, University of Connecticut, Storrs, Connecticut 06269-3043 USA
Received for publication January 31, 2003. Accepted for publication May 2, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Araceae • Arisaema triphyllum • Connecticut • environmental sex determination • jack-in-the-pulpit • local differentiation • plasticity • reciprocal transplant • sex change
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Warner, 1975
, 1988
). For example, individuals that are large will likely be female if female reproductive success increases more rapidly with increasing size than does male reproductive success. However, Charnov (1982)
pointed out that the size advantage hypothesis ignores the impact of size-dependent sex change on population sex ratios. If one sex is more common than the other, individuals of the rarer sex have a higher reproductive value than those of the common sex, because individuals of the rare sex contribute genetically to more offspring on average than do those of the common sex (Fisher, 1930
). For species that switch sex, population sex ratios may become biased in either direction and may change from season to season, but the rare sex in any given season has a higher reproductive value regardless of the direction of the bias. Thus, an individual's overall reproductive success depends on the reproductive decisions made by neighboring individuals. In short, reproductive efficiency under the size advantage hypothesis is best understood as including the population context in which individuals reproduce. As a result of selection for reproductive efficiency, the relationship between size and sexual expression may differ among populations that find themselves in different ecological circumstances.
Consider two populations of a species in which large individuals tend to be female and small individuals tend to be male. Suppose that in population A the median leaf area of individuals is 10 cm2, and in population B the median leaf area of individuals is 20 cm2. If all individuals with a leaf area greater than 10 cm2 are female, half of the individuals in population A will be female and half will be male. In population B, however, females will be over-represented. Thus, the rare sex reproductive advantage in population B will favor individuals that become female at a larger size. Indeed, a recent analysis by Charnov and Skuladottir (2000)
shows that the evolutionarily stable size of sex change will be larger in populations with a large maximum size than in those with a small maximum size. Therefore, we expect natural selection to cause population A and population B to become genetically differentiated for the relationship between sex and size. To determine whether this can be detected in natural populations, we investigated the relationship between size and sex in two populations of jack-in-the-pulpit, Arisaema triphyllum, in Connecticut, USA.
The genus Arisaema (Araceae) contains many species that exhibit some form of sex change, and among plant species, this genus has become a model system for looking at factors influencing sex determination (Schaffner, 1922
; Maekawa, 1924
, 1927
; Rust, 1980
; Treiber, 1980
; Policansky, 1981
, 1987
; Bierzychudek, 1982
, 1984a
, b
; Ewing and Klein, 1982
; Lovett Doust and Cavers, 1982
; Kinoshita, 1986
; Lovett Doust et al., 1986
; Takasu, 1987
; Clay, 1993
). The size advantage hypothesis appears to hold in those species where it has been tested (Arisaema triphyllum, Bierzychudek, 1984a
; Policansky, 1987
and A. dracontium, Clay, 1993
). Individuals switch from male to female with increasing size in some species (Policansky, 1981
; Maekawa, 1924
, 1927
; Kinoshita, 1986
; Takasu, 1987
), while in a many, like A. dracontium, individuals are male when small and monoecious when large, and the number of female flowers in an inflorescence increases with increasing size (Clay, 1993
). Several authors point out that populations of sex-changing species of Arisaema differ in mean size or sex ratio or both (e.g., Bierzychudek, 1984a
, b
; Kinoshita, 1986
; Schlessman, 1991
). Bierzychudek (1984a
, b
) noted that plants of A. triphyllum from one population were consistently larger when they became female than were those from a second population (280 cm2 leaf area at Brooktondale vs. 220 cm2 at Fall Creek). She further suggested that the differences between her study populations at Brooktondale and Fall Creek reflect genetic differences (Bierzychudek, 1984b
).
Sex expression in many plant and animal species is influenced by environment (e.g., turtles, Bull and Vogt, 1984
; other reptiles including crocodiles, Janzen, 1992
; Woodward and Murray, 1993
; some fishes, Conover, 1984
; and a variety of plants, Gregg, 1982
; Lloyd and Bawa, 1984
; Schlessman, 1986
, 1988
; Meagher, 1988
; Zimmerman, 1989
; Pannell, 1997
). Lovett-Doust and Cavers (1982)
showed that environment has a significant influence on sex expression Arisaema triphyllum. They transplanted individuals between two populations: one was male biased, the other female biased. The transplants did not retain the sex ratio of the site of origin. While Lovett-Doust and Cavers (1982)
conclude that sex change in A. triphyllum is function of environment, they suggest that the environment influences sex expression in the species primarily by influencing plant size.
In spite of 80 years of study on members of the genus Arisaema, however, the data currently available do not allow us to determine if differences among populations in the relationship between size and sex are due primarily to environmental effects or to genetic differences among the populations. In A. triphyllum, the best-studied example, we know that the relationship between size and sex can differ among populations, but we do not know whether this difference is a result of (1) variation in the availability of resources among sites, as suggested by Lovett-Doust and Cavers (1982)
, (2) genetic differences among populations as suggested by Bierzychudek (1984b)
, or (3) a combination of genetic differences and variation in resource availability among populations.
As suggested by Charnov and Skulladotir's (2000)
model, a species with environmentally sensitive sex determination could have highly skewed sex ratios in some environments unless there are genetic differences among populations (Bull, 1983
; Conover et al., 1992
). Under these circumstances, the reproductive advantage accruing to the rarer sex in the absence of genetic differences will cause natural selection to favor a sex-determination system that includes a genetic component (Bull, 1983
; Demas et al., 1990
; Schlessman, 1991
; Conover et al., 1992
; Girondot et al., 1994
; Pannell, 1997
; Girondot and Pieau, 1999
). Differentiation among populations of plant species has been profusely documented for traits with direct survival or reproductive value (see, for example Levin, 2000
). In animals with environmentally responsive sex determination, there is evidence for genetic variation in the response. For example, there is significant among-family variation for environmental sex determination in alligators and turtles (Rhen and Lang, 1998
), and Conover et al. (1992)
demonstrated that environmental sex determination responds to selection in laboratory populations of fish. We predict that selection in Arisaema triphyllum will result in genetic differentiation in the relationship between size and sex among populations as a buffer against highly skewed sex ratios.
We report here the results of a reciprocal transplant experiment designed to test this prediction. Our study had three parts. (1) Because of the variety of size measures that have been used in this and related species and because of the time-lag between sex determination and inflorescence expansion, we first determined whether plant size (measured as leaf area or pseudostem diameter) in the previous year, the current year, or a combination of both is the best predictor of sex in the current year. (2) Having identified a suitable measure of plant size, we then used this measure to explore differences in the relationship between size and sex in our study populations when grown in their native habitats. (3) Finally, we used reciprocal transplants between our study populations to determine the extent to which differences in the relationship between size and sex in our study populations are due to environmental site effects, to genetic differences between the populations, or to a combination of the two.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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To determine the relationship between size and sex of these populations in their native sites, reproductive status and current leaf size were recorded for each individual (see later for details on the size measurements). A separate subsample of individuals from each plot was collected and weighed before leaf expansion to estimate the mean corm mass for each population.
Reciprocal transplant experiment
In spring 1993, 60 individuals from each population were chosen at random from among those that were tagged in 1992. All were washed to remove the soil, gently hand dried to remove the water, and weighed. They were then randomly assigned to one of two treatments: reciprocal transplants were transplanted into the non-native site; and transplant controls were replanted in the spot from which they were collected. The reciprocally transplanted individuals from Dubos were randomly placed into the locations from which the Morneau reciprocal transplant individuals were removed, and vice versa. This resulted in each population having thirty transplant controls and thirty reciprocal transplants.
Size and sex expression of all tagged plants within each permanent plot was recorded from 1993 through 1996. Sex ratios for each population, broken down into Transplants and Controls, are reported in Table 5. Because sex for 1993 had already been determined when the experiment began, data for this year were used only to assess differences in mean size and sex ratios between the background native population, the 30 transplant controls, and the 30 reciprocal transplants within each of the two populations. Data collected from 1994 through 1996 were used to determine whether the functional relationship between size and sex differed between the populations, between the transplant control subsample and the native background population, and between the reciprocal transplant subsample and the non-native background population.
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Data analysis
Logistic regressions were performed using S-Plus version 4.0 (Venables and Ripley, 2002
) on a Pentium 166. As we were interested in the effect of size on sex expression, and sex is a categorical (binary) response variable, a generalized linear model (glm, family = binomial, link = logit) is the most appropriate method for analysis of the relationship between size and sex. Linear regressions and ANOVA's were done using SAS (Proc GLM) version 6.09 (SAS, 1995
) on an IBM 3090 mainframe.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2 = 0.0534; P > 0.25; df = 1; N = 199). Thus, individuals from the two populations show different relationships between size and sex when grown in their native population. Probability functions from a logistic regression of plant size and origin illustrate that individuals growing at the Dubos site have a smaller chance of being female at any particular size than do individuals growing at the Morneau site, i.e., individuals from Dubos tend to become female at a larger size than those from Morneau (Fig. 1).
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The transplant control and the native population did not differ detectably in the relationship between size and sex at either site (data not shown). Thus, our experimental protocols (i.e., digging plants, washing, weighing, and replacing them) had no detectable effect on the relationship between size and sex expression.
Any genetic differences between our study populations should be reflected in a significant effect of site of origin on sex expression. To investigate whether there are genetic differences between the populations in the relationship between size and sex (i.e., the probability of being female at any particular size), we analyzed a model with the following independent variables: pseudostem diameter, leaf size in the previous year, reproductive status in the previous year, the site at which an individual was currently grown (experimental site), and the site from which an individual was collected (site of origin), as well as all two-way interactions. Deleting nonsignificant interactions in a stepwise manner reduced this model to the one reported here (Table 4). The full and the reduced models were compared using an F test based on the residual deviance of each model (not shown). This test indicated that the full model was statistically indistinguishable from the reduced model presented in Table 4.
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The results presented in Table 4 also show a significant relationship between sex in the previous year and sex in the current year. Specifically, individuals that were male in one year were more likely to be female the next year than were females with the same leaf size and pseudostem diameter.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Maekawa, 1924
, 1927
; Rust, 1980
; Treiber, 1980
; Policansky, 1981
, 1987
; Bierzychudek, 1982
, 1984a
, b
; Ewing and Klein, 1982
; Lovett Doust and Cavers, 1982
; Kinoshita, 1986
; Lovett Doust et al., 1986
; Takasu, 1987
; Clay, 1993
). Nonetheless, previous studies of sex change in A. triphyllum have resulted in inconclusive observations about the relationship between size and sex. The size advantage hypothesis suggests that natural selection will favor sex change when one sex gains more by being large than does the other (Ghiselin, 1969
; Warner, 1975
, 1988
), but the gains either sex is able to accrue depend on the population sex ratio, as Charnov (1982)
pointed out. Thus, we expect natural selection to favor a sex-determination system that includes a genetic component and that long-established populations in different environments may diverge genetically in the relationship between sex and size (cf. Charnov and Skulladottir, 2000
). The purpose of our study was to test this hypothesis in two populations of A. triphyllum that are separated from one another by less than 15 km. Our study had three objectives: (1) to characterize the functional relationship between size and sex by determining the best predictor of current sex expression, (2) to use this measure of size to establish if differences exist between our study populations in the relationship between size and sex, and (3) to determine if the differences we find in that relationship are explained entirely by environmental influences or if there are also detectable genetic differences among populations.
Size and sex
Our results show that of our measures of plant size—current leaf size (the sum of four linear leaf measures, which is highly correlated with leaf area), previous leaf size, current pseudostem diameter, and previous pseudostem diameter—only one (previous pseudostem diameter) has no statistical relationship with current sex. As has been found in all previous studies on Arisaema triphyllum, females were significantly larger than males, and males were significantly larger than nonreproductive individuals. However, we found that the best overall predictor of current sex is a combination of pseudostem diameter and previous leaf size.
Pseudostem diameter is highly correlated with corm mass at the end of the preceding season, and the resources that were captured and stored in the previous year are reflected in the size and mass of the current year's corm as well as the predetermined sex expression (Vitt, 1997
). Similarly, previous leaf size is highly correlated with previous leaf area and therefore is a reflection of photosynthetic capacity during the period in which sex is determined (Vitt, 2001
). Thus, both the availability of stored resources and the ability to capture new resources appear to have an important effect on sex determination in Arisaema triphyllum. Unlike other plants in which reproductive structures are formed in a season prior to their expression, however, our data provide no evidence for a carryover effect that extends back further than the previous season (compare with Geber et al. [1997]
).
Vitt (2001)
showed that males and females have significantly different rates of photosynthesis, with males having a higher rate on a per unit area basis than females. Given the females much larger size, however, they have a greater carbon gain overall than males, concomitant with their greater costs of reproduction (Lovett Doust et al., 1986
). In males, there is no relationship between size and photosynthetic rate, while in females there is an inverse relationship early in the growing season (Vitt, 2001
). Given the overall patterns of carbon gain, sex expression and the usual male bias in sex ratio in the majority of natural populations (Richardson and Clay, 2001
), it is interesting to speculate on the overall strategy of sex change in this species. One intriguing possibility is that males, given their greater numbers, experience a greater variance in reproductive success than do females. An effective strategy for males would then be to gain as much carbon as possible, as quickly as possible, thereby increasing their chances of becoming female in the subsequent year. Indeed, our results show that individuals that were previously male had a higher probability of being female in the current year than plants with the same leaf size and pseudostem diameter that were previously female (Table 4). Thus, males of a given size are more likely to become female in the following year than females of the same size are to remain female. Bierzychudek's (1982)
results suggest that females are more likely to remain female than to become male in the subsequent year and males are more likely to remain male than to become female in the subsequent year. The apparent difference between our results and Bierzychudek's arises only because our analyses statistically control for the preexisting differences in male and female size.
The pattern of relationships between measures of size and current sex expression indicate that current sex expression is influenced more by the amount of resources available when sex is determined than by the amount of resources available when it is expressed. Vitt (1997)
showed that sex is determined by mid-growing season in the year prior to sex expression. This pattern also explains why there is a strong statistical relationship between leaf size and sex expression in the current season. Both sex expression in the current year and the size of the vegetative plant body are influenced by the stored resources available for growth. They are correlated because they are influenced by the same causal factors, not because current size is causally related to current sex expression. Consistent with this explanation, no relationship between current leaf size and current sex is detectable once differences in pseudostem diameter have been statistically controlled (Tables 3 and 4).
Population-level differences in the functional relationship between size and sex
Although the mean leaf size of plants differed between our two study sites, there was no detectable difference in sex ratio (see Table 5 for breakdown of population sex ratios for the study period). When populations differ both in size and sex ratio, no conclusion about the genetic or environmental basis of among-population differences is possible. When populations differ in size and have indistinguishable sex ratios, however, the populations most likely differ in their probability of being female at any given size, i.e., that the populations are genetically different for the relationship between size and sex. Our analysis of the relationship between size and sex in the background populations (Fig. 1) shows clearly that individuals from the Morneau site are more likely to be female at any given size than those from the Dubos site.
We have no historical data on either of our study sites, although each was second growth forest. The Dubos site appeared to be more mature, and portions of it were actively used for maple sugar production, an indication of average tree size, if not age. We therefore cannot determine how old our study populations might be, but it is likely that there have only been 3–4 generations at either site, given Bierzychudek's (1982)
estimate of a generation time of 25 years. Therefore, local differentiation in the size of sex change appears to have occurred rapidly in our populations.
Genetic vs. environmental effects on functional relationships
We used a reciprocal transplant experiment to determine whether genetic differences between the populations were responsible, at least in part, for the observed differences in the relationship between size and sex in our study populations or if the differences could be explained primarily by local site effects. Analyses of the results from this experiment show conclusively that both environmental and genetic factors influence sex expression in A. triphyllum. Sex determination in several other dioecious and monoecious plant species has also been shown to have both genetic and environmental components (Demas et al., 1990
; Girondot et al., 1994
; Pannell, 1997
; Ainsworth et al., 1998
). This is, however, the first study of which we are aware in which genetic and environmental influences on sex expression are mediated through their impact on the relationship between a third factor, in this case, size and sexual expression.
The overall relationship between size and sex expression is quite complex, and natural selection obviously acts to ensure reproductive efficiency in this character at the population level by mediating the effects of sex ratio. In effect, each population has undergone selection for a different size at which sex change should occur given the local environment. Bierzychudek (1984b)
addresses this by estimating the threshold size of sex change in her populations. Given the rapidity with which our populations appeared to respond, we may speculate that there is a good deal of heritable variation in this character. However, given that the sex expression is dependent upon resource acquisition, which in turn is dependent upon local, microclimate conditions, the ability to respond to stochastic variation in the short term is an excellent means of fine-tuning sex change as a strategy. Plasticity in the size of sex change allows the range of sizes of each sex to be somewhat broader than a strict genetically determined size at sex change might otherwise allow. Plasticity in this character therefore allows each individual to respond to the local conditions in which they find themselves, which is likely to be an important adaptation in a sessile organism. Interestingly, we found no evidence for genetic variation in the plastic response, as the site of origin by experimental site interaction is not significant.
Conclusion
We presented evidence that our study populations differ in the relationship between size and sex and that genetic differences between the populations are partly responsible for the differences observed in the intact populations. While we have no direct evidence that the genetic differences between populations upon which we report are the result of local adaptation, it is interesting to note that the direction of the difference we observe is what would be expected if natural selection were responsible for the differences between these two populations. In the population with larger plants (Dubos), individuals are more likely to be male at any given size than in the population with smaller plants (Morneau). Among-population genetic differences related to growth and survival have been extensively documented in plants. Our results show that even traits as tenuously related to immediate fitness as the relationship between size and sex may show the same pattern.
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FOOTNOTES |
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3 Present address: Chicago Botanic Garden, 1000 Lake Cook Road, Glencoe, Illinois 60022 USA (Telephone: 847-835-8268; Fax: 847-835-5484; e-mail: pvitt{at}chicagobotanic.org
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Bierzychudek P. 1982 The demography of jack-in-the-pulpit, a forest perennial that changes sex. Ecological Monographs 52: 335-351[CrossRef][ISI]
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Charnov E. L. U. Skuladottir 2000 Dimensionless invariants for the optimal size (age) of sex change. Evolutionary Ecology Research 2: 1067-1071[ISI]
Clay K. 1993 Size-dependent gender change in green dragon (Arisaema dracontium; Araceae). American Journal of Botany 80: 769.[CrossRef][ISI]
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