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0 USDA Forest Service, Rocky Mountain Research Station, Shrub Sciences Laboratory, 735 North 500 East, Provo, Utah 84606 USA; and 3 Department of Biological Sciences, Wayne State University, Detroit, Michigan 48202 USA
Received for publication May 22, 1998. Accepted for publication July 15, 1999.
ABSTRACT
We examined components of male and female reproductive success in
protogynous and protandrous sexual morphs of the heterodichogamous and
largely monoecious chenopod shrub Grayia brandegei. Percentage
femaleness of flowering stalks ranged from 0 to 37.6% female
(
= 15.5%) for protandrous plants and from 14
to 100% female ( = 55.8%) for
protogynous plants. Functional gender estimates based on ovule production
at two locations ranged from 23.0 to 31.8% female for the
protandrous morph, and from 65.3 to 77.0% female for the protogynous
morph. Realized gender estimates based on total seed production ranged in
value from 3.6 to 16.8% female for the protandrous morph and from
76.5 to 96.4% for the protogynous morph, depending on location and
year. Differences in reproductive success of the two morphs were largely
due to a reduction in the female function of protandrous plants.
Protogynous plants produced more female flowers per stalk and had a higher
percentage of seed-filled fruits than did protandrous plants. Differences
between sexual morphs were more pronounced in dry areas or years in which
overall seed production was minimal. Differential seed production between
morphs likely reflects temporal patchiness in environmental conditions,
particularly in water availability. The significance of these findings in
support of heterodichogamy as an evolutionary pathway to dioecy is
discussed.
Key Words: Chenopodiaceae • dichogamy • dioecy • floral sex ratio • Grayia brandegei • reproduction • spineless hopsage • temporal patchiness • Zuckia
Since
the late 1800s, numerous pathways by which dioecy may evolve have been
proposed. Particular attention has been given to the evolution of dioecy
from gynodioecy (Lloyd, 1974, 1980
; Charlesworth and Charlesworth,
1978a
;
Ross, 1978, 1980
;
Charlesworth, 1999
; Webb, 1999
), from monoecy (Lloyd, 1975,
1980
;
Charlesworth and Charlesworth, 1978b
; Charnov, 1982
; Ross, 1982
; Charlesworth, 1999
; Webb,
1999
), and from
distyly (Darwin, 1877
; Baker, 1958
; Ornduff, 1966
; Charlesworth and Charlesworth,
1979
;
Lloyd, 1979
;
Casper and Charnov, 1982
; Ross, 1982
; Muenchow and Grebus, 1989
; Webb, 1999
). The distylous pathway is
of particular interest because populations possessing distyly are already
dimorphic, often self-incompatible, and obligately outbreeding.
Consequently, factors other than inbreeding depression would likely have
provided the selective impetus for the transition from distyly to dioecy
(Lloyd, 1979
;
Bawa, 1980
;
Wyatt, 1983
;
Bertin, 1993
;
Webb, 1999
; but
see Ornduff, 1966
).
Heterodichogamy provides a
temporal analog of distyly (Faegri and van der Pijl, 1979
; Kubitzki and Kurz,
1984
; Lloyd
and Webb, 1986
;
Cruden, 1988
).
Dichogamy refers to a temporal separation of male and female sexual
functions [see Lloyd and Webb (1986)
, Cruden
(1988)
, Bertin (1993)
, and Bertin and Newman
(1993)
for discussions on the distribution and
evolutionary significance of dichogamy]. Heterodichogamous populations
consist of two mating types. Genetic control of this sexual system is
unknown, but data are consistent with a one-locus, two-allele model
(Gleeson, 1982
). In some species, such as the largely
wind-pollinated monoecious species of Juglans, Corylus, and
Acer, one morph is protogynous (pistillate flowers become
receptive several weeks prior to staminate anthesis) and the other
protandrous (stigmas of pistillate flowers do not become receptive until
after pollen is shed). In other, bisexually-flowered species, both morphs
are either protogynous (as in certain members of the Lauraceae and
Annonaceae) or protandrous (the genus Zizyphus in the Rhamnaceae),
but open on different days or at different times during the day. In either
case, flowering phases of the two mating types are synchronous and
reciprocal, facilitating cross-fertilization between sexual morphs (Stout,
1928
; Galil and
Zeroni, 1967
; de
Jong, 1976
;
Kubitzki and Kurz, 1984
; Lloyd and Webb, 1986
; Rogstad, 1994
). Such a temporal
separation in sexual functions that results in obligate outcrossing has
been referred to as a "temporal dioecism" (Cruden and
Hermann-Parker, 1977
; Cruden, 1988
).
Heterodichogamy as an
evolutionary pathway to dioecy has been largely ignored. Darwin
(1877)
briefly
referred to the possibility, saying "...their conversion into a
dioecious condition would probably be much facilitated, as they already
consist of two bodies of individuals, differing to a certain extent in
their reproductive functions." Others have speculated on the
possibility, noting evolutionary trends toward dioecy in families
containing heterodichogamous species (de Jong, 1976
; Kubitzki and Kurz,
1984
;
Pendleton, 1986
; Pendleton et al., 1988
). Lloyd
(1980)
also included a brief discussion on this little-known but intriguing
possibility in his paper on evolutionary pathways. More recently, the
discovery of a tetramorphic sexual system in Thymelaea hirsuta,
consisting of protandrous and protogynous hermaphrodites as well as
unisexual male and female plants, led researchers to readdress the
possibility of such a pathway (Dommée, Bompar, and Denelle,
1990
; Shaltout
and El-Keblawy, 1992
; Dommée et al., 1995
; El-Keblawy, Lovett
Doust, and Lovett Doust, 1996
). A similar tetramorphic system has been
described for spinach (Wachocki, 1992
).
The inherent appeal of
heterodichogamy as a pathway to dioecy lies in the relative ease with which
the transition could be achieved. De Jong (1976)
postulates an evolutionary
progression in the genus Acer from duodichogamy (a flowering
sequence of male-female-male) in the more primitive species through
heterodichogamy, present in roughly half of the species, to dioecy proper
in advanced species. Each transition involves a reduction in the number of
sexual stages.
Although there has been speculation concerning an
evolutionary pathway from heterodichogamy to dioecy, few quantitative
reproductive data are available for natural populations of
heterodichogamous plants. Available data come largely from planted
populations or cultivar studies (Wood, 1934
; Gleeson, 1982
). Recent studies on natural populations
of Thymelaea hirsuta, however, indicate substantial specialization
of protandrous and protogynous morphs (Dommée, Bompar, and Denelle,
1990
; Shaltout
and El-Keblawy, 1992
; Ramadan et al., 1994
; Dommée et al.,
1995
;
El-Keblawy, Lovett Doust, and Lovett Doust, 1996
).
Previously,
we reported the first known case of heterodichogamy in the Chenopodiaceae
(Pendleton et al., 1988
). In the course of that study, we
observed that floral sex ratios of the two mating types differed
substantially. Here, we examine the sexual specialization of protogynous
and protandrous morphs in one population of G. brandegei. Various
components of male and female reproductive success, including functional
gender, are presented for two groups of plants growing on different
substrates. Reciprocal dimorphic populations, such as heterodichogamy and
distyly, provide a singular means of studying sexual specialization using
functional gender. If illegitimate (self or within-morph) fertilizations
are shown to be of negligible frequency, then it follows that the female
function, or femaleness, of one morph is equal to the maleness of the other
(Lloyd, 1979
).
Functional gender can therefore be easily estimated using either floral sex
ratios or seed production totals. The probable effects of temporal
patchiness in contributing to observed specialization and possible
relationships to a dioecious pathway are
discussed.
MATERIALS AND METHODS
Grayia
brandegei is a small anemophilous shrub that occurs in the Colorado
River drainage of Utah, Arizona, New Mexico, Colorado, and Wyoming (Stutz
et al., 1987
). It
is found in isolated populations on heavy clay substrates of decomposing
shale that are often saline and seleniferous (Welsh et al., 1993
). Diploid and tetraploid
chromosome races have been reported (Stutz et al., 1987
).
Reproduction in
G. brandegei is primarily sexual, but a limited amount of
vegetative spread also occurs. Populations are largely monoecious and
heterodichogamous, with occasional unisexual individuals on which the
second sexual function fails to develop. Protandrous and protogynous
matings types occur in approximately equal proportions. Temporal separation
of staminate and pistillate flowering phases is complete within individual
plants. Branches flower synchronously, with a one to several day gap
between sexual functions. Little temporal overlap of sexual functions
occurs among plants of the same mating type; estimates of 4.9% and
14.2% for protandrous and protogynous morphs, respectively, were
previously reported (Pendleton et al., 1988
). These figures are likely an
overestimation for reasons discussed in the previous paper. The fruit is a
single-seeded utricle enclosed within a pair of foliaceous winged bracts
(Welsh et al., 1993
).
The taxonomic status of
Grayia brandegei is uncertain. Although first described as a
congener of G. spinosa (Gray, 1876), others have argued for its
inclusion within the genus Atriplex (Collotzi, 1966
). More recently, Welsh
(1984)
proposed that G. brandegei be combined with Zuckia
arizonica to form Zuckia brandegei. Through close
examination, we have observed that Zuckia arizonica shares the
same sexual system as Grayia brandegei, whereas G.
spinosa is monoecious, but not heterodichogamous. Breeding systems in
the genus Atriplex range from monoecy to dioecy and trioecy
(McArthur et al., 1992
; Freeman et al., 1993, 1997
), but heterodichogamy in
Atriplex has not been observed. In our view, Grayia
brandegei is most closely related to Zuckia arizonica, but
the exact status of this species within the taxonomic group could best be
clarified through the use of current molecular genetic techniques.
In this study, we examined a tetraploid population located 4 km northwest of Sterling, Utah (39°15' N, 111°46' W, 1850 m elevation), on a steeply sloping, weathered, shale substrate of the Colton and Green River formations. Vegetation consists almost entirely of Grayia brandegei on site, blending into pinyon-juniper (Pinus edulis-Juniperus osteosperma) and cliffrose (Cowania stansburiana) communities at the periphery.
Two adjacent areas within the population were marked off for study purposes: one (Red) was located on red-colored shale of the Colton formation and measuring ~11.3 x 12.5 m (141 m2) and the second area (White) was located on a white calcareous substrate also of the Colton formation and measuring 7.2 x 9.4 m (68 m2). We subsequently found that the White area was located on the tailings of an old mine. Plants within each area were mapped and numbered. In cases where it was difficult to determine what constituted an individual plant, whether one large plant whose lateral branches had become buried or several separate plants, we treated each entity as a separate plant. A total of 145 plants were mapped, 78 in the White area and 67 in the Red.
Plants were classified as protogynous or protandrous based on their flowering phenology. Twelve unisexual individuals were classified based on whether their flowering occurred in accordance with the protogynous or protandrous time frame. Many of these (6) had very few flowering stalks and few flowers per stalk, suggesting that resources available for reproduction were limited.
Reproductive output
In 1985, pistillate and
staminate flowers were counted on a minimum of three stalks taken from each
of the 78 plants that flowered that year. The stalks were taken from
different sides of the plant. The total number of flowering stalks per bush
was also recorded. Floral counts were made using a dissecting microscope.
For protogynous plants, only one collection of stalks was needed to
determine both pistillate and staminate numbers, since flower initials of
both types are present at the beginning of the flowering season. In
contrast, female flowers on protandrous plants delay initiation and
development until after male flowers begin to abscise, necessitating
collection of flowering stalks on two separate occasions during the season.
The first collection was used for staminate counts, the second for
pistillate counts. Pollen counts were made using a compound microscope on
anthers collected from four protogynous and four protandrous
plants.
In late September 1985, all fruits from each plant were harvested, cleaned, and weighed. Two hundred fruits per plant were then selected at random, weighed, and the number of filled fruits recorded. If fewer than 200 fruits were available, all fruits were counted and used. Seeds obtained from the 200-fruit sample were weighed and subsequently germinated at room temperature on wet filter paper after first soaking the seeds in distilled water for 10 min. The number of germinating seeds was recorded at regular intervals during a 10-d period.
In the fall of
1986, all fruits were collected from each of the 56 plants growing in the
Red area that flowered that year. The fruits were treated as above, except
the seeds were germinated at 25°C, and the viability of seeds not
germinating was determined by tetrazolium assay (Association of Official
Seed Analysts, 1988
).
Functional
gender
The functional genders for protandrous and protogynous plants
were determined using the formulas Lloyd (1979)
developed for heterostylous populations.
In its simplest form, the equation describing functional gender for the
protandrous morph is given as
a represents
the average femaleness of all protandrous plants; na
and ng are the number of protandrous and protogynous
plants, respectively; and
a and
g are the mean number of ovules or seeds produced by protandrous and protogynous plants, respectively. A parallel expression describes the protogynous morph. For these equations, illegitimate and self-fertilization are assumed to be negligible, and the female fitness of one sexual morph becomes equivalent to male fitness of the other.
If illegitimate or within-sexual morph fertilization is included, the equation for functional gender of the protandrous morph becomes
In Grayia, self-fertilization is assumed to be negligible because of the complete temporal separation of sexual functions of individual plants. The overlap of sexual functions among plants of the same sexual morph, and consequently, the opportunity for illegitimate fertilization, have been estimated at 4.9% for the protandrous morph and 14.2% for the protogynous morph (Pendleton et al., 1988
).
Data analysis
All statistical tests were run using SAS for the personal computer (SAS, 1989
). Total numbers of staminate and pistillate flowers were calculated by SAS on a per plant basis. Means of all reproductive measures reported were obtained using the Summary procedure. Reproductive data were analyzed using all values in the data set, as well as with unisexual plants excluded. Analyses were carried out using a dual analytical approach recommended by Conover and Iman (1976)
. Data were analyzed both parametrically, using a two-sample t test, and nonparametrically, using a t test on the data rankings (equivalent to the Wilcoxon-Mann-Whitney test; see Conover and Iman, 1981
). The two areas (White and Red) were treated separately. In most cases, the two test procedures gave similar results. The statistical results reported below all result from the nonparametric test procedure, with one exception. A standard parametric t test was used in analyzing pollen grain data because of the low number of observations. A sequential Bonferroni test (Rice, 1989
) was used to verify the significance of univariate results.
RESULTS
Reproductive output
Floral sex ratios (percentage femaleness) of protandrous and protogynous plants were significantly and consistently different throughout the study, regardless of whether or not unisexuals were included in the analysis. Percentage femaleness of flowering stalks (pistillate flowers/pistillate and staminate flowers), with unisexuals included, ranged from 0 to 37.6% for protandrous plants and from 14.0 to 100% for protogynous plants (Fig. 1). Flowering stalks of protandrous plants averaged 15.8% female in the Red area and 15.3% female in the White area. Protogynous plants averaged 61.2% female in the Red area and 49.7% female in the White area (Table 1). Overall means for the two morphs were 15.6 and 55.8%, respectively. Differences in percentage femaleness of flowering stalks were highly significant for both areas. The number of flowering stalks per plant did not differ significantly between sexual morphs (Table 1).
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The two sexual morphs also differed in the average number of fruits and seeds matured per flowering stalk. In 1985, protandrous plants averaged 2.1 fruits and 0.1 seeds per stalk in the Red area and 8.4 fruits and 0.5 seeds per stalk in the White area. Protogynous plants averaged 12.8 fruits and 2.2 seeds per stalk in the Red area and 27.7 fruits and 2.7 seeds per stalk in the White area. Overall means for 1985 were 4.2 fruits and 0.3 seeds per stalk for protandrous plants and 19.8 fruits and 2.6 seeds per stalk for protogynous plants. These differences were highly significant (t = -3.6419, df = 53.1, P = 0.0006 and t = -3.0886, df = 42.9, P = 0.0035, respectively).
Differences in reproductive output of the two sexual morphs were due primarily to the female sexual function, that is, in the number of female flowers per stalk and in the number of seeds matured per female flower. The greatest differences between sexual morphs were observed in plants growing in the Red area in 1985, where protogynous plants produced over twice the number of female flowers, six times the number of fruit, and many times the number of mature seeds per flowering stalk as did protandrous plants (Table 1). Protogynous plants in this area had a higher proportion of their flowers develop into fruit (40 vs. 18.7%) and a higher percentage of fruit containing seeds (18.8 vs. 5.4%) than protandrous plants from the same area. These differences in reproductive output of the two morphs were highly significant (Table 1).
Plants in the White area produced roughly twice as many female flowers and fruits as did those in the Red area (Fig. 2). For example, protogynous plants in the White area averaged a total of 10 695 female flowers, 14 907 male flowers, 5854 fruits, and 582 seeds per plant as compared with 4243 female flowers, 6169 male flowers, 2025 fruits, and 310 seeds for protogynous plants in the Red area. Differences in reproductive output of the two sexual morphs were less pronounced in the more productive White area. The average number of female flowers per stalk was still significantly greater for protogynous plants (Table 1). However, differences in the number of fruits and seeds per stalk were only marginally significant at best. No significant difference between morphs was observed in either the proportion of flowers setting fruit or in the percentage of filled fruits (Table 1).
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The quality of seed produced by the two morphs, as measured by fruit mass, seed mass, and seed germination rate, was not significantly different. Analysis of the 1985 data found no significant differences between sexual morphs in seed germination rate, fruit mass, or seed mass, although there was a slight trend for protandrous seeds to be heavier (Table 1). Univariate analyses on the 1986 data similarly showed no difference in fruit mass (Table 1), but did show a marginally significant difference in seed mass and germination rate. The sequential Bonferroni test, however, could not exclude the possiblity of a type II error in the latter case. Viability of seed produced in 1986, determined by tetrazolium assay, also did not differ significantly between morphs, averaging 94.9% viable seed for the protandrous morph and 97.9% viable for the protogynous morph (t = -0.7126, df = 19.3, P = 0.4846).
Functional gender
Functional gender, as a measure of femaleness, may be determined using either ovules (potential gender) or seeds (realized gender). The preferred method from a fitness standpoint is to use seeds, as this more closely approximates reproductive success (Lloyd, 1980
). In this way, functional gender becomes a measure of the mean fitness gains for each morph through the male and female functions.
Functional gender in this study was calculated with and without the inclusion of illegitimate fertilization. The actual gender for the population most likely falls between these two estimates for the following reasons: (1) illegitimate pollen must compete with the more plentiful legitimate pollen for access to ovules, (2) self pollen may fertilize proportionately fewer ovules due to incompatibility or slower growing pollen tubes, and (3) seeds produced through illegitimate fertilization may be less fit. Thus, the two provide conservative and liberal estimates of the degree of sexual specialization exhibited by the two sexual morphs.
Using ovule numbers (number of female flowers), functional gender for the protandrous morph was between 29.0 and 31.8% female in the Red area in 1985, and between 23.0 and 25.5% female in the White area (Table 2). Gender estimates for the protogynous morph fell between 65.3 and 71.0% female in the Red area, and between 70.2 and 77.0% female in the White area. Mean gender estimates for the two areas combined were 27.0–29.7% female for the protandrous morph and 67.6–73.8% female for the protogynous morph. Gender estimates from the two areas were remarkably similar and indicate some degree of specialization at the time of flowering.
Functional gender, based on seed production totals, reflected a greater dichotomy in fitness gains of the two morphs through male and female sexual functions. Nearly 90% of the total seed produced in the White area in 1985 was produced by the protogynous morph (Table 2). The resulting gender estimates for this morph are 79.9 and 89.7% female, depending on the degree to which protogynous plants also fathered some of the seed. In the Red area, the protogynous morph produced 96% of the total seed production, with gender estimates of 84.9 and 96.4% female. Gender estimates for the protandrous morph were 3.6–4.2% female in the Red area, and 10.3–11.7% female in the White area. Seed-based gender estimates for the Red area in 1986 were somewhat less extreme, however the protogynous morph still produced 83.5% of the total seed crop. In all cases, a considerable degree of sexual specialization present at the beginning of the flowering season was accentuated in the widely divergent seed production totals of the two sexual morphs at the end of the season.
DISCUSSION
Much of the discussion concerning the evolution of dioecy has focused on the multiplicity of pathways by which dioecy may evolve. Sexual specialization of dimorphic populations, particularly in genera where a gradation exists, has been used to illustrate possible transitional pathways from one sexual system to another (Freeman et al., 1997
). Estimates of reproductive function, including use of quantitative formulas, have been used to detect sexual specialization of reproductive morphs in phenotypic gynodioecious, monoecious, and heterostylous genera (Lloyd, 1979, 1980
; Webb, 1979
; Wyatt, 1983
, and references therein). Here we found that by comparing functional gender at different points in the reproductive process, we can get an estimate of the relative strength of any selective force operating between flower initiation and seed maturation.
In G. brandegei, all measures of reproductive function indicate a specialization in sexual function by the two morphs. Potential gender estimates based on ovule number reveal considerable specialization at the beginning of the season. Differences in realized gender, based on seed production, were even greater. In 1985, sexual morphs in the Red area were functionally close to dioecy by the end of the season. A similar pattern of divergence, though less extreme, was exhibited in the White area in 1985 and in the Red area in 1986.
The above difference in sexual function of the two morphs reflects a reduced ability of protandrous plants to set fruit. Female flowers of protandrous plants set a lower percentage of fruit and had a lower percentage of their fruits filled than did those from protogynous plants. Protogynous plants produced adequate amounts of pollen during the second flowering period, but fitness gains through the male function were constrained by the limited number of available ovules. It would appear, therefore, that selective pressure on the female function is driving sexual specialization in this population, and that the strength of that selection varies with location and year. If, as hypothesized by Bateman (1948)
, the female function is frequently more limited by resources, then it would be expected that the female function would experience greater selective pressure in a resource-limited environment (Delph, 1990
; Dawson and Geber, 1999
). Our data support this conclusion.
The failure of protandrous plants to mature seed is likely attributable to increased moisture stress occurring during the later season. Most precipitation in the northern and central portions of the Great Basin cold desert comes in the form of winter snowfall (West, 1983a
; Caldwell, 1985
). Infiltration from summer storms, particularly high-intensity storms, are of minimal value to plant growth (West, 1983b
; Caldwell, 1985
). Complete separation of sexual functions in Grayia brandegei results in protandrous plants maturing fruits several weeks later than protogynous plants under conditions of reduced moisture availability. Evidence supporting this argument is apparent in the observed correlation between moisture availability and seed production totals. The White area, which was located just below a seep, produced more than twice as much seed as the dryer Red area. In 1986, winter and early spring precipitation was 28% greater than in 1985 (NOAA, 1985, 1986
), resulting in a threefold increase in seed production on the Red area.
A decline in female function as the season progresses or in years of lower overall flowering has been reported in other temperate-zone species (Stephenson, 1981
; Thomson and Barrett, 1981
; Ashman and Baker, 1992
, and references therein; Thomas and LaFrankie, 1993
). Numerous studies report that a lack of soil moisture may be particularly detrimental to the female function (Freeman and McArthur, 1982
; Freeman and Vitale, 1985
; Vitale and Freeman, 1986
; Dawson and Bliss, 1989
; Delph, 1990
; Mazer and Schick, 1991
; Ashman and Baker, 1992
; Freeman et al., 1993
; Thomas and LaFrankie, 1993
). Environmental stresses, including inadequate soil moisture and extremes in temperature, are often associated with shifts toward maleness (Freeman, Klickoff, and Harper, 1976
; Freeman, Harper, and Charnov, 1980
, and references therein). In dioecious species, this may result in partial niche separation, in which males are proportionately more common on more stressful sites (Putwain and Harper, 1972
; Freeman, Klikoff, and Harper, 1976
; Onyekwelu and Harper, 1979
; Cox, 1981
; Fox and Harrison, 1981
; Parrish and Bazzaz, 1982
; Freeman and Vitale, 1985
; Vitale and Freeman, 1986
; Vitale et al., 1987
; Bierzychudek and Eckhart, 1988
; Dawson and Ehleringer, 1993; Freeman et al., 1993
; Dawson and Geber, 1999
; Geber, 1999
).
The possibility of a heterodichogamous pathway to dioecy has heretofore been based primarily on conjecture. Gender specialization between sexual morphs of heterodichogamous species has seldom been addressed. Schuster (1924)
observed that filbert strains that produced a lot of pollen were generally poor nut producers. Gleeson (1982)
found no difference in reproductive efforts of protandrous and protogynous Juglans hindsii. However, heterodichogamy in the Juglandaceae appears to be stable and is the only breeding system known in that family (Gleeson, 1982
). In tetramorphic Thymelaea, protandrous plants produce large amounts of fruit similar to amounts produced by female plants. Protogynous plants are functionally closer to males, leading to the conclusion that male and female plants may have evolved from protogynous and protandrous plants, respectively (Dommée, Bompar, and Denelle, 1990
; Dommée et al., 1995
; El-Keblawy, Lovett Doust, and Lovett Doust, 1996
). In Spinacea oleracea var. americana, the reverse is true; males likely evolved from protandrous hermaphrodites and females from protogynous hermaphrodites (Wachocki, 1992
; Miglia and Freeman, 1996
).
Strong selection against the female function of protogynous plants may result in the development of androdioecy as a transitional stage in the evolution to dioecy. Lloyd briefly speculated on the possibility of such a stage in his 1980 paper on pathways. The concept was apparently based on the observations of de Jong (1976)
, who described a continuum of sexual systems in Acer, from heterodichogamy to dioecy. Heterodichogamous species in the genus consist of protogynous individuals intermixed with either duodichogamous, protandrous, or male plants. Species that are intermediate in sexual expression include those in which protogynous individuals are partly replaced by females, and the evolution of protandrous plants to males is nearly complete. In Grayia, a similar pattern is observed. Floral sex ratios of protandrous plants are markedly skewed to the male function, whereas floral sex ratios of protogynous plants are more balanced. Androdioecy, if it did constitute a transitional stage, would apparently only occur in wind-pollinated species.
In genetic models, the loss of one sexual function by an outbreeding hermaphrodite is assumed to result in a 50% reduction in reproductive fitness that must be countered by a twofold increase in offspring quality or quantity. (Charlesworth and Charlesworth, 1978a, b
). In Grayia, loss of one sexual function would reduce reproductive fitness by as little as 3.6–16.5%. This potential loss in fitness could be at least partially compensated for through the reallocation of these resources to the retained sexual function (Darwin, 1877
; Charnov, 1982
). Offspring quality may also be affected by the quality of the maternal resource environment (Stephenson, 1981
), with those seeds produced under more resource-abundant conditions outperforming those produced under less favorable conditions. Together, these factors may be sufficient to overcome the twofold penalty and allow dioecy to evolve.
Conversely, some degree of sexual lability may be maintained within the population. Sexual lability in the Chenopodiaceae is well documented (see McArthur, 1977
; Freeman, McArthur, and Harper, 1984
; Freeman and Vitale, 1985
). Muenchow and Grebus (1989) assert that very small gains in fitness may be sufficient to maintain the biomass expenditures of a second sexual function. Growth and reproduction of perennial species in the salt desert vegetation type can vary as much as 800%, depending on the timing and amount of precipitation (West, 1983c
). During wet years or years of low seed predation, protandrous plants may be more successful at maturing seed. Fitness gains through the second sexual function in these optimal years may well be sufficient to maintain some level of bisexuality.
In summary, the data presented here strongly support the possibility of a heterodichogamous pathway to dioecy. Protogynous and protandrous sexual morphs of Grayia brandegei are highly specialized in sexual function, apparently due to selection against the female function of protandrous plants. Under harsh environmental conditions, loss of the second sexual function would result in only a 3.6% loss of fitness, which could be partially mitigated by reallocation of those resources. Clearly, there exists the potential for dioecy to evolve. However, in a highly variable environment such as the salt desert, sexual lability may be adaptive (Lloyd, 1984; Freeman et al., 1993, 1997
; El-Keblawy et al., 1995
). Heterodichogamy (bisexuality) may be maintained in this species by relatively small fitness gains accrued by the second sexual function during optimal years.
Further research needs are twofold. First, manipulative studies wherein resource levels are controlled and reproductive output monitored are necessary before the evolutionary status of this species can be clearly defined. Second, additional studies on the genetics of heterodichogamy are also warranted. Currently, we have rooted cuttings from plants of known gender. By accelerating the flowering time of some ramets, both self-fertilization and within-morph crosses could be achieved.
FOOTNOTES
1 The authors thank Clyde Blauer and Susan Garvin for assistance in data collection; Robert Cruden, Geraldine Allen, and John Graham for reviews of the manuscript; and Jeff Vitale, Anton Hough, William Moore, and John Zawiskie for comments on an earlier draft. This research was facilitated in part by the Pittman-Robertson Wildlife Habitat Project W-82-R. 
LITERATURE CITED
Ashman, T.-L., and I. Baker. 1992 Variation in floral sex allocation with time of season and currency. Ecology 73: 1237–1243. [CrossRef][ISI]
Association of Official Seed Analysts. 1988 Rules for testing seeds, 1988 revision. AOSA, Beltsville, Maryland, USA.
Baker, H. G. 1958 Studies in the reproductive biology of West African Rubiaceae. Journal of the West African Science Association 4: 9–24.
Bateman, A. J. 1948 Intrasexual selection in Drosophila. Heredity 2: 349–369.
Bawa, K. 1980 Evolution of dioecy in flowering plants. Annual Review of Ecology and Systematics 11: 15–39.
Bertin, R. I. 1993 Incidence of monoecy and dichogamy in relation to self-fertilization in angiosperms. American Journal of Botany 80: 557–560. [CrossRef][ISI]
———, and C. M. Newman. 1993 Dichogamy in angiosperms. Botanical Review 59: 112–152. [CrossRef][ISI]
Bierzychudek, P., and V. Eckhart. 1988 Spatial segregation of the sexes in dioecious plants. American Naturalist 131: 901–910. [CrossRef][ISI]
Caldwell, M. M. 1985 Cold desert. In B. F. Chabot and H. A. Mooney [eds.], Physiological ecology of North American plant communities, 198–212. Chapman and Hall, New York, New York, USA.
Casper, B. B., and E. L. Charnov. 1982 Sex allocation in heterostylous plants. Journal of Theoretical Biology 96: 143–149. [CrossRef]
Charlesworth, B., and D. Charlesworth. 1978a A model for the evolution of dioecy and gynodioecy. American Naturalist 112: 975–997. [CrossRef][ISI]
Charlesworth, D. 1999 Theories of the evolution of dioecy. In M. A. Geber, T. E. Dawson, and L. F. Delph [eds.], Gender dimorphism in flowering plants, 33–60. Springer-Verlag, New York, New York, USA.
———, and B. Charlesworth. 1979 A model for the evolution of distyly. American Naturalist 114: 467–498. [CrossRef][ISI]
———, and ———. 1978b Population genetics of partial male-sterility and the evolution of monoecy and dioecy. Heredity 41: 137–153. [ISI]
Charnov, E. L. 1982 The theory of sex allocation. Princeton University Press, Princeton, New Jersey, USA.
Collotzi, W. W. 1966 Investigations in the genus Grayia, based on chromatographic, morphological, and embryological criteria. Master's thesis, Utah State University, Logan, Utah, USA.
Conover, W. J., and R. L. Iman. 1976 On some alternative procedures using ranks for the analysis of experimental designs. Communications in Statistics—Theory and Methods A 5: 1349–1368.
———, and ———. 1981 Rank transformation as a bridge between parametric and nonparametric statistics. American Statistician 35: 124–133. [CrossRef][ISI]
Cox, P. A. 1981 Niche partitioning between the sexes of dioecious plants. American Naturalist 117: 295–307. [CrossRef][ISI]
Cruden, R. W. 1988 Temporal dioecism: systematic breadth, associated traits, and temporal patterns. Botanical Gazette 149: 1–15. [CrossRef]
———, and S. M. Hermann-Parker. 1977 Temporal dioecism: an alternative to dioecism? Evolution 31: 863–866. [CrossRef][ISI]
Darwin, C. 1877 The different forms of flowers on plants of the same species. Murray, London, UK.
Dawson, T. E., and L. C. Bliss. 1989 Patterns of water use and the tissue water relations in the dioecious shrub Salix arctica: the physiological basis for habitat partitioning between the sexes. Oecologia 79: 332–343. [CrossRef][ISI]
———, and J. R. Ehleringer. 1993 Gender-specific physiology, carbon isotope discrimination, and habitat distribution in boxelder, Acer negundo. Ecology 74: 798–815.
———, and M. A. Geber. 1999 Sexual dimorphism in physiology and morphology. In M. A. Geber, T. E. Dawson, and L. F. Delph [eds.], Gender dimorphism in flowering plants, 175–215. Springer-Verlag, New York, New York, USA.
de Jong, P. C. 1976 Flowering and sex expression in Acer L. A biosystematic study. Mededelingen Landbouwhogeschool Wageningen 76-2: 1–201.
Delph, L. F. 1990 Sex-differential resource allocation patterns in the subdioecious shrub Hebe subalpina. Ecology 71: 1342–1351.
Dommée, B., A. Biascamano, N. Denelle, J.-L. Bompar, and J. D. Thompson. 1995 Sexual tetramorphism in Thymelaea hirsuta (Thymelaeaceae): morph ratios in open-pollinated progeny. American Journal of Botany 82: 734–740. [CrossRef][ISI]
———, J.-L. Bompar, and N. Denelle. 1990 Sexual tetramorphism in Thymelaea hirsuta (Thymelaeaceae): evidence of the pathway from heterodichogamy to dioecy at the interspecific level. American Journal of Botany 77: 1449–1462. [CrossRef][ISI]
El-Keblawy, A., J. Lovett Doust, and L. Lovett Doust. 1996 Gender variation and the evolution of dioecy in Thymelaea hirsuta (Thymelaeaceae). Canadian Journal of Botany 74: 1596–1601.
———, ———, ———, and D. H. Shaltout. 1995 Labile sex expression and dynamics of gender in Thymelaea hirsuta. Ecoscience 2: 55–66.
Faegri, K., and L. van der Pijl. 1979 The principles of pollination ecology, 3rd ed. Pergamon Press, Oxford, UK.
Fox, J. F., and A. T. Harrison. 1981 Habitat assortment of sexes and water balance in a dioecious grass. Oecologia 49: 233–235. [CrossRef][ISI]
Freeman, D. C., K. T. Harper, and E. L. Charnov. 1980 Sex change in plants: old and new observations and new hypotheses. Oecologia 47: 222–232. [CrossRef][ISI]
———, L. G. Klikoff, and K. T. Harper. 1976 Differential resource utilization by the sexes of dioecious plants. Science 193: 597–599.
———, J. Lovett Doust, A. El-Keblawy, K. Miglia, and E. D. McArthur. 1997 Sexual specialization and inbreeding avoidance in the evolution of dioecy. Botanical Review 63: 65–92.
———, and E. D. McArthur. 1982 A comparison of twig water stress between males and females of six species of desert shrubs. Forest Science 28: 304–308.
———, ———, and K. T. Harper. 1984 The adaptive significance of sexual lability in plants using Atriplex canescens as a principal example. Annals of the Missouri Botanical Garden 71: 265–277. [CrossRef][ISI]
———, ———, S. C. Sanderson, and A. R. Tiedemann. 1993 Influence of topography on male and female fitness components of Atriplex canescens. Oecologia 93: 538–547.
———, and J. J. Vitale. 1985 The influence of environment on the sex ratio and fitness of spinach. Botanical Gazette 146: 137–142. [CrossRef][ISI]
Galil, J., and M. Zeroni. 1967 On the pollination of Zizyphus spina-Christi (L.) Willd. in Israel. Israel Journal of Botany 16: 71–77.
Geber, M. A. 1999 Theories of the evolution of sexual dimorphism. In M. A. Geber, T. E. Dawson, and L. F. Delph [eds.], Gender dimorphism in flowering plants, 97–122. Springer-Verlag, New York, New York, USA.
Gleeson, S. K. 1982 Heterodichogamy in walnuts: inheritance and stable ratios. Evolution 36: 892–902. [CrossRef][ISI]
Gray, A. 1876 Miscellaneous botanical contributions. Proceedings of the American Academy of Arts and Sciences 11: 101–103.
Kubitzki, K., and H. Kurz. 1984 Synchronized dichogamy and dioecy in neotropical Lauraceae. Plant Systematics and Evolution 147: 253–266.
Lloyd, D. G. 1974 The genetic contributions of individual males and females in dioecious and gynodioecious angiosperms. Heredity 32: 45–51. [ISI]
———. 1975 Breeding systems in Cotula. III. Dioecious populations. New Phytologist 74: 109–123. [CrossRef][ISI]
———. 1979 Evolution towards dioecy in heterostylous populations. Plant Systematics and Evolution 131: 71–80. [CrossRef][ISI]
———. 1980 The distribution of gender in four angiosperm species illustrating two evolutionary pathways to dioecy. Evolution 34: 123–134. [CrossRef][ISI]
———, and C. J. Webb. 1986 The avoidance of interference between the presentation of pollen and stigmas in angiosperms I. Dichogamy. New Zealand Journal of Botany 24: 135–162. [ISI]
Mazer, S. J., and C. T. Schick. 1991 Constancy of population parameters for life-history and floral traits in Raphanus sativus L. II. Effects of planting density on phenotpye and heritability estimates. Evolution 45: 1888–1907. [CrossRef][ISI]
McArthur, E. D. 1977 Environmentally induced changes of sex expression in Atriplex canescens. Heredity 38: 97–103.
———, D. C. Freeman, L. S. Luckinbil, S. C. Sanderson, and G. L. Noller. 1992 Are trioecy and sexual lability in Atriplex canescens genetically based? Evidence from clonal studies. Evolution 46: 1708–1721. [CrossRef][ISI]
Miglia, K. J., and D. C. Freeman. 1996 The effect of delayed pollination on stigma length, sex expression, and progeny sex ratio in spinach, Spinacia oleracea (Chenopodiaceae). American Journal of Botany 83: 326–332. [CrossRef][ISI]
Muenchow, G., and M. Grebus. 1989 The evolution of dioecy from distyly: reevaluation of the hypothesis of the loss of long-tongued pollinators. American Naturalist 133: 149–156. [CrossRef][ISI]
National Oceanic and Atmospheric Administration (NOAA). 1985, 1986 Climatological Data, Utah, Annual Summary. U.S. Department of Commerce, Asheville, North Carolina, USA.
Onyekwelu, S. S., and J. L. Harper. 1979 Sex ratio and niche differentiation in spinach (Spinacia oleracea L.). Nature 282: 609–611. [CrossRef]
Ornduff, R. 1966 The origins of dioecism from heterostyly in Nymphoides (Menyanthaceae). Evolution 20: 309–314. [CrossRef][ISI]
Parrish, J. A. D., and F. A. Bazzaz. 1982 Niche responses of early and late successional tree seedlings on three resource gradients. Memoirs of the Torrey Botanical Club 109: 451–456. [CrossRef]
Pendleton, R. L. 1986 Studies in plant population biology: Grayia brandegei and Quercus gambelii. Ph.D. dissertation, Wayne State University, Detroit, Michigan, USA.
———, E. D. McArthur, D. C. Freeman, and A. C. Blauer. 1988 Heterodichogamy in Grayia brandegei: report from a new family. American Journal of Botany 75: 267–274. [CrossRef][ISI]
Putwain, P. P., and J. L. Harper. 1972 Studies in the dynamics of plant populations. V. Mechanisms governing the sex ratio in Rumex acetosa and R. acetosella. Journal of Ecology 60: 113–129.
Ramadan, A. A., A. El-Keblawy, K. H. Shaltout, and J. Lovett-Doust. 1994 Sexual polymorphism, growth, and reproductive effort in Egyptian Thymelaea hirsuta (Thymelaeaceae). American Journal of Botany 81: 847–857. [CrossRef][ISI]
Rice, W. R. 1989 Analyzing tables of statistical tests. Evolution 43: 223–225. [CrossRef][ISI]
Rogstad, S. H. 1994 The biosystematics and evolution of the Polyalthia hypoleuca species complex (Annonaceae) of Malesia. III. Floral ontogeny and breeding systems. American Journal of Botany 81: 145–154. [CrossRef][ISI]
Ross, M. D. 1978 The evolution of gynodioecy and subdioecy. Evolution 32: 174–188. [CrossRef][ISI]
———. 1980 The evolution and decay of overdominance during the evolution of gynodioecy, subdioecy, and dioecy. American Naturalist 116: 607–620. [CrossRef][ISI]
———. 1982 Five evolutionary pathways to subdioecy. American Naturalist 119: 297–318. [CrossRef][ISI]
SAS. 1989 SAS/STAT user's guide, version 6, 4th ed. SAS Institute Inc., Cary, North Carolina.
Schuster, C. E. 1924 Filberts. Oregon Agricultural Experiment Station Bulletin 208: 1–39.
Shaltout, K. H., and A. A. El-Keblawy. 1992 Sex expression in Egyptian Thymelaea hirsuta (Thymelaeaceae) populations. Plant Systematics and Evolution 181: 133–141. [CrossRef][ISI]
Stephenson, A. G. 1981 Flower and fruit abortion: proximate causes and ultimate functions. Annual Review of Ecology and Systematics 12: 253–279.
Stout, A. B. 1928 Dichogamy in flowering plants. Bulletin of the Torrey Botanical Club 55: 141–153. [CrossRef]
Stutz, H. C., S. C. Sanderson, E. D. McArthur, and G. Chu. 1987 Chromosome races of Grayia brandegei (Chenopodiaceae). Madroño 34: 142–149.
Thomas, S. C., and J. V. LaFrankie. 1993 Sex, size, and interyear variation in flowering among dioecious trees of the Malayan rain forest. Ecology 74: 1529–1537. [CrossRef][ISI]
Thomson, J. D., and S. C. H. Barrett. 1981 Temporal variation of gender in Aralia hispida Vent. (Araliaceae). Evolution 35: 1094–1107. [CrossRef][ISI]
Vitale, J. J., and D. C. Freeman. 1986 Partial niche separation in Spinacia oleracea L.: an examination of reproductive allocation. Evolution 40: 426–430. [CrossRef][ISI]
———, ———, L. A. Merlotti, and M. D'Alessandro. 1987 Patterns of biomass allocation in Spinacia oleracea (Chenopodiaceae) across a salinity gradient: evidence for niche separation. American Journal of Botany 74: 1049–1054. [CrossRef][ISI]
Wachocki, B. A. 1992 Maternal effects on sex ratio and sex expression in spinach. Ph.D. dissertation, Wayne State University, Detroit, Michigan, USA.
Webb, C. J. 1979 Breeding systems and the evolution of dioecy in New Zealand Apioid Umbelliferae. Evolution 33: 662–672. [CrossRef][ISI]
———. 1999 Empirical studies: evolution and maintenance of dimorphic breeding systems. In M. A. Geber, T. E. Dawson, and L. F. Delph [eds.], Gender dimorphism in flowering plants, 61–95. Springer-Verlag, New York, New York, USA.
Welsh, S. L. 1984 Utah flora: Chenopodiaceae. Great Basin Naturalist 44: 183–209.
———, N. D. Atwood, S. Goodrich, and L. C. Higgins. 1993 A Utah flora, 2nd ed. Brigham Young University, Provo, Utah, USA.
West, N. E. 1983a Great Basin-Colorado Plateau sagebrush semi-desert. In N. E. West [ed.], Ecosystems of the world, vol. 5, 331–349. Elsevier Scientific Publishing Company, New York, New York, USA.
———. 1983b Overview of North American temperate deserts and semi-deserts. In N. E. West [ed.], Ecosystems of the world, vol. 5, 321–330. Elsevier Scientific Publishing Company, New York, New York, USA.
———. 1983c Intermountain salt-desert shrubland. In N. E. West [ed.], Ecosystems of the world, vol. 5, 375–397. Elsevier Scientific Publishing Company, New York, New York, USA.
Wood, M. N. 1934 Pollination and blooming habits of the Persian walnut in California. U.S. Department of Agriculture, Technical Bulletin 387.
Wyatt, R. 1983 Plant-pollinator interactions and the evolution of breeding systems. In L. Real [ed.], Pollination biology, 51–95. Academic Press, Orlando, Florida, USA.
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x), expressed as average femaleness of protogynous and protandrous plants for the 1985 and 1986 seasons. Values were calculated both assuming negligible illegitimate fertilization and using illegitimate fertilization frequency estimates of 4.9% for protandrous plants and 14.2% for protogynous plants (in parentheses). 
x is the average number of either ovules or seeds produced per plant